Witzany G. Uniform categorization of biocommunication in bacteria, fungi and plants. World J Biol Chem 2010; 1(5): 160-180
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Dr. Guenther Witzany, Telos-Philosophische Praxis, Vogelsangstrasse 18c, A-5111-Buermoos, Austria. email@example.com
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Uniform categorization of biocommunication in bacteria, fungi and plants
Guenther Witzany, Telos-Philosophische Praxis, Vogelsangstrasse 18c, A-5111-Buermoos, Austria
ORCID number: $[AuthorORCIDs]
Author contributions: Witzany G was responsible for all aspects of the study and manuscript preparation.
Correspondence to: Dr. Guenther Witzany, Telos-Philosophische Praxis, Vogelsangstrasse 18c, A-5111-Buermoos, Austria. firstname.lastname@example.org
Telephone: +43-6274-6805 Fax: +43-6274-6805
Received: March 17, 2010 Revised: May 11, 2010 Accepted: May 18, 2010 Published online: May 28, 2010
This article describes a coherent biocommunication categorization for the kingdoms of bacteria, fungi and plants. The investigation further shows that, besides biotic sign use in trans-, inter- and intraorganismic communication processes, a common trait is interpretation of abiotic influences as indicators to generate an appropriate adaptive behaviour. Far from being mechanistic interactions, communication processes within organisms and between organisms are sign-mediated interactions. Sign-mediated interactions are the precondition for every cooperation and coordination between at least two biological agents such as cells, tissues, organs and organisms. Signs of biocommunicative processes are chemical molecules in most cases. The signs that are used in a great variety of signaling processes follow syntactic (combinatorial), pragmatic (context-dependent) and semantic (content-specific) rules. These three levels of semiotic rules are helpful tools to investigate communication processes throughout all organismic kingdoms. It is not the aim to present the latest empirical data concerning communication in these three kingdoms but to present a unifying perspective that is able to interconnect transdisciplinary research on bacteria, fungi and plants.
Citation: Witzany G. Uniform categorization of biocommunication in bacteria, fungi and plants. World J Biol Chem 2010; 1(5): 160-180
Until the last decade of the 20th century, the interactions within and between organisms have been investigated in a great variety of biological disciplines under the assumption of a rather mechanistic stimulus-reaction pattern, which in principle can be reconstructed by quantifiable and formalizable procedures expressed in terms like “machinery”, “apparatus” and “mechanism”. In the last decade, it has become undoubtedly clear that organisms interact by using signals as signs according to combinatorial rules (syntax), contextual rules (pragmatic) and content-specific rules (semantic) that cannot be reduced to one another but are crucial for successful communication processes.
In this article, the organization and coordination of common behaviour are shown to depend on successful communication. If one level of rules is deformed, damaged or incomplete, either by the transmitting or the receiving organism, or interferences within the information transmitter-medium, communication may fail with even fatal consequences for the organisms. At first it seemed that communication processes were limited to simple signal exchange, however, we have become aware that this is the exception and from bacterial communication processes up to fungi and plants different levels of rule-governed sign-mediated interactions must function in a parallel and in a continuous way. This includes the often mixed use of different signalling levels in gaseous, aqueus, cristalysed or even tactile types. This means that behavioural patterns may act as signs.
In a first step, this article will show some examples of biocommunicative processes; i.e. sign-mediated interactions within and between bacteria-, fungi- and plant-organisms which are governed by semiotic rules on three levels (syntax, pragmatics and semantics). Syntactic rules regulate the combinatorial patterns of signs, pragmatic rules determine the (situational) context in which sign-using agents are interwoven and semantic rules determine the content specifity; i.e. the meaning function which is transported by the signs. Overall, we must keep in mind that in life processes there are always sign-using individuals that generate, combine and recombine signs in communicative interactions. Therefore, communication processes are rule-governed sign-mediated interactions between cellular components, cells, tissues, organs and organisms (Figure 1).
Figure 1 Levels of biocommunicative competences of bacteria, fungi and plants.
Communication processes occur within organisms (intraorganismic). Signals from the Mitwelt (biotic) or inputs from the Umwelt (abiotic) are received by sensory organs and lead to sensory centers in the organism where appropriate behaviour is generated after internal interpretation according available background experiences; i.e. memory. This functions in a parallel way for both intercellular (between cells) and intracellular (within cells) communication. von Uexküll termed intraorganismic sign-mediated interactions endosemioses. Communication processes occur between the same or related species of organisms that share a species-specific repertoire of rules and signs (interorganismic).
Interestingly, we find communication processes also between non-related species (transorganismic); symbiotic interactions would not be possible without them. Therefore, we recognize that only 20% of the cells in a human body are originally human and 80% are from symbiotic settlers.
BIOCOMMUNICATION OF BACTERIA
Bacteria (prokaryotes) communicate and are therefore able to organize and coordinate their behaviour similarly to a multicellular organism. Communication processes are rule-governed, sign-mediated interactions. Signs are, in most cases, chemical molecules (in some cases also tactile interactions) that serve as signals both within and between prokaryotic organisms. Bacteria are symbiotic organisms whole ranging from mutualism to parasitism. They may be beneficial for their (eukaryotic) hosts and without them hosts could not survive. Others are neutral; i.e. do not harm the host, and many of them also cause diseases, sometimes with an epidemic character and often lethal consequences. Bacteria are important hosts for multi-viral colonization and a virally determined order of nucleic acid sequences.
Communicative competences of bacteria
Although bacteria are relatively simple organisms, they represent one of the main success stories of evolution (Table 1). They started at the beginning of life on earth, similarly to archaea, which represent a different organismic kingdom. Bacteria are found in all ecological niches, share a common flux of their gene-pool with a high rate of gene order recombination for adaptive purposes and exist in great diversity. It is common to speak about the languages of bacteria more than in any other organismic kingdom[7-10].
Table 1 Evolutionary chronology of the 5 organismic kingdoms.
Million of years ago
Ribozymatic pre-cellular agents
Prokaryotic microfossils (bacteria, archaea)
Protoctist fossils (unicellular eukaryotes)
Quorum sensing is the term for sign-mediated interactions in which chemical molecules are produced and secreted by bacteria[11-13]. They are recognized by the bacterial community and, dependent on a critical concentration and in a special ratio, control the population density. These molecules trigger the expression of a great variety of gene transcriptions. Many bacteria use multiple quorum sensing codes and each may be modulated by posttranscriptional or other regulatory engineering.
There are also communication processes between different species of bacteria and between bacteria and non-bacterial life, such as eukaryotic hosts. Beneath the semiochemicals (Greek: Semeion = sign) necessary for developmental processes, such as division, sporulation, and synthesis of secondary metabolites, there are physical contact-mediated behavioural patterns important in biofilm organization[17-20]. Also, abiotic influences serve as signals for specific nutrients or other environmental circumstances like hydrodynamic changes.
Because communities of bacteria species that are able to coordinate their behaviour have advantages against single bacteria organisms, evolutionary drive went into rising communicative complexity[21,22]. We should not forget that in comparison to the first 2 billion years of life on earth with closed prokaryotic symbiology, the rise and growth of the eukaryotic superkingdom (protoctists, animals, fungi, plants) was a crucial advantage for bacteria colonize vertical hosts with their great spatial and motility resources.
We can differentiate three classes of signalling molecules used for different purposes; i.e. signalling within the organism to coordinate gene expressions to generate adequate response behaviours, signalling between the same or related species and signalling among different species. With a limited number of molecules and a limited number of combinatorial rules, bacteria generate many different sign mediated interactions for different purposes.
As in every sign-mediated interaction, sign-users share a common set of syntactic rules; i.e. how signs may be combined using pragmatic rules for a variety of interactional contexts (e.g. development, growth, mating, virulence, attack and defense). The situational context of these complex interactions determines the meaning of the signs; i.e. semantics of signals. In principle, we can identify in every sign-mediated interaction within and between organisms the complementarity of these three levels of semiotic rules. This leads to the generation of intra- and intercellular processes that enable bacterial communities to generate memory, which may be inheritable but can be altered epigenetically; i.e. different reading/meaning patterns of the same genetic dataset with differences on the phenotypic level.
Interpretation and coordination
Bacteria have profound deleterious effects on human health, agriculture, industry and other ecospheres. Therefore, multiple drugs have been created to fight them. Bacteria can develop drug resistance, for instance, by coordination of special defense behaviours called biofilm organization. Biofilm organization is a special kind of coordination with high density of physical contact and contact specific signalling. If bacteria realize a critical mass via quorum sensing they organize a high density communal body by moving their flagellas, which may resist even strong antibiotics. Biofilms are constructed on both abiotic as well as biotic surfaces; e.g. on stones in rivers and other aqueous surfaces or in the respiratory tract of animals. Nutrient availability also regulates the structure of biofilm organization as hydrodynamic forces. Interestingly, biofilm organisation has been linked with coordinated DNA release, which is integrated in the biofilm.
Semiochemical vocabulary of bacteria
The semiochemical vocabulary used by bacteria is diverse, especially because some signaling molecules are re-usable components. Acyl homoserine lactones and linear oligopeptides are used as signs in diverse processes. Cyclized oligopeptides can function in virulence. γ-Butyrolactones are used as antibiotics and in sporulation processes. Furanosyl diester (AI-2) is used in diverse processes and in luminescence. Cis-11-methyl-2-dodecenoic acid (DSF) serves in virulence and pigmentation. 4-Hydroxy-2-alkyl quinolines (PQS, HAQs) are important in regulation processes and for virulence as are palmic acid methyl esters. Putrescine is important in swarming motility such as biofilm organisation. A-signal is used in early developmental processes and aggregation C-signal is a cell surface-associated protein that serves to coordinate motility. The developmental process of fruiting body building cyclic dipeptide is a secondary metabolite.
Gram-negative bacteria use homoserine lactones (LuxR/LuxI) as signs in communication processes, whereas gram-positive bacteria use oligopeptides in quorum sensing communication. As in all organisms, non-coding RNAs are important in higher order regulatory pathways. Small RNAs and microRNAs are used by bacteria to regulate special genetic expression patterns that play an important role in appropriate response behaviour to stress or nutrient availability; e.g. in controlling the quorum sensing pathways.
Today, three kinds of communicative goals are distinguished: (1) reciprocal communication; active sign-mediated interactions that are beneficial for both interacting parts; (2) messages that are produced as responses to a triggering event, which may be an indicator to a receiver that was not especially targeted by the producer. A coincidental event that is neutral, except for the energy costs of production, to the producer but beneficial to the receiver; and (3) signalling to manipulate the receiver; i.e. to cause a response behaviour that is beneficial to the producer and harms the receiver, which is often against their normal goals.
The three classes of intra-, inter- and transorganismic communication enable bacteria to generate and coordinate different behavioural patterns: self and non-self identification (i.e. “recognition” and identification of other colonies and measurement of their size, and pheromone based courtship for mating), alteration of colony structure in formation of fruiting bodies, initiation of developmental and growth processes (e.g. sporulation).
In receiving signals from the same or related species, or non-bacterial organisms, the signalling molecules bind to specialized sensor proteins that function as receptors. They transmit the message to intracellular regulators[32,37]; i.e. the signal molecule transits the cell membrane through diffusion or by specific transport pathways. Inside the cell, the signalling molecule, in most cases, binds to a cytoplasmic target protein. A diffusible molecule may be chemically engineered to an active signal after entering the target cell and production of response molecules leads to signal-dependent transcription control of DNA.
Bacteria must distinguish between species-specific signalling, and signalling that is able to modulate behaviours interspecifically. With these communicative competences, they are able to coordinate species-specific behavorial patterns as well as coordinating behaviours among diverse species.
Transorganismic communication of bacteria
Starting with beneficial symbioses between bacteria and plants, we will consider the complex communication networks between soil bacteria, mychorrizal fungi and plant roots. Mychorrizal fungi secret molecules into the surrounding environment that serve as nutrients for soil bacteria and trigger their activation to degrade special nutrients, which are then available for mychorrizal fungi. Their hyphal growth serves as developmental and growth stimulation of plant roots, which are dependent on nutrients that are prepared by the mychorrizal fungi. Plant roots can also mimic bacterial signalling molecules, either by triggering bacterial production of special molecules or by disturbing bacterial communication pathways[14,34,35,38].
Rhizobia bacteria are integrated into plant cells by phagocytosis when they interact symbiotically with plant roots. In other cases where rhizobia fail to fix nitrogen inside the root nodules because they are “cheating”, plants sanction these rhizobia and prevent their spread in order to stabilize mutualistic symbioses with bacterial colonies. Different kinds of root exudates regulate plant and microbial communities in the rhizosphere. This is necessary to maintain equilibrium and inhibit the continuity of attacks by pathogenic bacteria in the soil[41,42]. The full range of trans-specific communication processes between bacteria and plant roots are important for developmental and growth processes in the entire plant kingdom[12,43].
Chemical molecules that serve as signs in intercellular communication processes of bacteria are similar to pheromones in social insects and animals. This may be an indicator of evolutionary lineages that evolved in the bacterial “chatter”.
Marine eukaryotes are able to mimic bacterial quorum sensing to inhibit successful bacterial communication. Interbacterial communications use hormone-like signalling to sense specific host locations such as an intestinal habitat. In this specialized ecosphere, a bacteria-host communication occurs, which means the host cells and bacterial cells share a common function based on the same signalling molecules.
Living as endosymbionts and as potential candidates for symbiogenesis[47-50], as documented in the origin of eukaryotic endosomes like mitochondria and chloroplasts, indicates the important roles of bacteria for the entire history of evolution. The interactions may be pericellular colonization events but also are an intracellular lifestyle. These different symbiotic interactions range from acquisition of novel genetic material to reduction in size and content connected with gene loss. Successful living processes of higher eukaryotes would not be possible without beneficial symbiosis with bacteria. As mentioned in the introduction, the cell mass of an adult human is 20% of human origin and up to 80% of exogenic settlers, most of which are bacteria.
Interorganismic communication of bacteria
For a long time it was assumed that bacteria live predominantly as monads. Meanwhile, it has been recognized that this is a very rare exception[52,53]. Bacterial colonies live, in nearly all cases, in coexistence with other bacterial species self-coordinated by a diversity of sign-mediated interactions[54,55]. Bacteria use intraspecific and interspecific signalling in all ecological in vivo situations. This also implies a broad variety of conflicts within and between species. The mutual, neutral and manipulative aims of communication processes are special kinds of response behaviours to certain degrees of beneficial, neutral and conflictual relationships.
Dependent on the availability of nutrients, some bacteria suppress normal cell development, which leads to the development of a different cell type that is better suited for adequate response behaviour in the situational context. Therefore, different environmental conditions can lead to different gene expressions within the same genomic dataset. If the same colony is exposed several times to these changing contexts, it has been shown that they react more immediately. This indicates that bacterial communities are able to develop memory and learn from their experiences[10,54]. These functions are similar to neuronal networks in higher eukaryotes. In the case of changing environmental conditions, the suppression of cell division may lead to cell elongation, which enables the cell colony to change the modus of motility. This is an important feature of socio-bacterial behaviour; e.g. swarming coordination and organization for surface colonization[57,58].
Some authors documented altruistic strategies in mixed colony formations, which seems to be an advantage for mixing among microcolonies. Altruistic behavioural strategies enable strengthening of self-identity and assist with sustainable equilibrium in multilevel colonized ecological niches[59,60].
Interestingly, bacteria use a common contextual interpretation for incoming signals by each member of the colony. The response behaviour is appropriate to the “majority vote” in the context dependent decision.
The identification of non-self species is a competence that is possible through species-specific and group-specific quorum sensing and is coherent with the assumption that smaller groups of the same bacterial species are able to build types of quorum sensing “dialects”. These are important in the high density coexistent bacterial life habitats to prevent confusion and enable more complex coordination. Interestingly, the prokaryotic cell-cell communication has structural analogues to cross-kingdom signalling between bacteria and fungi.
In special cases, bacteria decide to form fruiting bodies of different types and shapes for sporulation. This enables bacterial communities to produce a more efficient dissemination of the spores. The fruiting body construction is governed by pragmatic rules with different coordinating roles for different sub-groups of bacterial communities. Some serve motility density, followed by the direction decision and decisions on cell types, cell growth and developmental stages during all steps until the fruiting body is ready for sporulation.
Without a communicative hierarchical organization this would not be possible. If communication is disturbed, body building is not insured, and so bacterial communities have developed special strategies to single out so called cheaters who don’t follow the rules of coordination.
One of the most interesting and best investigated phenomena of bacterial communication is the symbiology of multiple colonies coexisting in the human oral cavity[64-66]. Bacteria on human teeth and oral mucosa establish a homeostasis of pathogenic and mutualistic bacteria by a complex system of sign-mediated interactions, both species-specific and trans-specific. The dental plaque in the oral cavity of humans is a unique habitat that is not found in any other species. The homeostasis is not static but the result of a dynamic relationship between different species-colonies dependent on intervals of daily hygiene. About 500 species interact in this community[67-69]. Each member of the community must be capable of self and non-self distinction, and to distinguish between species-specific signalling and trans-specific signalling, or even “noise” (no biotic content). As a community, they must be able to measure their own colony size and the size of the other colonies and identify molecules that have the same chemical structure but are not part of a biotic message[64,65].
Special communication patterns with detailed hierarchical steps of signal production and transmission include: (1) metabolite exchange; (2) cell-cell recognition; (3) genetic exchange; and (4) host signal recognition and signal recognition of the same or related species. Because of the high number of competing and cooperating species, both short- and long-term community architectures are established. If communication on the intra-, inter- and meta-organismic level is successful; i.e. the signal transmission and reception enables colonies to live in a dynamic homeostasis, then the human oral cavity will not have cavity diseases.
Intraorganismic communication of bacteria
Interestingly, prokaryotic gene order is not as conserved as protein sequences. Only some higher order regulations (operons) that code for physically interacting proteins are found in almost all bacterial (and archaeal) genomes. However, eukaryotic organisms (and a few archaea), where the protein vocabulary underlies higher order regulatory functions encoded in the non-coding DNA, lack such gene order conservation.
This indicates a high dynamic of new gene orders, as documented in the horizontal gene transfer events with intensive intragenomic recombination[70,71]. This exchange of whole genes or gene-blocks enables bacteria to combine several phenotypes. The transformation process includes the release of naked DNA, followed by uptake and recombination; i.e. integration, with 17 steps currently identified. Therefore, we can recognize the diverse outcomes of mobile DNA-contents, which is not a mass of individualized genetic texts, but a bacterial gene pool as text repertoire that is available for each individual bacteria and is the resource for bacterial genome innovation and evolution. Horizontal gene transfer is a main resource for integrating newly evolved genes into existing genomes and does not need slow steps of chance mutations to alter the genomes, but accelerates genome innovations in both bacteria and archaea[75-77]. Important in this context of genomic innovation is not only sequence acquisition but the contextualization, including sequence loss. The phylogeny of microbial species is not a tree of life, but an evolutionary network or a ring of life, mediated by genetic exchange; i.e. acquisition and loss of genetic data-sets[79,80].
Intracellular communication: Signal-dependent transcription regulation of DNA serves a great variety of response behaviours. One of the most interesting phenomena is the fact that, in the earliest 2 billion years of life on earth, the immense density of bacterial life was not an event of individual organisms but their commonly shared gene-pool, which was in constant flux through horizontal gene transfer. This means that the evolution of bacteria was not a random event of chance mutations and their selection, but transfer of whole genes and gene-blocks assicated with real phenotypes. This leads to different combinatorial patterns of genetic encoded phenotypes and the rise of bacterial diversity. It also enables bacterial pathogens to optimize their disease causing coordination, which is therefore the target of drug developments for medical purposes. New empirical data seems to suggest that the phenomenon of horizontal gene transfer is driven by viral competences inherent to bacterial organisms.
For a long time it has been proposed that tubulin plays an important role in cytoskeletal functions of eukaryotes, whereas prokaryotes lack this system. Recent research has shown that tubulin is a very ancient system for genetic dataset segregation also in bacteria, which plays important roles in filament formation, movement and orientation[83-86].
Bacteria develop, organize and coordinate a great variety of behavioral patterns, which represents one of the most successful life histories of all the organismic kingdoms. Although they have existed for nearly 4 billion years, they still survive, participating in some of the most dramatic changes in evolutionary history, such as DNA evolution, evolution of nearly all protein types, eukaryotic cells, vertical colonization of all eukaryotes, high adaptability through horizontal gene transfer and multi-species colonization of all ecological niches.
Horizontal gene transfer seems to be one of the main forces in bacterial evolution because it is derived from a commonly shared and transferable gene pool where new genetic inventions from a broad variety of sources can be integrated and recombined. Bacteria are the main sources for symbiotic relationships, without which eukaryotes would not have evolved and would not be able to survive. If we agree that biology is a history of symbiology, then bacteria are the driving force.
Recent phylogenetic analyses demonstrate that these competences of bacteria are derived from the capability of viruses to carry out natural genome editing with an astonishing variety of genomic creativity. Bacteria seem to be the optimal biotic matrix for viral induced genetic inventions. The main actors in genetic content arrangements of bacteria are phages, plasmids and related non-lytic but persistent viral settlers. Therefore, the communicative competences of bacteria and the genome editing competences of viruses cannot be separated.
BIOCOMMUNICATION OF FUNGI
The oldest fungal fossils are 450 million years old. The kingdom of fungi emerged approximately 300 million years after the appearance of the first animal species, although they have a common ancestor[82,87,88]. In addition, they share common traits with eukaryotic organisms. In contrast to animals and higher plant life, monocellular representatives are fairly common among fungi; i.e. fungi are by no means mere multicellular eukaryotes. A fact that can be easily and coherently reconstructed through the lineages of Protoctista is that coordinated behavioural patterns are found among single-celled eukaryotes that closely resemble those of single-celled fungi. However, there are unmistakable and significant differences in protoctist structure (flagellated) compared to fungi (non-flagellated). Obviously, fungi have evolved out of the coordinating competence of protoctists, such as red and joch algae.
Different from most animals, fungi are sessile organisms that can live for extremely long periods or extend over large areas. One exemplar has been found that covers as much as 15 hectares with an age structure of approximately 1500 years. Endolithic fungi of the Antarctic are known to be among the most long-lived organisms on this planet.
Most fungi feed on and decompose non-living organic matter. They secrete powerful enzymes that enable the cells to digest organic matter outside of their body in the nearby environment, which in turn is broken down to smaller molecules that can be absorbed and reincorporated in a dissolved form. To deter potential predators, a number of complex and highly efficient deterring substances are produced by fungi.
For 1000s of years, fungal competences have been actively utilized by humans in beer, wine and bread production. Since fungi are very simple organisms, sequencing and technical manipulation are relatively easy, making them ideal organisms for laboratory experiments, such as Neurospora crassa[90,91] or yeasts. Recent research on yeast genomes has demonstrated important features of higher order regulatory functions hidden in their DNA. Studies have shown that DNA encodes its own packaging; i.e. DNA sequences code how to package their own genome in the nucleosomes.
Although fungal infections cause a wide range of diseases, they also serve as important resources for drug production. Their application as producers of various antibiotics is comprehensive and well appreciated.
Semiochemical vocabulary of fungi
Since coordination and organizational processes occur in all organismic kingdoms, fungi are no exception. Such processes occur during the formation of mycelia and fruiting bodies (intraorganismic), between species of the same kind; i.e. relatively closely related species (interorganismic), and between fungi and nonfungal organisms (transorganismic). These processes occur as rule-governed sign-mediated interactions. The signalling processes are nothing less than distinct biosemiotic communication processes. The semiochemicals are of biotic origin and they trigger the fungal organism to react in a specific manner. This means that fungal organisms are able to identify differences among molecules, determine whether they are biotic messages or lack these features.
So far, five different primary signalling molecules are known that serve to coordinate very different behavioural patterns, such as filamentation, mating, growth and pathogenicity[96-100]. Behavioural coordination and the production of such substances can only be achieved through interpretation processes: self or non-self, abiotic indicator, biotic message from similar, related, or non-related species, or even “noise”; i.e. similar molecules without interpretational content. Furthermore, there are numerous, lesser-investigated subunits that play an accompanying role as they are weaker in effect. Globally, these semiochemicals serve to coordinate similar goals in different fungal species, yet species variation among them cannot be ignored. These patterns include: (1) cell integrity, cell wall construction, pheromone/mating and osmo-regulation by mitogen activated protein kinase (MAPK) signalling; (2) fungal development and virulence by the cyclic adenosine monophosphate cAMP/PKA system; (3) cross-talk between signalling cascades by the RAS protein; (4) cell survival under oxidative stress, high temperature, membrane/cell wall perturbation by calcium-calmodulin-calcineurin; and (5) control of cell growth and proliferation by rapamycin.
Until now, 400 different secondary metabolites have been documented. These are known to contain mycotoxins and are used both for defensive and aggressive behavioural patterns.
Interpretation of abiotic information
Fungi react sensitively to varying nutrient availability and nutrient fluxes, responding by initial intraorganismic communication. That is, in the case of carbon or nitrogen insufficiencies, the internal communication of the organism responds adequately and is phenotypically expressed by a change in hyphal growth. Until now, two specific signalling pathways have been found that coordinate such behaviour. These diverging patterns have also been documented among other fungi, including those that are pathogenic to plant and animal life.
As in animals and plants, seasonality as a part of the circadian system is also found in fungi[91,102]. In particular, there are light regulated physiologic processes that coordinate the internal fungal clock.
Almost all fungi digest food outside their bodies. The excretion of extracellular digestive enzymes fragments larger biomolecules and makes them soluble, which are then readily accessible for the fungal organism. This is particularly important for the digestion of cellulose (through the enzymatic activity of exocellulase and endocellulase, and lignin; i.e. lignin peroxidase and manganese peroxidase). Enzymatic breakdown of organic matter yields simple sugars, amino acids, fatty acids and other smaller molecular components.
Transorganismic communication of fungi
One of the most striking trans-kingdom communication processes among fungi and non-fungal species can be found in lichens. Fairly early associates of the fungal kingdom are those organisms that interact symbiotically with fungi, as is the case with lichens. All higher fungal life forms originated from these symbiotic ways of life, which later became independent by detaching themselves from this close and vital dependence. Lichens are complementary symbiotic partnerships between photobionts (algae or bacteria with fungi); i.e. they are only viable together. As pioneering organisms, they may settle on blank rock. Being essential bioeroders, they extract nutrients from mineral matter, thereby initiating the process of soil formation and paving the way for successive organisms that include even root-forming species.
Lichens are polyphyletic. They have been derived many times independently from different kinds of ascomycetes, so undoubtedly, their nature of symbiosis varies. In lichens, the algae provides the fungi with photosynthate, while the fungi caters to the algae with nutrients. Lichens constitute one of the oldest known fungal members and are capable of resisting quite adverse environmental conditions. The symbiosis between fungi and algae or fungi and bacteria results in a mutual supply of nutrients and their associated competences. Through quorum sensing, the fungi benefit from the bacterial association. In turn, the bacteria utilize dissolved fungal metabolites to satisfy their nutritional requirements. A similar co-dependence is observed with algae as symbiotic partners.
Fungi are known to utilize a broad variety of different symbiotic interactions with animals, plants and eukaryotic unicellular organisms for both mutual benefit as well as parasitic and even lethal associations. They also settle on specific types of tissue. Fungal diseases are known to affect both plant and animal life where they can induce devastating effects on agriculture. A typical example of mutually beneficial symbiosis can be found between the bark beetles and quite a few different fungi. The fungal spores benefit from the locomotion provided by the beetles in several aspects: there is access to new hosts, while the beetle benefits by the availability of fungal nutrients and pheromones. Some fungi provide nitrogen, amino acids and sterols, which are crucial for the development of beetle larvae, however, this gives effect only after the adult beetle has colonized a host. Interestingly, many bark beetles even evolved transportation pockets for fungal hyphae, which points to the common evolutionary history.
Another trans-kingdom symbiotic signalling happens between fungi and ants, which derives from a co-evolutionary relationship that lasted for millions of years. Interestingly, some lignin-degrading fungi also produce semiochemicals that have effects on the feeding and foraging behaviour of a Formosan subterranean termite.
Many of the known indicators stress the fact that both the fungal as well as the animal kingdoms share common ancestors, such as protoctists with a true nucleus (e.g. choanoflagellates). Fungi and animals are more related to each other than to the plant kingdom. This is further strengthened by the sign-mediated processes, which regulate cellular functions. Yet, a different indicator of their common ancestor is found in a particular signalling pathway, termed MAPK cascade. It plays a crucial role in cell wall stabilization of fungi and pheromone/mating interaction among mammal cells.
Then, there are fungi that parasitize plants. For example, they colonize host tissues with an intercellular mycelium that forms haustoria fungal mats within plant cells that penetrate the cell to utilize the nutrients of the plant. Investigations of hazardous fungal infections on plants revealed the crucial role of enzymes, such as cutinase, pisatin, demethylase and HC-toxins.
Today, several hundred species of fungi colonize more than 100 000 different plant species. This type of cohabitation requires symbiotic signalling; e.g. the starting of filamentous growth of fungi through plant hormones. Roots of plants provide better conditions for mycorrhizal fungi, which in turn supply plants with better nutrients. For fungus, such a relationship is either balanced or predatory. Endophytic fungi, however, live in plants without triggering symptoms of disease. Today, scientists consider the origin of plant cells to be the result of terrestrial activity of mycorrhiza; i.e. settlement on land is a coevolutionary event that is comparable in the mode of complementarity to that between flowering plants and insects. Thereby fungi excrete digestive enzymes into the surrounding soils, convert nutrients into aqueous solutions that in turn can be readily absorbed by the plant. Therefore, a staggering majority of 80% of all terrestrial plants, especially trees, rely on the activity of mycorrhiza.
Fungi affecting animals are usually dependent on the host’s body temperature; i.e. host colonization by the fungi is possible only if the body temperature is sufficiently high. Especially Aspergillus fumigatus colonizes animal hosts if they are under thermal stress. Although fungal disease is common in birds, the relative resistance of endothermic vertebrates to fungal diseases may be a result of immune responses connected with higher body temperatures.
Interorganismic communication of fungi with same or related species
Since there are both single and multicellular fungal species, determination of communication processes between same species and related fungal species cannot be distinguished unambiguously from intercellular communication (intraorganismic). Thereby communication processes of monocellular yeasts, which resemble those of the amoeba (e.g. Dictyostelium), must be considered as interorganismic communication. Cell-to-cell communication, however, between multicellular fungal species is truly intercellular. To verify whether cell-to-cell communication is inter- or intraorganismic, we have to consider intercellular processes on a case-by-case basis.
Herein is another fundamental characteristic of biota; identification competence is necessary for the determination of “self” and “non-self”. This competence could be successfully proven in Neurospora crassa. It is obvious that this competence to distinguish between oneself and others is vital for fungi; that is, the encounter of mycelia among same species individuals results in the merger of their fungal hyphae. However, such dikaryotic mycelia can also result from the merger of different fungal species. While peripheral hyphae tend to avoid merging with hyphae of other species, the opposite is the case with those at the center of the mycelium[120-122].
If one assigns mycelia the role of a wrapper within which the fungi, so to speak, is enveloped into a fluid-like continuum, the nuclei of compatible but different species are then “flowing” through the same mycelium. The overall result is an organism, that houses nuclei of different genetic origin in its cytoplasm. However, if specific genetic sequences are incompatible, then repulsion sets in, forcing the approaching hyphae to an immune-like response.
Resource competition in fungi occurs directly, indirectly and via mechanical interaction. Indirect competition involves absorption of all available resources within the reach of the mycelium, thereby famishing potential competitors by maintaining a nutritional deficiency gradient. Direct interaction, on the other hand, involves secondary metabolites, which suppress growth or even induce death of the competing fungi. The fungicides employed in such cases can be either volatile or non-volatile. Mechanical interaction simply requires overgrowth of one fungal species by the other, in which the overgrowing species exerts its lytic action on the other. In some cases lysis is induced via antibiotic agents[124,125].
As bacteria are also single-celled, fungi use quorum sensing to regulate and affect biofilm formation and pathogenesis. This is mediated by small molecules that accumulate in the extracellular environment. If it reaches a sufficiently high concentration, a response regulator is activated within the local population of cells leading to the coordination of special gene expression.
In parasitic interactions between fungal organisms, even cytoplasmic fusion during infection processes was found, which indicated genetic transfer in the host parasite relationship. The recognition pattern in this predator-prey relationship is mediated by trisporoids that also serve in a non-parasitic behavioural pattern; i.e. is responsible for sexual communication.
The countless variety of fungal organisms represents a major challenge when establishing a homogeneous designation of the sign processes employed. Research activities so far have predominantly focused on those fungal species that posed a serious threat to agriculture, are pathogenic to humans or possessed antibacterial properties. Species of this kind are relatively well investigated, whereas the large majority of species, which do not have the aforementioned properties, are hardly known.
Intercellular communication: Higher fungi are modular hyphal organisms in that they reproduce by clonation or also parasexually. They establish interlocked networks. Like red algae, they “merge” their cytoplasms to form multi-nucleated cells. A spore germinates under appropriate environmental conditions and is followed by the formation of filaments called hyphae. The latter is characterized by nuclear division and spore formation, which develops into monokaryotic filaments (tip growing). The embryological stage, a characteristic of higher plants and animals, is completely absent in fungi. Hyphae formation is also found among certain bacteria, like Streptomyces and Actinomyces. Hyphae tightly packed together into a mat are called a mycelium. Each filament of hyphae has tubular side walls made mostly of chitin, a feature that is common also in Arthropoda. The cell walls that seem to separate adjacent cells in a filament are called septa; however, their porous nature does not really assign them separating properties. The merger of filamental tips of the same or different species triggers a self/non-self identification process. This process is sign-mediated and results either in repulsion or attraction. If the latter occurs, merger to a dikaryotic mycelium takes place and initiates the formation of a fruiting body. Hyphal growth is a totally different pattern of conduct than normal cell growth: such cells change shape, become long, and reorient themselves into specific directions to come into physical contact or even “merge” with each other, only to colonize a potential growth resource, which is usually dead organic matter. Fungal hyphae simultaneously extend into a given direction only when nutritional resources are ideally distributed. However, this is a rare event. Usually the fungi propagate in conditions rich with organic matter (carbon and its derivatives) just to halt growth when little or no resources are available; here the fungi coordinate their growth by employing certain properties. In order to do so, the fungi use intercellular signals that enable them to comprehend the overall state of the organism. Once the fungus encounters a resource-depleted substrate or even poisonous compounds, it responds by halting its growth cycle or by propagating in another direction.
The protein signals involved in such processes are quite complex; the apex of hyphae houses specialized receptors that are able to respond to any environmental condition. Any carbon-enriched substrate makes these receptors active, which in turn results in the production and release of protein signals into the hyphal cytosol where the corresponding signalling cascade is triggered. In turn, the mycelium responds with the mobilization and translocation of resources into the activated area. In the absence of carbon-rich substrates, or at increasingly acidic pH levels, the hyphae respond by activating yet other receptors that slow down growth and eventually make the organism withdraw resources from the affected area. Since septa within the hyphae are perforated, they perform similar functions as observed with gap junctions in higher animals, micro-plasmodesmata in cyanobacteria or plasmodesmata in higher plants[128,129].
Intracellular communication: By investigating a great number of signal transduction events from the outside through the cell membrane into the cytoplasm, it was possible to decode some important intracellular communication processes. Thereby, it has been found that sign processes coordinate cell polarity, mating, pheromone control and cellular morphology. Some of these sign processes even adjust the cell cycle, perform polarized growth activity and modify the transcription profiles of fungal cells[87,101,130]. By examining the fungal pathogen Paracoccidioides brasiliensis, it has been revealed that some signalling pathways are identical to those of other species, such as in Saccharomyces cerevisiae, Cryptococcus neoformans, Candida albicans and Aspergillus fumigatus.
The involved “protein cascades” that characterize production pathways of appropriate chemicals and messenger signals determine behavioural contexts, which are to some extent completely different, as outlined in the chapter about semiochemical vocabulary. In addition, combinatorial communication procedures such as MAPK and cAMP pathways are also part of the behavioural contexts. This in turn serves to multiply the semantic contents of the encoded messages.
To sense extracellular stimuli and convert them into intracellular signals, which regulate developmental and growth processes, several signalling pathways have been found. The guanine nucleotide-binding protein is essential for extracellular detection of nutrients and sexual partners[131-133]. The TOR protein kinases that are bound and inhibited by rapamycin function as nutrient-sensing signals and regulate cellular responses like proliferation, transcription, translation, autophagy and ribosome biogenesis[134-137].
As with any sign-mediated interaction that can be achieved with molecules, the same components are employed for different behavioural contexts and in various messages. That is, different modes of behaviour can be coordinated by syntactic identical molecules. The signalling pathways use identical proteins to coordinate different response patterns. Even if they are syntactically identical they have completely different meanings. For example, activated cAMP triggers filamentous growth in Sacharomyces cerevisiae, regulates positive virulence in Cryptococcus neoformans, suppresses mating in Schizosacharomyces pombe and inhibits filamentous growth in Ustilago maydis[87,138] or activates protein kinase for directly or indirectly indicated developmental changes in Magnaporthe grisea during infection of rice. Another example is the Ustilago maydis pheromone response, which regulates both cell fusion as well as the pathogenicity program for plant infection[140-142].
These examples show that different behavioural contexts determine different meanings for identical signalling molecules, or in biocommunicative terms, pragmatics determines semantics of syntactic identical substances. In such cases, identical signs induce opposite responses in their associated life-related relationships among different organisms. It is interesting to note that fungi are not just capable of differentiating various messages and responding appropriately, but moreover, they differentiate molecules that are chemically identical from molecules that obviously contain no relevant meaning (“noise”); i.e. they are not parts of biotic messages.
Recent genome comparisons have given new insights into evolutionary aspects of fungi. The thesis that evolution happened through whole genome duplication events, followed by selective gene-loss and stabilization, is strengthened by analysis of Saccharomyces cerevisiae. Interestingly, the signal-to-noise ratio in yeasts is approximately 70% protein coding regions and 15% regulatory elements in non-protein coding regions, in comparison to humans with 3% and 97%, respectively.
The important role of viruses in the evolution of fungi, especially virally induced natural genome editing functions for the evolution of fungal communicative competences, is not part of this paper but is outlined in great detail in a recent publication.
An overview about significant levels of fungal communication shows that identification of sign-mediated processes in signalling pathways are context dependent, both within and among fungal cells as well as between fungi and other organisms. Such dependence is prevalent in either (beneficial or parasitic) colonization or defence responses. Depending on the utilization context, molecular components are integrated into unique signalling pathways where they gain the corresponding meanings. Such meanings are subject to change; i.e. they rely on various behavioural contexts, which differ in altering conditions. These contexts concern cell adhesion, pheromone response, calcium/calmodulin, cell integrity, osmotic growth, stress-response or cell growth through rapamycin. The interactional context (pragmatics) determines the semantic relation; i.e. its meaning and the function of the chemical components, and is found to be a sign-mediated communicational pattern of fungi.
After recognizing how versatile fungal communication competences really are, we can see that a main principle is followed throughout all these signalling processes. With a core set of chemical molecules, fungal organisms coordinate all of their behavioural patterns. The interactional (pragmatic) context and the different modes for coordinating appropriate response behaviors; e.g. in development, growth, mating, attack, defence and virulence, determine combinations of signals to generate the appropriate meaning-function (informational content of messages). In contrast to former systematizations that have been investigating combinatorial rules of meaning and functions in signalling molecules, the biosemiotic perspective differentiates all three levels of rules involved in signalling: the syntactic level (combinations), the pragmatic level (context) and the semantic level (content). These generating processes normally function in a very conservative way but under certain circumstances may fail, or selective pressure may lead to changes that can be a driving force in fungal evolution.
BIOCOMMUNICATION OF PLANTS
Plants are also sessile organisms that actively compete for environmental resources both above and below ground. They assess their surroundings, estimate how much energy they need for particular goals, and then realize the optimum variant. They take measures to control certain environmental resources. They can distinguish between self and non-self. This capability allows them to protect their territory. They process and evaluate information and then modify their behavior accordingly.
Communicative competences of plants
Highly diverse communicative competences of plants are possible due to parallel communication processes in the plant body (intraorganismic), between the same and different species (interorganismic), and between plants and non-plant organisms (transorganismic). Successful communication processes allow the plants to prosper, and unsuccessful ones have negative, potentially lethal repercussions. Intraorganismic communication involves sign-mediated interactions in cells (intracellular) and between cells (intercellular). Intercellular communication processes are crucial in coordinating growth and development, shape and dynamics. Such communication must function on both the local level as well as between widely separated plant parts. This allows plants to react in a differentiated manner to the current developmental status and physiological influences.
As we will see, communicative competence refers to chemical and physical communication processes. Chemical communication is either vesicular trafficking or cell-cell communication via the specifity of plant tissue connections (“plasmodesmata”). Moreover, numerous signal molecules are produced in or controlled by the cell walls. Physical communication takes place through electrical, hydraulic and mechanical signs.
Semiochemical vocabulary of plants
The chemical communication in and between plants is so complex that more than 20 different groups of molecules with communicatory function have currently been identified. Up to 100 000 different substances, known as secondary metabolites, are active in the root zone, for example. This diversity is necessary considering the high diversity of microbes, insects and plants in this zone. For example, the continuous defence against pathogenic microorganisms in the root zone requires the constant production, exact dosage and secretion of phytoalexins, defence proteins and other substances. Examples of the molecular vocabulary in plant communication include a broad variety. Major substances are auxin, several phytohormones, RNAs and multiply-reusable components.
Auxin: Plant roots and plant shoots (stems) detect environmental signals as well as development levels, and communicate over long-distance pathways. The decentralized neuronal-like signaling of plants is advantageous for decentral growth and development under constantly changing environmental conditions. Auxin is used in hormonal, morphogenic and transmitter signalling pathways. Because the context of use can be very complex and highly diverse, identifying the momentary usage is extremely difficult. For synaptic neuronal-like cell-cell communication, plants use neurotransmitter-like auxin and presumably also neurotransmitters such as glutamate, glycine, histamine, acetylcholine, dopamine, all of which they also produce. Auxin is detected as an extracellular signal at the plant synapse in order to react to light and gravity. However, it also serves as an extracellular messenger substance to send electrical signals and functions as a synchronization signal for cell division. In intracellular signalling, auxin serves in organogenesis, cell development and differentiation. In the organogenesis of roots, for example, auxin enables cells to determine their position and their identity. The cell wall and the organelles it contains help regulate the signal molecules. Auxin is, as the name suggests, a growth hormone. Intracellularly, it mediates in cell division and cell elongation. At the intercellular, whole plant level, it supports cell division in the cambium, and at the tissue level it promotes the maturation of vascular tissue during embryonic development, organ growth as well as tropic responses and apical dominance.
Phytohormones: Alongside the classical phytohormones auxin, cytokinin, gibberellin, ethylene and abscisic acid, the plant peptide hormone systemin has been noticed to be important. Plants use this to systematically react to local injuries. For example, the abiotic stress hormone, absisic acid, imparts disease resistance by acting on several levels involved in biotic stress signalling. Peptide signal-mediated responses are merely one part of a biological process that is controlled by a combination of several hormones. In activating an effective defence response, a combination of systemin, jasmonate and ethylene serves as signal molecules.
The production (biosynthesis) of brassinolide hormones is important for cellular processes and development steps. They are therefore termed metahormones. Arabidopsis plants that lack this hormone remain small and are male-sterile. Many plant hormones apparently play a key role as signals in cell functions and developments that enormously impact the activities of insects. Plant hormones control not only plant growth and development but also serve in communication within the same species, with related or unrelated plant species, and with insects; i.e. they serve in classical metaorganismic communication. The fact that plants and insects produce their hormones differently but apply them for similar purposes, namely to coordinate overall development, points to their use in their unicellular ancestors.
RNAs: Plants can react to the full range of outside influences only through behaviors that are expressed in growth and development; correct timing, which can be very precise, is crucial. Beyond phytohormones, the chemical messenger substances include peptides such as phytosulfokine growth factors and RNAs. Micro-RNAs play an important role in intracellular communication during plant development, either in cleavage during translation/transcription or in preventing translation. Micro-RNAs are apparently necessary for meristem function, organ polarity, vascular development, floral patterning and hormone response. Many of them are developmentally or environmentally regulated. Small interfering RNAs probably serve as signals during early development. In later developmental phases, the RNAi-dependent epigenetic processes are reminded of this early development phase, for example, the heterochromatin configuration. At any rate, these RNAs play important roles in chromatin regulation and therefore in epigenetic silencing.
Re-usable components: Small molecules and proteins that normally support important functions in plant immunity, such as nitric oxide (NO) and reactive oxygen species (ROS), have now been identified as multiply re-usable components of other biological processes. Messenger substances and signal molecules are used as a versatile basic vocabulary in other contexts and other regulation networks, a common principle in the evolution, growth and development of organisms[158,159]. NO is a substance that has a regulatory function in numerous signal processes such as germination, growth, reproduction and disease resistance. The same is true for diverse species of ROS[161,162].
Interpretation of abiotic influences
Mechanical contact has an influence on the overall organism and on the cell level, both in plants and in other eukaryotes. Contact can cause plants: (1) to react aggressively, for example, toward the animals that want to eat them; (2) to discard their pollen; and (3) can cause the plant stem to grow into the sunlight. The entire configuration of a plant (morphogenesis) is partially determined by mechanical inputs, for example, wind and gravity[164,165]. Responses to contact involve signal molecules and hormones along with intracellular calcium, reactive oxygen, octadecanoids and ethylenes. Another common feature is contact-related gene expression. Many of these genes code for calcium bonds, cell wall changes, defence, transcription factors and kinase proteins.
The detection of resources and their periodic, cyclic availability plays a key role in plant memory, planning, growth and development. When, for example, young trees obtain water only once a year, they learn to adjust to this over the following years and concentrate their entire growth and development precisely in the expected period.
Interpretation processes in the plant body are highly sensitive. In taller-growing plants, for example, the water balance places enormous demands on cell wall development and cell wall structures, which must adapt to the often extreme pressures involved in storage and pressure distribution. A sophisticated and multi-levelled feedback- and feedforward-system guarantees a plant-compatible water balance even under extreme environmental conditions[167,168]. To date, 7 different levels of sensitivity to water shortage have been described. They are based on the different types of physiological and phenotypic responses. Plants are especially sensitive to light and have various receptors for UV, blue, green, red and far-red light. The angle of the light, combined with sensation of the growth of adjoining plants, is decisive in enabling plants to coordinate their growth with respect to the optimal light angle and shade avoidance. The adaptive response of the plant; i.e. altered growth, depends on the seconds-, minutes- and hours-long dominating wavelength of the incoming light, and on the combination of wavelengths across the whole day. The roots receive constant signals from the aboveground parts of the plant for specific growth orientations.
Transorganismic communication of plants
Sign-mediated interactions with organisms belonging to other species, genera, families and organismic kingdoms are vital for plants and are coordinated and organized in parallel. They are almost always symbiotic or parasitic and range from mutually beneficial via neutral, up to damaging behaviours. The different forms of symbiotic communication require very different behaviours from the participating partners. This involves large numbers of complementary direct and indirect defence behaviors.
Coordination of defence behaviour: A good example of parallel meta-, inter- and intraorganismic communication are coordinated defence strategies of plants. Chemical signal substances are the oldest form of signs and are used by microbes, fungi, animals and plants. They are transmitted via liquids in the environment or within the plant body; they can be distributed and perceived through the atmosphere. Leaves always emit such volatiles in small doses, but emit greater quantities when infested by parasitic insects. This allows them to attack the parasites either directly by producing substances that deter them, or indirectly by attracting other insects that are natural enemies of the parasites. These volatiles are also perceived by neighboring plants, allowing them to initiate preemptive defensive responses. Volatile phytochemicals serve as airborne semiochemicals. Depending on the behavioural context, destruction, injury or parasitic infestation, the emitted scents clearly differ for both the insects and neighboring plants. The plants coordinate complementary direct and indirect defence mechanisms in a step-wise manner and tailor them flexibly to the severity of the injury or the density of pest infestation[173,174].
When plants are attacked by pests, they develop immune substances that function in a way similar to animals. Injured plants produce aromatic substances that warn other plants. They then rapidly produce enzymes that make the leaves unpalatable for herbivorous insects. Rather than being passive prisoners of their surroundings, plants are active organisms that identify their pests and actively promote the enemies of these pests.
In lima beans, for example, a total of 5 different defence strategies against mite infestation have been discovered. First, they change their scent to make them unattractive to the mites. Then the plants emit scents that are perceived by other plants, which then do precisely the same thing to warn surrounding lima beans before the mites even reach them. Some of the emitted substances had the effect of attracting other mites that ate the attacking red mites. Similar defence processes have been described in tomato plants[173,179].
Plants possess a non-self warning system to fend off dangerous parasites. So-called pattern recognition receptors detect patterns of chemical substances associated with parasite infestation. The microbes, in turn, react to this pattern recognition.
Because plants are sessile, their reaction potential is geared toward defence against mechanical damage and pest infestation. One of the many reaction types to infestation is the production of protease inhibitors I and II, which block protein degradation in the digestive tracts of insects. This defence reaction is produced both at the injured site and throughout the surrounding tissue: the local wound response triggers the production of mobile signals that prompt a systematic reaction of the overall plant.
Plant roots have the capacity to produce 100 000 different compounds, largely secondary metabolites, many with cytotoxic properties, in order to prevent the spread of microbes, insects and other plants[40,41]. For example, plants have developed defence strategies in which substances are emitted in the root zone such as signal mimics, signal blockers and/or signal-degrading enzymes to respond to bacterial quorum sensing. In the defensive position, they can disrupt the communication of parasitic microorganisms to the point that the internal coordination of the parasitic behavior collapses.
“Friendly” arthropods, such as predaceous or fungivorous mites, are supported by plant “domatia”, similar to the situation in complex communities of grasses and fungal endophytes. These symbiospheres, however, can also be misused, for example, by mites that colonize these domatia for themselves without benefiting the host cell.
Communicative coordination: A limited number of chemical messenger substances is available to maintain and simultaneously conduct the communication between: (1) root cells of three different types; (2) root cells and microorganisms; (3) root cells and fungi; and (4) root cells and insects[40,41,52,53,183,184]. The communication process in the root zone is generally meta-, inter- and intraorganismic and requires a high communicative competence in order to be successfully interactive on all three levels and to distinguish messenger molecules from molecules that are not part of messages[42,51,185].
It has been postulated that the origin of root cells in plants, and therefore the basis for the youngest organismic kingdom on our planet, arose through the symbiogenesis of fungi and algae[168,186,187]. One hypothesis assumes that land plants are the symbiogenetic product of green algae and a tip-growing fungus-like organism that combined autotrophic and heterotrophic capabilities.
Symbiosis of plant roots with bacteria, fungi and insects: Plants use their plant-specific synapses to conduct neuronal-like activities and establish symbiotic relationships with bacteria. Similar mutually advantageous relationships are established with mycorrhizal fungi. A special type of plant synapse resembles the immunological synapse of animal cells and allows plants to respond to pathogen and parasite attacks as well as to establish stable symbiotic interactions with rhizobia bacteria and fungal mycorrhiza[70,168,190-194]. Electrical signals can reinforce chemical signals or overcome short-distance responses of fungal mycelia that can be present on root surfaces. Interestingly, rhizobia bacteria are taken up in plant cells via phagocytosis during symbiotic interactions with roots of leguminous plants.
The symbiotic relationship between legumes and rhizobial bacteria leads to the formation of nitrogen-binding nodules in the root zone. Nod factor signalling and thigmotropic responses of root hairs overlap here as well. This once again shows how the same pathways are used for different signal processes.
Plants, insects and microbes share a particular repertoire of signals. Some are therefore also employed strategically. Thus, plants also use insect hormones and signals (prostaglandins) for specific defence behavior. Signal theft is common. Because plants can detect their own signals, they can presumably also detect similar signals that are used in communication between insects.
Viral interactions: In particular, the evolution of plant viruses shows that viruses complement plants both competitively and symbiotically. A healthy plant body is better for most viruses than a sick body. Plant viruses and their development provide a good explanation for the observation that new species originate through symbiogenesis[198,199]. Viruses use intergenomic gene transfer and intragenomic duplication.
Many DNA viruses have encoded numerous nucleic acid metabolisms that are very similar to cell proteins. Examples include DNA polymerases, ribonucleotide reductase subunits, DNA-dependent RNA polymerase II subunits, DNA topoisomerase II, thymidylate synthase, helicases and exoribonuclease. Viruses probably invented DNA to protect their genetic material from being changed by RNA or RNA encoded enzymes.
One of the interaction processes between plant viruses and their host organisms creates a defence level against foreign nucleic acids. Plant viruses code for silencing suppressors in order to act against host RNA silencing, and some of these suppressors effect micro-RNA multiplication and hinder plant development. But also viroids play a symbiotic role. Despite their small size and their non-coded genome, viroids can multiply, systematically spread from cell to cell, and trigger symptoms in the host.
Interorganismic communication of plants
Research has shown that plants can distinguish between damage caused by insects and mechanical injuries. Mechanically injured plants emit substances that are ignored by neighboring plants, whereas they all react immediately to pest infestation.
Plants can distinguish between self and non-self. Thus, defence activities are initiated against foreign roots in order to protect the plant’s own root zone against intruders. The individual sphere of a root, along with its symbiotic partners, requires certain fundamental conditions in order to survive and thrive. When these prerequisites are threatened by the roots of other plants, substances are produced and released in the root zone that hinder this advance[40,41,52,184]. Such defence activities are also deployed as anti-microbial substances against the microflora in the root zone.
Plant roots produce a wide range of chemical substances: (1) some enable species-specific interactions; (2) many of these substances are released tens of centimeters into the surroundings; (3) these substances have strong but not necessarily negative effects on animals, bacteria, viruses and fungi; (4) released substances have a defensive function against other plants; and (5) many substances have absorbtive characteristics that reduce the negative effects of substances.
As reported above in lima beans and tomatoes, corn plants also use a sophisticated communication system to warn each other about pests. By emitting green leafy volatiles, the corn plants attract the natural enemies of the pests and alarm neighboring plants. The alarmed neighbor then produces a protective acid that is normally produced only in response to external injuries.
Plants use biotic signals to inform each other about the presence, absence and identity of neighboring plants, growth space, growth disturbances and competition. Plants that are removed and planted elsewhere remember the identity of their former closest neighbors for several months. Recognition patterns in neuronal-like networks are one possible explanation.
Intraorganismic communication of plants
As opposed to the central nervous system of animals, which controls metabolism and reactions centrally, the control in plants is decentralized. This enables plants to start independent growing or developmental activities in certain regions of their body, for example, on how a particular branch should grow, depending on the wind, light angle and overall “architecture” of the plant. Most of the activities that plants make with regard to growth and development require communication processes (synapse-like communication) between all parts of the plant.
Intercellular communication of plants: Short-distance communication differs considerably from long-distance communication. As a rule, both complement each other. Intercellular communication in the root zone (in the soil) differs from that in the stem region above ground. Both are necessarily coordinated with one another in order to enable life in these different habitats. Intercellular communication informs other plant parts about events in specific organs or regions of the plant (especially in large plants), for example, sugar production in leaves, the reproduction in flowers and resource utilization by the roots.
Plant cells are connected by specific connecting channels (“plasmodesmata”). These connecting channels enable the flow of small molecules as well as ions, metabolites and hormones, and allow the selective exchange (size exclusion limit) of macromolecules such as proteins, RNAs and even cell bodies. The plasmodesmata impart plants with a cytoplasmatic continuum known as the symplasm[101,203]. But plasmodesmata are more than mere transport channels; they also regulate and control the exchange of messenger substances in a very complex manner. In symplastic signalling, the intercellular communication of plants differs fundamentally from that in other organismic kingdoms. It integrates various communication types such as local and long-distance communication. Beyond symplastic communication (especially in the meristem, where new tissues are produced), plants also exhibit the receptor-ligand communication typical of animals. While receptor-ligand communication determines stomatal patterning in the epidermis of mature leaves, trichome patterning is mediated by symplastic signalling.
For long-distance signalling movement, proteins play an important role. Movement proteins convey information bearing RNA, from the stem and leaves, to the remote roots and flowers. The movement protein allows the mRNA to enter the plasmodesmata tunnel, into the phloem flow. Once it has entered this transport system, it can relatively rapidly reach all parts of the plant. These RNAs can control the levels of other proteins. The level contains information for local tissues, for example, about the general physical condition of the plant, the season, or the presence of dangerous enemies.
Plasmodesmata are prerequisites for intercellular communication in higher plants. In embryogenesis they are an important information channel between embryonal and maternal tissue. The further the development of the embryo, the more reduced the cell-cell communication between embryo and maternal tissue. Cell-cell communication via direct transmission of transcription factors plays a central role in root radial and epidermal cell patterning as well as in shoot organogenesis. The cellular organization of the roots is determined during the plant’s embryonic development and is controlled by intercellular communication. Bonke et al provide a particularly good example of communicative control of these 10 phases of embryogenesis. This confirms the presence of local signalling centers and the complex relationship between numerous different signalling pathways.
A wounded plant organizes an integrated molecular, biochemical and cell biological response. This strategy enables information to be transported across great distances, for example, in tall trees. Proteins that can be detected by receptors enable a “thoughtful response” by plants. There are about one thousand known protein kinases/phosphatases, numerous secondary messengers and many thousands of other proteins. Through their life cycles and their growth zones, plants develop a life history of environmental experience that they can pass on to later generations and, should they themselves grow to be several hundred years old, utilize themselves. Even small plants store stress experiences in their memories and then use these memories to coordinate future activities. Especially during growth, key information about the current status often takes a back seat to future-oriented processes, for example, early root growth and nutrient supply to secure future developments such as larger leaves. From this perspective, plants must plan for the future and coordinate growth, food uptake and communication with symbionts.
The complementary differentiation of communication types into short-distance and long-distance signalling, with their different yet ultimately complementary tasks, requires cells to identify their position. They accomplish this by, among other things, detecting signals from neighboring cells. Thus, the identification competence of “self” and “non-self” by cells can be interpreted as a result of social interaction rather than solipsistic behaviour. For example, signals from leaves trigger flower development at the tip of a plant. An entire network involving 4 different signal pathways regulates this transition from the vegetative to the reproductive phase. Most flowers bear closely adjoining male and female reproductive organs. Self-incompatibility is therefore crucial in distinguishing between own (related) and foreign (non-related) pollen. This self-/non-self differentiation ability is promoted by signal processes also used in other plant responses.
Intracellular communication of plants: Intracellular communication in plants takes place between the symbiogenetically assimilated unicellular ancestors of the eukaryotic cell, mainly between the cell body and cell periphery. It transforms and transmits external messages into internal messages that exert a direct (epigenetic) influence on the DNA storage medium and trigger genetic processes; this leads to the production of signal molecules that generate a response behavior. Via endocytosis, however, bacteria, viruses and viroids interfere with this intracellular communication and can support, disrupt or even destroy it. Intracellular communication offers viruses the opportunity to integrate certain genetically coded abilities of the host into their own genome or to integrate their own genetic datasets into the host genome. The ability of viruses to integrate different genetic datasets probably plays a major role in symbiogenetic processes.
The eukaryotic cell is composed of a multicompetent nucleus as a basic building block of life and a cell periphery “apparatus” that was symbiogenetically the ancestor of other endosymbionts. Interestingly, both the nucleus and viruses have several similar features and capabilities: they both lack the protein synthesis “machinery” and the fatty acid-producing pathways. Both transcribe DNA but do not translate it into RNA. Viruses were probably very important in the evolution of eukaryotic cells because they were able to conduct cell-cell “fusion”. There are also strong reasons to believe that the eukaryotic nucleus has a viral origin[220,221].
Neuronal plasticity refers to the ability of neuron populations to alter (either strengthen or weaken) their connections based on experience. This is the basis for learning and memory. Like memory, long-term neuronal plasticity requires new RNA and protein synthesis. Accordingly, the signals must be transported from the synapse, from where they are sent, to the nucleus, where they are transformed to change the gene transcription. Then, the products of gene transcription (proteins, RNAs) must be sent back to the synapse in order to permanently change synaptic strength. This communication process is well described in animals[222-224]; if plants exhibit neuronal-like plasticity, then similar descriptions may follow.
Reports on the transfer of mitochondrial genes between unrelated plant species caused some surprise. While gene transfer is an extremely rare event in animals and fungi, it is common amng plant mitochondria. Variations in repetitive DNA that manifest themselves as variation in the nuclear DNA complex have far-reaching ecological and life history consequences for plants.
The function of a eukaryotic cell depends on successful communication between its various parts. Plastids send signals to regulate nuclear gene expression and thus to reorganize macromolecules in response to environmental influences. It has been shown that micro-RNAs regulate certain developmental processes such as organ separation, polarity and identity, and that they define their own biogenesis and function. Eukaryotic genomes are regionally divided into transcriptionally active euchromatin and transcriptionally inactive heterochromatin. Epigenetic changes can also take place without changes in genomes, for example, through various inactivations and activations of genetic datasets via chromatin remodeling, transposon/retro release, DNA methylation, novel transcription, histone modification and transcription factor interactions. Epigenetic changes are also reversible. Various stress situations in plants are known to cause transposon movements, and bacterial infections or UV stress can cause chromosomal rearrangements[233,234]; i.e. changes in higher-order regulation levels that control the transcription processes of the protein-coding DNA.
Repetitive DNA is present in two syntactic combinations: tandem repeats and dispersed repeats. Tandem repeats consist of sequences that can contain several thousand copies of elements that are dispersed throughout the genome. Pericentromeric sequences consist of a central repetitive nucleus flanked by moderately repetitive DNA. Telomeric and subtelomeric sequences consist of tandem repeats at the physical end of the chromosomes. Retroelements and transposable elements are involved in replication and reinsertion at various sites in complex processes: these include activation of excision, DNA-dependent RNA transcription, translation of RNA into functioning proteins, RNA-dependent DNA synthesis (reverse transcription) and reintegration of newly produced retroelement copies into the genome.
Endocytosis and vesicle recycling via secretory endosomes are indispensable for many processes in multicellular organisms. Plant endocytosis and endosomes are important for auxin-mediated cell-cell communication as well as for gravitropic responses, stomatal movements, cytokinesis and cell wall morphogenesis. As in animals, synaptic cell-cell communication is based on rapid endocytosis and vesicular recycling in plants.
Plants can overwrite the genetic code they inherited from their parents and revert to that of their grandparents or great-grandparents[236-238]. This contradicts traditional DNA-textbook convention that children simply receive combinations of the genes carried by their parents. Now a backup code has been found; it can bypass unhealthy sequences inherited from the parents and revert to the healthier sequences borne by their grandparents or great-grandparents. Research has shown that plants are able to replace abnormal parental code sequences with the regular code possessed by earlier generations. Does this require inheritance not only of the parental genetic make-up but also that of the grandparents and former ancestors? What is proposed is that higher-order regulation function in non-coding DNA, a type of genome-editing MetaCode, save ancestor genome structures, which overrule protein-coding DNA under certain circumstances such as stress. This means that the (pragmatic) situational context of the living plant body may induce epigenetic intervention on the genome-editing MetaCode; i.e. active small non-coding RNAs activate a certain signalling pathway network that can restructure the semantics of a genetic make-up. By initiating chromosomal methylation and histone-modifications, certain silencings, start and stops, and alternative splicing processes constitute alternative sequences. The result is that, in the existing genome architecture, the inherited parental sequences are not translated and transcribed but the backup copy of grandparents or great-grandparents is translated. Under normal conditions, the operative genetic make-up stems from the parents. These research results indicate that not only is a combination of parental genes inherited, but also ancestral genome-regulating features in “non-coding” DNA. This enables alternative splicing pathways; i.e. different use and multiple protein meanings of one and the same genetic data set[236-238].
In contrast to animals and fungi, plants are the youngest organismic kingdom and perhaps the main success story of evolution. They arose approximately 350 million years ago, and terrestrial plants, which flower and bear fruits (a key prerequisite for feeding in larger animals), only developed 150 million years ago. Higher plants make up 99% of the biomass on our planet; of this, nearly 84% are trees. The lack of mobility is often construed as a disadvantage vis-à-vis representatives of the animal kingdom. From an objective perspective, such immobility and the sessile life style must have been an advantage.
Plants fundamentally depend on successful communication. The behaviour in the specific interaction can be misinterpreted. A plant can feign mutualism, for example, in order to gain a one-sided advantage from the interaction and to damage, permanently exploit or kill the partner. This, however, cannot be the representative form of communication because no individuals would survive if all plants behaved in this manner. The majority of interactions must be successful for several participants.
Communication processes are successful when the rules governing sign use are correctly followed. Clearly, rules can be broken. In such cases, the messages transmitted via the signs are incomplete, incorrect, and induce no or a false behavioural response. Messages can also be misinterpreted. The sign user uses: (1) the sign incorrectly/misleadingly, and the message does not arrive in the manner intended or for the envisioned purpose because it is mutilated or fragmentary. In due course, the recipient cannot respond to the message in the manner required by the non-mutilated message; (2) The sign continuously expresses a message that does not conform to reality (“insect enemies are attacking”); the recipient of the message will respond in a manner adapted to the reality of this inconformity; and (3) The message is used to mean something other than is normally conveyed (in order to gain one-sided advantages). Any constant rule-breaking blocks the organization of life processes (communicative coordination of evolution, reproduction, growth and development) within and between organisms.
Integrating this biocommunicative perspective will help to more gradually decipher the specific meaning of the full range of semiochemicals (in their broader sense) and to become aware of the high level communicative competences of plants.
In this paper, I demonstrated that life of the organismic kingdoms of bacteria, fungi and plants is far from being a mechanistic process of action and reaction similar to mere physical entities, but life in these organisms is organized and coordinated by communication processes. These communication processes function, in most cases, very conservatively and error free. Because they depend on syntactic, pragmatic and semantic rules, additionally to natural laws, they may even fail or, in some cases, are error prone. But this flexibility is the precondition for invention, generation, combination or recombination of semiotic rules, which enable organisms to use available chemical molecules in a new way, to generate new sequences and create new sequence regulations. In contrast to non-animate nature, living nature depends on functioning semiosis.
The communicative competences of organisms in these three organismic kingdoms share common features. They resemble transorganismic communication, interorganismic communication, intraorganismic (inter- and intracellular) communication. Additionally, any organism is able to distinguish whether the received chemical molecules are part of a(n): (1) biotic message (Mitwelt); (2) indicator of an abiotic environment (Umwelt); or (3) “noise”, having no biosemiotic feature (Figure 1).
Additionally to the semiotic rules of biocommunication (rule-governed sign-mediated interactions), the biocommunicative approach investigates also the linguistic features of natural genetic engineering and natural genome editing. This is a crucial difference, because there are semiotic rules that determine sign use to generate a context-specific behaviour such as: mating, attack, defense, monitoring, nutrition uptake, and most of all coordination within the organism and between organisms of the same, related or un-related species. The semiotic rules that determine the generation, combination, recombination or insertion of correct nucleic acid sequences have another context. Communicative interaction between organisms is another context, other than correct editing of nucleic acid sequences as I have outlined in another book.
Therefore, successful biocommunicative processes are a precondition for both living organisms (individuals are able to coordinate their behavior) and for all editorial processes in the nucleic acid language; i.e. the genomic content. Without biocommunicative processes, prokaryotic organisms could not coordinate their behavior as multicellular organisms do, nor could real multicellular organisms like animals, fungi and plants live without rule-governed sign-mediated interactions between the cells of their body, and multicellular organisms could not coordinate their behaviour.
Peer reviewers: Herve Seligmann, PhD, Center for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Blindern, 3016 Oslo, Norway; Conceição Maria Fernandes, Professor, Escola Superior Agrária, Instituto Politécnico de Bragança, Escola Superior Agrária, Campus de Santa Apolónia, Apartado 1172, Portugal
Sun J, Daniel R, Wagner-Döbler I, Zeng AP. Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways.BMC Evol Biol. 2004;4:36.
Visick KL, Fuqua C. Decoding microbial chatter: cell-cell communication in bacteria.J Bacteriol. 2005;187:5507-5519.
Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae.Cell. 2004;118:69-82.
Teplitski M, Robinson JB, Bauer WD. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria.Mol Plant Microbe Interact. 2000;13:637-648.
Bauer WD, Robinson JB. Disruption of bacterial quorum sensing by other organisms.Curr Opin Biotechnol. 2002;13:234-237.
Keller L, Surette MG. Communication in bacteria: an ecological and evolutionary perspective.Nat Rev Microbiol. 2006;4:249-258.
Fuqua C, Winans SC, Greenberg EP. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators.Annu Rev Microbiol. 1996;50:727-751.
Witzany G. Plant communication from biosemiotic perspective: differences in abiotic and biotic signal perception determine content arrangement of response behavior. Context determines meaning of meta-, inter- and intraorganismic plant signaling.Plant Signal Behav. 2006;1:169-178.
Samaj J, Baluska F, Voigt B, Schlicht M, Volkmann D, Menzel D. Endocytosis, actin cytoskeleton, and signaling.Plant Physiol. 2004;135:1150-1161.
Kiers ET, Rousseau RA, West SA, Denison RF. Host sanctions and the legume-rhizobium mutualism.Nature. 2003;425:78-81.
Walker TS, Bais HP, Grotewold E, Vivanco JM. Root exudation and rhizosphere biology.Plant Physiol. 2003;132:44-51.
Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM. How plants communicate using the underground information superhighway.Trends Plant Sci. 2004;9:26-32.
Sharma A, Sahgal M, Johri BN. Microbial communication in the rhizosphere: Operation of quorum sensing.Curr Sci. 2003;85:1164-1172.
Velicer GJ. Social strife in the microbial world.Trends Microbiol. 2003;11:330-337.
Rice SA, Givskov M, Steinberg P, Kjelleberg S. Bacterial signals and antagonists: the interaction between bacteria and higher organisms.J Mol Microbiol Biotechnol. 1999;1:23-31.
Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. Bacteria-host communication: the language of hormones.Proc Natl Acad Sci USA. 2003;100:8951-8956.
Margulis L. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life.Proc Natl Acad Sci USA. 1996;93:1071-1076.
Margulis L. Die andere Evolution. Heidelberg: Spektrum Akademischer Verlag; 1999;.
Margulis L. Serial endosymbiotic theory (SET) and composite individuality. Transition from bacterial to eukaryotic genomes.Microbiol Today. 2004;31:172-174.
Margulis L, Sagan D. Acquiring Genomes: A Theory of the Origins of Species. New York: Basic Books; 2002;.
Batut J, Andersson SG, O'Callaghan D. The evolution of chronic infection strategies in the alpha-proteobacteria.Nat Rev Microbiol. 2004;2:933-945.
Federle MJ, Bassler BL. Interspecies communication in bacteria.J Clin Invest. 2003;112:1291-1299.
Dunn AK, Handelsman J. Toward an understanding of microbial communities through analysis of communication networks.Antonie Van Leeuwenhoek. 2002;81:565-574.
McNab R, Lamont RJ. Microbial dinner-party conversations: the role of LuxS in interspecies communication.J Med Microbiol. 2003;52:541-545.
Ben-Jacob E, Levine H. Self-engineering capabilities of bacteria.J R Soc Interface. 2006;3:197-214.
Velicer GJ, Kroos L, Lenski RE. Developmental cheating in the social bacterium Myxococcus xanthus.Nature. 2000;404:598-601.
Shapiro JA. Thinking about bacterial populations as multicellular organisms.Annu Rev Microbiol. 1998;52:81-104.
Shapiro JA. Bacteria are small but not stupid: cognition, natural genetic engineering and socio-bacteriology.Stud Hist Philos Biol Biomed Sci. 2007;38:807-819.
Velicer GJ, Yu YT. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus.Nature. 2003;425:75-78.
Taga ME, Bassler BL. Chemical communication among bacteria.Proc Natl Acad Sci USA. 2003;100 Suppl 2:14549-14554.
Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L. A bacterial cell-cell communication signal with cross-kingdom structural analogues.Mol Microbiol. 2004;51:903-912.
Kaiser D, Welch R. Dynamics of fruiting body morphogenesis.J Bacteriol. 2004;186:919-927.
Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ Jr. Communication among oral bacteria.Microbiol Mol Biol Rev. 2002;66:486-505, table of contents.
Moore WE, Moore LV. The bacteria of periodontal diseases.Periodontol 2000. 1994;5:66-77.
Kroes I, Lepp PW, Relman DA. Bacterial diversity within the human subgingival crevice.Proc Natl Acad Sci USA. 1999;96:14547-14552.
Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE. Bacterial diversity in human subgingival plaque.J Bacteriol. 2001;183:3770-3783.
Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots.Nature. 2005;433:527-531.
Xie G, Bonner CA, Song J, Keyhani NO, Jensen RA. Inter-genomic displacement via lateral gene transfer of bacterial trp operons in an overall context of vertical genealogy.BMC Biol. 2004;2:15.
Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria.Nat Rev Microbiol. 2005;3:711-721.
Bordenstein SR, Reznikoff WS. Mobile DNA in obligate intracellular bacteria.Nat Rev Microbiol. 2005;3:688-699.
Olendzenski L, Gogarten JP. Evolution of genes and organisms: the tree/web of life in light of horizontal gene transfer.Ann N Y Acad Sci. 2009;1178:137-145.
Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: the complexity hypothesis.Proc Natl Acad Sci USA. 1999;96:3801-3806.
Jain R, Rivera MC, Moore JE, Lake JA. Horizontal gene transfer accelerates genome innovation and evolution.Mol Biol Evol. 2003;20:1598-1602.
Brown JR. Ancient horizontal gene transfer.Nat Rev Genet. 2003;4:121-132.
Berg OG, Kurland CG. Evolution of microbial genomes: sequence acquisition and loss.Mol Biol Evol. 2002;19:2265-2276.
Rivera MC, Lake JA. The ring of life provides evidence for a genome fusion origin of eukaryotes.Nature. 2004;431:152-155.
Kunin V, Goldovsky L, Darzentas N, Ouzounis CA. The net of life: reconstructing the microbial phylogenetic network.Genome Res. 2005;15:954-959.
Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome".Proc Natl Acad Sci USA. 2005;102:13950-13955.
Villarreal LP. Viruses and the Evolution of Life. Washington: American Society for Microbiology Press; 2005;.
Graumann PL. Cytoskeletal elements in bacteria.Curr Opin Microbiol. 2004;7:565-571.
Graumann PL, Defeu Soufo HJ. An intracellular actin motor in bacteria?Bioessays. 2004;26:1209-1216.
Defeu Soufo HJ, Graumann PL. Dynamic movement of actin-like proteins within bacterial cells.EMBO Rep. 2004;5:789-794.
Guerrero R, Berlanga M. The hidden side of the prokaryotic cell: rediscovering the microbial world.Int Microbiol. 2007;10:157-168.
Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J. Signal transduction cascades regulating fungal development and virulence.Microbiol Mol Biol Rev. 2000;64:746-785.
Lang BF, O'Kelly C, Nerad T, Gray MW, Burger G. The closest unicellular relatives of animals.Curr Biol. 2002;12:1773-1778.
Margulis L, Schwartz KV. Five Kingdoms. New York: WH Freeman and Company; 1988;.
Fungal Genetics Stock Center. The Neurospora Homepage. New York: WH Freeman and Company; 2010; Available from: http://www.fgsc.net.
Dunlap JC, Loros JJ, Denault D, Lee K, Froelich A, Colot H, Shi M, Preguero A. Genetics and molecular biology of circadian rhythms.The Mycota III. Biochemistry and Molecular Biology. 2nd ed. Berlin/Heidelberg: Springer; 2004;209-229.
Ercan S, Lieb JD. New evidence that DNA encodes its packaging.Nat Genet. 2006;38:1104-1105.
Arora DK. Handbook of Fungal biotechnology. New York: Marcel Dekker; 2004;.
Witzany G. Biocommunication and natural genome editing. Dordrecht: Springer; 2010;.
Sullivan BT, Berisford CW. Semiochemicals from fungal associates of bark beetles may mediate host location behavior of parasitoids.J Chem Ecol. 2004;30:703-717.
Adachi K, Hamer JE. Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea.Plant Cell. 1998;10:1361-1374.
Wang P, Heitman J. Signal transduction cascades regulating mating, filamentation, and virulence in Cryptococcus neoformans.Curr Opin Microbiol. 1999;2:358-362.
Hemenway CS, Heitman J. Calcineurin. Structure, function, and inhibition.Cell Biochem Biophys. 1999;30:115-151.
Alspaugh JA, Cavallo LM, Perfect JR, Heitman J. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans.Mol Microbiol. 2000;36:352-365.
Borges-Walmsley MI, Walmsley AR. cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity.Trends Microbiol. 2000;8:133-141.
Fernandes L, Araújo MA, Amaral A, Reis VC, Martins NF, Felipe MS. Cell signaling pathways in Paracoccidioides brasiliensis--inferred from comparisons with other fungi.Genet Mol Res. 2005;4:216-231.
de Paula RM, Lamb TM, Bennett L, Bell-Pedersen D. A connection between MAPK pathways and circadian clocks.Cell Cycle. 2008;7:2630-2634.
Bell-Pedersen D, Dunlap JC, Loros JJ. Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa eas (ccg-2) gene.Mol Cell Biol. 1996;16:513-521.
Sanders WB. A feeling for the superorganism: expression of plant form in the lichen thallus.Bot J Linn Soc. 2006;150:89-99.
Sanders WB. Lichens: the interface between mycology and plant morphology.Bioscience. 2001;51:1025.
Hogan DA. Talking to themselves: autoregulation and quorum sensing in fungi.Eukaryot Cell. 2006;5:613-619.
Kopper BJ, Klepzig KD, Raffa KF. Components of antagonism and mutualism in Ips pini-fungal interactions: Relationship to a life history of colonizing highly stressed and dead trees.Environ Entomol. 2004;33:28-34.
Poulsen M, Boomsma JJ. Mutualistic fungi control crop diversity in fungus-growing ants.Science. 2005;307:741-744.
Cornelius ML, Bland JM, Daigle DJ, Williams KS, Lovisa MP, Connick WJ Jr, Lax AR. Effect of a lignin-degrading fungus on feeding preferences of Formosan subterranean termite (Isoptera: Rhinotermitidae) for different commercial lumber.J Econ Entomol. 2004;97:1025-1035.
Jakupović M, Heintz M, Reichmann P, Mendgen K, Hahn M. Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae.Fungal Genet Biol. 2006;43:8-19.
Lammers PJ. Symbiotic signaling: new functions for familiar proteins.New Phytol. 2004;16:324-326.
Prusty R, Grisafi P, Fink GR. The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae.Proc Natl Acad Sci USA. 2004;101:4153-4157.
Brundrett MC. Coevolution of roots and mycorrhizas of land plants.New Phytol. 2002;154:275-304.
Schwarze FW, Engels J, Mattheck C. Fungal strategies of wood decay in trees. Second Edition, Heidelberg: Springer; 2004;.
Bhabhra R, Zhao W, Rhodes JC, Askew DS. Nucleolar localization of Aspergillus fumigatus CgrA is temperature-dependent.Fungal Genet Biol. 2006;43:1-7.
Casadevall A. Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection?Fungal Genet Biol. 2005;42:98-106.
Banuett F. Signalling in the yeasts: an informational cascade with links to the filamentous fungi.Microbiol Mol Biol Rev. 1998;62:249-274.
Glass NL, Jacobson DJ, Shiu PK. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi.Annu Rev Genet. 2000;34:165-186.
Glass NL, Saupe SJ. Vegetative incompatibility in filamentous ascomycetes.Molecular biology of fungal development. New York: Marcel Dekker; 2002;109-131.
Glass NL, Kaneko I. Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi.Eukaryot Cell. 2003;2:1-8.
Wu J, Glass NL. Identification of specificity determinants and generation of alleles with novel specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa.Mol Cell Biol. 2001;21:1045-1057.
Reynolds TB, Fink GR. Bakers' yeast, a model for fungal biofilm formation.Science. 2001;291:878-881.
Schultze K, Schimek C, Wöstemeyer J, Burmester A. Sexuality and parasitism share common regulatory pathways in the fungus Parasitella parasitica.Gene. 2005;348:33-44.
Belozerskaya TA. Cell-to-cell communication in differentiation of mycelial fungi.Membr Cell Biol. 1998;11:831-840.
Gessler NN, Aver'yanov AA, Belozerskaya TA. Reactive oxygen species in regulation of fungal development.Biochemistry (Mosc). 2007;72:1091-1109.
Bardwell L. A walk-through of the yeast mating pheromone response pathway.Peptides. 2004;25:1465-1476.
Dohlman HG. G proteins and pheromone signaling.Annu Rev Physiol. 2002;64:129-152.
Kays AM, Borkovich KA. Signal transduction pathways mediated by heterotrimeric G proteins.editors. The mycota III. Berlin: Springer; 2004;175-207.
Hoffman CS. Except in every detail: comparing and contrasting G-protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe.Eukaryot Cell. 2005;4:495-503.
Crespo JL, Hall MN. Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae.Microbiol Mol Biol Rev. 2002;66:579-591, table of contents.
Beck T, Hall MN. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors.Nature. 1999;402:689-692.
Cutler NS, Pan X, Heitman J, Cardenas ME. The TOR signal transduction cascade controls cellular differentiation in response to nutrients.Mol Biol Cell. 2001;12:4103-4113.
Rohde JR, Cardenas ME. Nutrient signaling through TOR kinases controls gene expression and cellular differentiation in fungi.Curr Top Microbiol Immunol. 2004;279:53-72.
D'Souza CA, Heitman J. Conserved cAMP signaling cascades regulate fungal development and virulence.FEMS Microbiol Rev. 2001;25:349-364.
Mitchell TK, Dean RA. The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea.Plant Cell. 1995;7:1869-1878.
Krüger J, Loubradou G, Regenfelder E, Hartmann A, Kahmann R. Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis.Mol Gen Genet. 1998;260:193-198.
Hartmann HA, Kahmann R, Bölker M. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis.EMBO J. 1996;15:1632-1641.
Hartmann HA, Krüger J, Lottspeich F, Kahmann R. Environmental signals controlling sexual development of the corn Smut fungus Ustilago maydis through the transcriptional regulator Prf1.Plant Cell. 1999;11:1293-1306.
Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae.Nature. 2004;428:617-624.
Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. Sequencing and comparison of yeast species to identify genes and regulatory elements.Nature. 2003;423:241-254.
Flores HE, Vivanco JM, Loyola-Vargas VM. 'Radicle' biochemistry: the biology of root-specific metabolism.Trends Plant Sci. 1999;4:220-226.
Baluska F, Volkmann D, Barlow PW. Eukaryotic cells and their cell bodies: Cell Theory revised.Ann Bot. 2004;94:9-32.
Baluska F, Volkmann D, Barlow PW. Cell-cell channels and their implications for cell theory.editors. Cell-cell channels. Georgetown: Eurekah.com; 2005;1-17.
Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluska F. Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices.Plant Signal Behav. 2006;1:122-133.
Campanoni P, Blasius B, Nick P. Auxin transport synchronizes the pattern of cell division in a tobacco cell line.Plant Physiol. 2003;133:1251-1260.
Casson SA, Lindsey K. Genes and signalling in root development.New Phytol. 2003;158:11-38.
Friml J, Wisniewska J. Auxin as an intercellular signal.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;1-26.
Xia Y. Peptides as signals.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;27-47.
Mauch-Mani B, Mauch F. The role of abscisic acid in plant-pathogen interactions.Curr Opin Plant Biol. 2005;8:409-414.
Amzallag GN. Brassinosteroids as metahormones: evidence for their specific influence during the critical period in sorghum development.Plant Biol (Stuttg). 2002;4:656-663.
Thummel CS, Chory J. Steroid signaling in plants and insects--common themes, different pathways.Genes Dev. 2002;16:3113-3129.
Fleming AJ. The plant extracellular matrix and signalling.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;85-107.
Kidner CA, Martienssen RA. The developmental role of microRNA in plants.Curr Opin Plant Biol. 2005;8:38-44.
Farmer E, Schulze-Lefert P. Biotic interactions: From molecular networks to inter-organismal communities.Curr Opin Plant Biol. 2005;8:343-345.
Torres MA, Dangl JL. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Curr Opin Plant Biol. 2005;8:397-403.
Delledonne M. NO news is good news for plants.Curr Opin Plant Biol. 2005;8:390-396.
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Annu Rev Plant Biol. 2004;55:373-399.
Carol RJ, Dolan L. The role of reactive oxygen species in cell growth: lessons from root hairs.J Exp Bot. 2006;57:1829-1834.
Braam J. In touch: plant responses to mechanical stimuli.New Phytol. 2005;165:373-389.
Morita MT, Tasaka M. Gravity sensing and signaling.Curr Opin Plant Biol. 2004;7:712-718.
Ross JJ, Wolbang CM. Auxin, gibberellins and the gravitropic response of grass leaf sheath pulvini.Plant Signal Behav. 2008;3:74-75.
Heilmeier H, Erhard M, Schulze ED. Biomass accumulation and water use under arid conditions.Plant resource allocation. London: Academic Press; 1997;93-113.
Zimmermann U, Schneider H, Wegner LH, Haase A. Water ascent in tall trees: does evolution of land plants rely on a highly metastable state?New Phytol. 2004;162:575-615.
Buckley TN. The control of stomata by water balance.New Phytol. 2005;168:275-292.
Trewavas A. Green plants as intelligent organisms.Trends Plant Sci. 2005;10:413-419.
Ballaré CL. Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms.Trends Plant Sci. 1999;4:97-102.
Baluška F, Volkmann D, Hlavacka A, Mancuso S, Barlow PW. Neurobiological view of plants and their body plan.Communication in plants. Berlin/Heidelberg: Springer; 2006;19-35.
Pare PW, Tumlinson JH. Plant volatiles as a defense against insect herbivores.Plant Physiol. 1999;121:325-332.
Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC. Differential timing of spider mite-induced direct and indirect defenses in tomato plants.Plant Physiol. 2004;135:483-495.
Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. Airborne signals prime plants against insect herbivore attack.Proc Natl Acad Sci USA. 2004;101:1781-1785.
Nürnberger T, Brunner F, Kemmerling B, Piater L. Innate immunity in plants and animals: striking similarities and obvious differences.Immunol Rev. 2004;198:249-266.
Peak D, West JD, Messinger SM, Mott KA. Evidence for complex, collective dynamics and emergent, distributed computation in plants.Proc Natl Acad Sci USA. 2004;101:918-922.
Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists.Trends Ecol Evol. 2001;16:547-554.
Mithöfer A, Wanner G, Boland W. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission.Plant Physiol. 2005;137:1160-1168.
Pearce G, Ryan CA. Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene.J Biol Chem. 2003;278:30044-30050.
Zipfel C, Felix G. Plants and animals: a different taste for microbes?Curr Opin Plant Biol. 2005;8:353-360.
Nomura K, Melotto M, He SY. Suppression of host defense in compatible plant-Pseudomonas syringae interactions.Curr Opin Plant Biol. 2005;8:361-368.
Romero GQ, Benson WW. Biotic interactions of mites, plants and leaf domatia.Curr Opin Plant Biol. 2005;8:436-440.
Callaway RM. The detection of neighbors by plants.Trends Ecol Evol. 2002;17:104-105.
Faure D, Vereecke D, Leveau JHJ. Molecular communication in the rhizosphere.Plant Soil. 2009;321:279-303.
Hirsch AM, Bauer DW, Bird DM, Cullimore J, Tyler B, Yoder JI. Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms.Ecology. 2003;84:858-868.
Jorgensen R. The origin of land plants: a union of alga and fungus advanced by flavonoids?Biosystems. 1993;31:193-207.
Zyalalov AA. Water flows in higher plants: physiology, evolution and system analysis.Russ J Plant Physiol. 2004;51:547-555.
Jorgensen RA. Restructuring the genome in response to adaptive challenge: McClintock's bold conjecture revisited.Cold Spring Harb Symp Quant Biol. 2004;69:349-354.
Denison RF, Toby Kiers E. Why are most rhizobia beneficial to their plant hosts, rather than parasitic?Microbes Infect. 2004;6:1235-1239.
Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JP. Extensive fungal diversity in plant roots.Science. 2002;295:2051.
Estabrock EM, Yoder JI. Plant-plant communications: rhizosphere signalling between parasitic angiosperms and their hosts.Plant Physiol. 1998;116:1-7.
Yoder JI. Parasitic plant responses to host plant signals: a model for subterranean plant-plant interactions.Curr Opin Plant Biol. 1999;2:65-70.
Keyes WJ, O'Malley RC, Kim D, Lynn DG. Signaling Organogenesis in Parasitic Angiosperms: Xenognosin Generation, Perception, and Response.J Plant Growth Regul. 2000;19:217-231.
Kahmann R, Basse C. Fungal gene expression during pathogenesis-related development and host plant colonization.Curr Opin Microbiol. 2001;4:374-380.
van West P, Morris BM, Reid B, Appiah AA, Osborne MC, Campbell TA, Shepherd SJ. Oomycete plant pathogens use electric fields to target roots.Mol Plant Microbe Interact. 2002;15:790-798.
Geurts R, Fedorova E, Bisseling T. Nod factor signaling genes and their function in the early stages of Rhizobium infection.Curr Opin Plant Biol. 2005;8:346-352.
Schultz JC, Appel HM. Cross-kingdom cross-talk: Hormones shared by plants and their insect herbivores.Ecology. 2004;85:70-77.
Roossinck MJ. Symbiosis versus competition in plant virus evolution.Nat Rev Microbiol. 2005;3:917-924.
Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance.Science. 2007;315:513-515.
Shackelton LA, Holmes EC. The evolution of large DNA viruses: combining genomic information of viruses and their hosts.Trends Microbiol. 2004;12:458-465.
Dunoyer P, Voinnet O. The complex interplay between plant viruses and host RNA-silencing pathways.Curr Opin Plant Biol. 2005;8:415-423.
Wang MB, Metzlaff M. RNA silencing and antiviral defense in plants.Curr Opin Plant Biol. 2005;8:216-222.
Dunnoyer P, Voinnet O. RNA as a signalling molecule.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;49-83.
Turkington R, Sackville Hamilton R, Gliddon C. Within-population variation in localized and integrated responses of Trifolium repens to biotically patchy environments.Oecologia. 1991;86:183-192.
Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, McFarland KC, Franceschi VR, Lucas WJ. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem.Science. 1999;283:94-98.
Gillespie T, Oparka KJ. Plasmodesmata-gateways for intercellular communication in plants.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;109-146.
Golz JF. Lessons from the vegetative shoot apex.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;147-177.
Srinivas BP, Hülskamp M. Lessons from leaf epidermal patterning in plants.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;225-239.
Tassetto M, Maizel A, Osorio J, Joliot A. Plant and animal homeodomains use convergent mechanisms for intercellular transfer.EMBO Rep. 2005;6:885-890.
Kim I, Zambryski PC. Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis.Curr Opin Plant Biol. 2005;8:593-599.
Kurata T, Okada K, Wada T. Intercellular movement of transcription factors.Curr Opin Plant Biol. 2005;8:600-605.
Bonke M, Tähtiharju S, Helariutta Y. Lessons from the root apex.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;199-223.
Schilmiller AL, Howe GA. Systemic signaling in the wound response.Curr Opin Plant Biol. 2005;8:369-377.
McClintock B. The significance of responses of the genome to challenge.Science. 1984;226:792-801.
Goh CH, Nam HG, Park YS. Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants.Plant J. 2003;36:240-255.
Trewavas A. Aspects of plant intelligence.Ann Bot. 2003;92:1-20.
Coupland G. Intercellular communication during floral initiation and development.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;178-197.
McCubbin AG. Lessons in signalling in plant self-incompatibility systems.Intercellular communication in plants. Annual plant reviews. Oxford: Blackwell Publishing; 2005;240-275.
Baluska F, Volkmann D, Menzel D. Plant synapses: actin-based domains for cell-to-cell communication.Trends Plant Sci. 2005;10:106-111.
Bell PJ. Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?J Mol Evol. 2001;53:251-256.
Villarreal LP. Origin of Group Identity: Viruses, Addiction and Cooperation. New York: Springer; 2009;.
Thompson KR, Otis KO, Chen DY, Zhao Y, O'Dell TJ, Martin KC. Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway.Neuron. 2004;44:997-1009.
Martin KC. Local protein synthesis during axon guidance and synaptic plasticity.Curr Opin Neurobiol. 2004;14:305-310.
Moccia R, Chen D, Lyles V, Kapuya E, E Y, Kalachikov S, Spahn CM, Frank J, Kandel ER, Barad M. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs.J Neurosci. 2003;23:9409-9417.
Andersson JO. Lateral gene transfer in eukaryotes.Cell Mol Life Sci. 2005;62:1182-1197.
Meagher TR, Vassiliadis C. Phenotypic impacts of repetitive DNA in flowering plants.New Phytol. 2005;168:71-80.
Strand A. Plastid-to-nucleus signalling.Curr Opin Plant Biol. 2004;7:621-625.
Dugas DV, Bartel B. MicroRNA regulation of gene expression in plants.Curr Opin Plant Biol. 2004;7:512-520.