Crosstalk in Plant Cell Signaling: Structure and Function of the Genetic Network

trends in plant science perspectives

analysis of Arabidopsis has unraveled the Crosstalk in plant cell components involved in ethylene signal transduction11,12. The pathway defined by this approach is a system of MAP kinase cascades. signaling: structure and The ethylene precursor 1-aminocyclo- propane-1-carboxylic acid can phenocopy many effects of the gin1 allele identified in a function of the genetic new glucose-insensitive Arabidopsis mutant defective in various glucose-specific responses, such as cotyledon expansion and greening, network shoot development, floral transition and gene expression13. In addition, ethylene antagonizes Thierry Genoud and Jean-Pierre Métraux the glucose signal in the wild type, and the ethylene-insensitive mutants exhibit a glucose hypersensitivity13. Thus, the glucose pathway Cell signaling integrates independent stimuli using connections between and probably an ethylene-inhibited MAPK biochemical pathways. The sensory apparatus can be represented as a cascade interact positively to activate a com- network, and the connections between pathways are termed crosstalk. Here, mon branch of signal transduction leading to the we describe several examples of crosstalk in plant biology. To formalize the control of germination and cotyledon devel- network of signal transduction we evaluated the relevance of mechanistic opment (Figs 1 and 2). However, modulation models used in artificial intelligence. Although the perceptron model of neural of photosynthetic gene repression by sucrose, networking provides a good description of the process, we suggest that or control of the ethylene triple-response13 are Boolean networks should be used as a starting framework. The Boolean not subjected to this interference. network model allows genetic data to be integrated into the logical network of connections deduced from DNA microarray data. Crosstalk between light signal transduction and pathogenesis-related gene signaling wing to their sedentary lifestyle, plants wound-peptide signal) and by jasmonic acid pathway have evolved plasticity in metabolism (Ref. 4). This inhibition presumably occurs at Crosstalk has been observed between red light Oand morphology, which allowed the the level of an enzyme involved in jasmonic and PR-expression-signaling pathways14. The colonization of diverse environments. To acid synthesis. However, in rice, the salicylic Arabidopsis light-hypersensitive psi2 mutant accommodate their metabolism to the sur- acid-analog INA (2,6-dichloroisonicotinic acid) exhibits a light fluence-dependent amplification rounding conditions, plant cells integrate dif- stimulates the expression of genes induced by of salicylic acid-induced PR1a gene expres- ferent environmental stimuli with internal jasmonic acid in a synergistic manner5, and sion (T. Genoud et al., unpublished; Figs 1–3). signals through a parallel processing of infor- reciprocal treatment with jasmonic acid pro- To confirm observations that the light signal mation. Signal transduction and amplification duces a positive regulating effect on the sali- regulates the sensitivity to salicylic acid, the has been described in many cases of stimuli cylic acid-induced pathway. In Arabidopsis, expression of PR genes was scored in mutants sensing, such as hormone, heat, light, salt or an additional element (CPR6) can modulate containing no detectable phytochrome A and pathogen perception. So far, the sequences of the expression of pathogenesis-related (PR) B proteins. In these plants, expression of PR the biochemical steps, which are initiated after genes via the salicylic acid signal transduction genes elicited by salicylic acid or benzo- perception, have been represented by a para- pathway, as well as thionin or defensin genes (1,2,3)-thiadiazole-7-carbothioic acid S-methyl digm of independent cascade events. through the jasmonic acid pathway6. ester (a salicylic acid-agonist) is strongly However, experimental evidence has shown reduced and the resistance to Pseudomonas recently that interactions between signal trans- Ethylene and jasmonic acid pathways syringae pv. maculicola, is significantly reduction pathways do exist. Direct connections crosstalk duced (T. Genoud et al., unpublished). A between specific pathways furnish a rapid and In tobacco, a synergy has been observed screen has been set up with a mutagenized efficient tuning mechanism for optimizing between ethylene and methyl jasmonate (Figs population of psi2 to find plants that are non-cognitive behavior in response to various 1 and 2) for the induction of two PR genes that blocked in the crosstalk between the phy- combinations of stimuli. code for PR1b and osmotin7. In tomato, upon tochrome pathway and PR induction. This Crosstalk connections between pathways, wounding, both ethylene and jasmonic acid should eventually lead to the identification of also called interferences or intersections, are are required for the induction of proteinase a trans-signaling element. widespread in plants, as illustrated by the fol- inhibitor genes8. In the case of Arabidopsis, lowing examples. ethylene and methyl jasmonate concomitantly Phytochrome signaling crosstalk with induces the expression of a gene coding for an cryptochrome signaling Crosstalk in controlled defense responses antifungal plant defensin PDF1.2 (Ref. 9), The proportion of blue, red and far-red light in Leaves wounded by insects or by mechanical whereas neither substance induces PR1. In incoming white light is interpreted by the sig- damage induce the proteinase inhibitor pro- Arabidopsis, the growth responses controlled naling network in different ways. For exam- duction both locally and systemically1 (Figs 1 by each hormone are independent. ple, blue light acts synergistically with red and 2). Transduction of the wound-related sig- light in the activation of the phytochrome nal involves the octadecanoid pathway, and Ethylene and glucose pathways crosstalk pathway, which controls processes such as can be mimicked by treatment with jasmonic The phytohormone, ethylene, affects many cotyledon unfolding and cell elongation15. acid2. Salicylic acid is implicated in the per- developmental stages of plants, for instance Further experiments performed with ception of pathogen attack in many plant cell elongation, seed germination, fruit ripen- Arabidopsis mutants deficient in one or sev- species3, and inhibits the activation of wounding and senescence, and is also implicated in eral photoreceptors have confirmed these induced genes elicited by systemin (a systemic biotic10,11 and abiotic stress perception8. Genetic physiological observations. The results suggest

(a) (a) aR NOT a R Wounding JA JA-responses 01 10 Dicot. Rice (b) abR Pathogen SA PRs a 000 AND R b 010 (b) 100 AND AND 111 Wounding JA JA-responses (c) abR NOT Dicot. Rice a 000 OR R 011 PRs b Pathogen SA 101 AND 111

(c) (d) abR a 001 Ethylene Growth response NAND R PDF1.2 or b 011 Pathogen or PR1b 101 wounding 110 AND osmotin MeJA Growth response (e) abR a 001 (d) NOR R b 010 Photosynthesis genes 100 Glucose GIN1 NOT 110 Germination Cotyledon development (f) abR MAPK cascade AND a 000 XOR R NOT b 011 Ethylene Triple response 101 110 (e) (g) abR Light phyA, phyB Light-induced genes a 001 XNOR R b 010 100 111 Pathogen SA PR1a, other PRs (?) AND Trends in Plant Science Trends in Plant Science Fig. 2. Representation of logical gates. Fig. 1. Schematic representations of some examples of crosstalks between plant signal trans- Input signals are represented by a and b, duction pathways using Boolean symbols. The crosstalks between the salicylic acid (SA) the resulting signal leaving the switch is and jasmonic acid (JA) pathways are represented in intuitive formalism (a) and in a Boolean represented by R. Presence or absence of a translation (b) as defined in Fig. 2. (c) Activation of defense-related genes in Arabidopsis by phenomenologically significant signal is the concomitant control of ethylene and methyl jasmonate (MeJA). (d) Crosstalk between designated by 1 and 0, respectively. ethylene and glucose signaling in Arabidopsis. (e) Crosstalk between light and patho- Abbreviations: NAND,: not-and; NOR, genesis-related (PR) gene signaling. The AND gates combine signals synergetically whereas not-or; XOR, exclusive-or; XNOR, repressions are represented by a NOT gate connected to an AND gate. exclusive-not-or. that the level of active phytochrome strongly photoreceptor phyA, phyB and cry1, it was by a phyA-associated kinase activity, indicating modulates the activity of the cry1 photore- shown that: that crosstalk probably occurs at the receptors ceptor16, whereas the absence of cry1 does not • The blue-light-response mediated by cry1 level19 (Fig. 4). modify the activity of the phytochrome path- in blue light is modulated by phyB. From the various observations mentioned way. However, this synergistic effect is con- • The effect of phyA and phyB on chloro- here, it is inferred that blue and far-red light ditional17: in experiments where blue light is phyll accumulation in de-etiolated act antagonistically to modify signaling by added to a red-light background, under short seedlings is modulated by cry1. phyB. In addition, UV-B and UV-A wave- exposures of blue light, cry1 activity requires • In far-red light, both phyB and cry1 are lengths can replace the blue light required for phyB. Whereas, under prolonged exposures of modulators of the accumulation of antho- the stimulation of chalcone synthase expres- blue light, the effects of cry1 and phyB are cyanin controlled by the phyA molecule18. sion, and a synergism occurs between these independent for the control of hypocotyl elon- Recent results demonstrate that cry1 and phyA UV-pathways and the cry1 signal20. These few gation and cotyledon opening17. Using a com- photoreceptors interact in a two-hybrid system examples highlight the complexity of light bination of specific mutants in the and that the cry1 molecule is phosphorylated signal processing in plants.

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Pathogen Far-red light Blue light

SA phyA PSI2 ? cry1

PR1a cry1-Modulated other PRs (?) blue-light responses G-prot. cGMP Ca2+ and CaM Fig. 3. Lesions in Arabidopsis leaves caused by high fluence white light in a light-hypersensitive mutant psi2 (a), scale bar ϭ 1 mm, and by the bacterium Pseudomonas syringae in a wild-type plant (b), scale bar ϭ 2 mm. Both treat- ments lead to the activation of disease ChS resistance and the corresponding defense genes. The signal transduction pathways CAB initiated by light stimulus and pathogen SUN1,6,7 Suc attack crosstalk synergetically for the As1 subsequent induction of resistance. Pc Trends in Plant Science Fig. 4. Connections and crosstalks within the phyA signaling network. The signal transduction induced by activation of phytochrome A is not fully linear, but divides into at least two Crosstalk between sucrose and light signal subpathways33,34. The first events might implicate a trimeric G-protein (Ref. 33). Later, the transduction pathways pathway divides in two branches, one regulated by calcium and calmodulin and the other In contrast with nitrate reductase or chalcone involving cGMP (Ref. 34). Activation of phyA-controlled genes, such as chalcone synthase synthase21, the phyA-activated genes involved (ChS), only requires mobilization of the cGMP-controlled pathway, whereas the activation in photosynthesis, such as CAB, RBCS and of genes coding for photosystem II components [such as chlorophyll a/b-binding protein PLASTOCYANIN (PC), are repressed by glu- (CAB)] is controlled by the calcium-modulated branch. A third group of genes [correspond- cose or sucrose21,22 (Fig. 4). PC expression is ing to components of phytosystem I, such as plastocyanin (PC)] is inducible by an adequate 35 upregulated by the phyA pathway (activated combination of both pathway activities, and a fourth [asparagine synthase gene (AS1)] is by far-red light) and repressed by sucrose, repressed by the same combination. A negative reciprocal crossregulation has been found between the cGMP pathway and the calcium pathway36. This regulation is timely controlled whereas hypocotyl elongation is reduced by and only manifested in the presence of high amounts of signaling intermediates. The level of both factors. The antagonistic and the positive cGMP is also subjected to a desensitization process, which is potentially regulated by a neg- activity of sucrose on the phyA pathway can ative feedback loop of the cGMP-activated pathway. The activity of the phytochrome A be blocked in Arabidopsis sun mutants23. This pathway is regulated near the photoreceptor by the PSI2 protein14. Induction of the PR1a uncoupling identifies transduction elements of gene through salicylic acid signaling is probably modulated by the phytochrome signal the sucrose pathway, which are responsible for because an elevated expression of PR genes is found in the phytochrome A and B signaling the interaction with the phyA-controlled light mutant psi2 under high light intensities14. The phyA receptor can phosphorylate the blue- 19 signal transduction pathway (SUN proteins23). light receptor and therefore modulate the blue-light perception . Sucrose inhibits light- 23 Such interactions presuppose the existence of responsive genes via a pathway involving SUN proteins . The broken lines represent common elements integrating the signal pathways that are only active above a certain level of signal. converging from both pathways, either additively (for the inhibition of hypocotyl elongation) or substractively (for the activation of PC Such a system would integrate internal as well • Phytochrome A and B signaling pathways. and CAB genes). It remains to be determined as environmental signals to modulate the • Blue-light receptor pathway. whether SUN proteins are such elements, or if activity of the various metabolite biosynthesis • Circadian clock. they simply interact with these elements. pathway. • Sucrose and gibberellin pathways. A major challenge will be to functionally Crosstalk between amino acids Crosstalk in the control of flowering characterize these interactions and the corre- and purine metabolism In Arabidopsis, flowering induction is sponding elements forming such a complex The various amino acid metabolisms are inter- controlled by a complex system of signaling network. connected, and can be linked up to the purine pathways acting in partial redundancy, the metabolism24. Indeed, Arabidopsis plants signals of which are downstream-integrated by Signaling network: a neural network? treated with a histidine biosynthesis inhibitor a group of proteins, such as LFY and From a set of linear and separated signal trans- overexpress genes related to not only histidine AP1, which further cooperate additively to con- duction pathways, the model describing per- biosynthesis but also to aromatic amino acids, fer floral meristem identity (reviewed in Refs ception and information processing is now to lysine synthesis and, curiously, to purine 26–28). Multiple opportunities for crosstalk shifting towards a network-structured para- synthesis24. In addition, a reduction in glu- must occur in this system because Ͼ80 genes digm29. As a much higher level of complexity is tamine synthetase activity is observed. As in the have been found to influence the transition observed, new models are emerging to account case of other eukaryotes25, a general control sys- from vegetative to reproductive stage28. For for the properties of living cells. In line with tem might coordinate metabolite biosynthesis. example, the time of flowering is influenced by: the mechanistic representations adapted from

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in a single output (R). In signal transduction, Table 1. Examples of Boolean gates and logical integration the value 0 corresponds to no signal or a low of signals found in plant signal processinga signal and the value 1 indicates that a phe- nomenological significant signal is passing Type of gate Example Ref. through the pathway. Such a Boolean network model can serve AND See Fig. 1 as a starting point for a functional description of the network activity. If the signal level is OR CAB gene induction by red or far-red light. 37 determining, there is the possibility for further investigation of the quantitative ‘rule’ of signal NAND Switch controlling down-regulation of genes involved in vegetative 28 integration associated with the element by a development in the shoot apical meristem or inactivation of a separate examination. Using a similar proce- flowering inhibitor in this organ: input information might represent dure, every element of the network could be signals controlling the activity of a flowering inhibitor concomitantly characterized by a particular algorithm or rule. (such as LFY and AP1 signals). In the future, assembling these algorithms XOR Activity of red and far-red light in combination to control 38 or rules together in a neural network should cell elongation. lead to a useful simulation of the cell signal transduction apparatus. aThe gate types are described in Fig. 2. Conclusion An isomorphism between signaling and research into artificial intelligence, the also possible. For example, a phosphatase Boolean networks appears to be emerging. cell apparatus involved in internal or external activity might be modulated by two indepen- This provides a logical framework that allows signal interpretation can be considered a dent kinases. These two kinases could phos- a materialistic description of the flow of infor- molecular network. In this more realistic phorylate the enzyme at different sites, both mation in cells. It implies that Boolean (global) description, the structure of the modifications leading to a cumulative and switches have a molecular identity, presum- signaling network resembles a type of neural possibly non-linear effect on the phosphatase ably as proteins that are susceptible to various network called a perceptron30. activity. This implies that a signal-integrating modifications from convergent signals. More A perceptron is a group of interacting algo- protein molecule can be considered a small detailed information on pathways and cross- rithms (neurons) divided into at least three lay- computing network. talk are needed to fill the gaps in our knowl- ers: an input layer where the information is The ability to ‘memorize’ sets of conditions edge concerning signal processing. Molecular entered, an output layer where information is is a typical property of neural-like networks29,30. characterization of the individual elements of read after processing by the network, and an In plants, the maintenance of circadian rhythm the processing apparatus is a current challenge. intermediate layer linking output and input in darkness is an example of ‘memory’31. Therefore, future work should focus on an neurons. Information enters the network in the extensive characterization of the elements form of sigmoidal or gaussian signals, which Structure of signaling networks: the involved in given signaling pathways and are processed by the algorithm-containing Boolean network those linking these pathways in networks. The neurons to generate new sigmoidal or gaussian Overall, signaling networks are structured like use of DNA microarrays to associate signal- signals that will be treated by the next neurons neural networks. However, the use of such a ing networks with gene expression, and in the ‘cascade’. In such networks, fluctuating model to identify the molecular components genetic approaches based on transgenic plants information is divided into a set of arbitrary of a signal transduction network would restrict containing sets of reporter genes, should help components, which is transported and modi- advances in research because information- in this task. It might be possible to represent fied by the algorithms through a complex par- processing in neural networks is diffusely signal networks and crosstalk using models that allel processing. localized. Thus, for use with a genetic and, possess good predictive power. In the case of a biochemical network, the consequently, reductionistic approach, a sim- signal flowing through two molecular neurons pler model is needed. A Boolean representa- Acknowledgements can be represented as a pulse of cytoplasmic tion of signaling networks allows for a We thank Ted Farmer and Cris Kuhlemeier calcium or a change in the concentration of reductive and rational representation from for suggestions concerning the manuscript, cyclic nucleotides. The cell’s equivalent of a which experiments can be designed and a cer- and Dominique Genoud for helping us with molecular ‘neuron’ might be, for example, a tain predictive power gained. Indeed, interfering the concepts of artificial intelligence. Support particular phosphatase activity in the cyto- signals can be considered as ‘inputs’ reaching from the Swiss National Science Foundation plasm, which is modulated locally and tempo- a Boolean gate (or switch), and the signal that (grant FN 3100-055662.98) is gratefully rally by elevated calcium or cyclic nucleotide results from the combination can be defined acknowledged. concentrations. In this way, the quantitative as the ‘output’ of such a logical gate32. value or intensity of the calcium signal reach- For example, with two inputs, where the References ing such a molecular neuron would be trans- value 0 or 1 corresponds to the presence or the 1 Ryan, C.A. (1990) Protease inhibitors in plants: lated by the phosphatase-associated ‘algorithm’ absence of a signal, four combinations are genes for improving defenses against insectsand (i.e. the associated transduction rule) in a new possible: 00, 01, 10, 11. In this way, for two pathogens, Annu. Rev. Phytopathol. 28, 425–449 signal possessing its own intensity. For exam- signals, ‘a’ and ‘b’, converging from different 2 Farmer, E.E. and Ryan, C.A. (1992) ple, the generated signal could be the phos- pathways, and possibly modulated by a NOT Octadecanoid precursors of jasmonic acid phorylation rate of the downstream element. gate, there are six possible logical operations activate the synthesis of wound-inducible In perceptrons, one single neuron can inte- (Fig. 2, Table 1). These operations are called proteinase inhibitors, Plant Cell 4, 129–134 grate two or more different inputs. In the con- AND, OR, NAND, NOR, XOR and XNOR, 3 Sticher, L. et al. (1997) Systemic acquired text of cell perception, such integrations are each combining two afferent inputs (a and b) resistance, Annu. Rev. Phytopathol. 35, 235–270

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(1997) Sucrose control of repression of gene expression requires calcium synergistically induced by ethylene and methyl phytochrome A signalling in Arabidopsis, Plant and cGMP, EMBO J. 16, 2554–2564 jasmonate, Plant Cell 6, 1077–1085 Cell 9, 583–595 36 Bowler, C. et al. (1994) Phytochrome signal 8 O’Donnell, P.J. et al. (1996) Ethylene as a signal 24 Guyer, D. et al. (1995) Evidence for cross- transduction pathways are regulated by reciprocal mediating the wound response of tomato plants, pathway regulation of metabolic gene expression control mechanisms, Genes Dev. 8, 2188–2202 Science 274, 1914–1917 in plants, Proc. Natl. Acad. Sci. U. S. A. 92, 37 Millar, A.J. and Kay, S. (1996) Integration of 9 Penninckx, I.A. et al. (1998) Concomitant 4997–5000 circadian and phototransduction pathways in the activation of jasmonate and ethylene response 25 Kilberg, M.S. et al. (1994) Amino acid-regulated network controlling CAB gene transcription in pathways is required for induction of a plant gene expression in eukaryotic cells, FASEB J. 8, Arabidopsis, Proc. Natl. Acad. Sci. U. S. A. 93, defensin gene in Arabidopsis, Plant Cell 10, 13–19 15491–15496 2103–2113 26 Weigel, D. (1995) The genetics of flower 38 Smith, H. (1995) Physiological and ecological 10 Penninckx, I.A. et al. (1996) Pathogen-induced development: from floral induction to ovule function within the phytochrome family, systemic activation of a plant defensin gene in morphogenesis, Annu. Rev. Genetics 29, 19–39 Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, Arabidopsis follows a salicylic acid-independent 27 Koornneef, M. et al. (1998) Genetic control of 289–315 pathway, Plant Cell 8, 2309–2323 flowering time in Arabidopsis, Annu. Rev. Plant 11 Fluhr, R. (1998) Ethylene perception: from two- Physiol. Plant Mol. Biol. 49, 345–370 component signal transducers to gene induction, 28 Levy, Y.Y. and Dean, C. (1998) The transition to Thierry Genoud and Jean-Pierre Métraux Trends Plant Sci. 3, 141–146 flowering, Plant Cell 10, 1973–1989 are at the Département de Biologie, 12 Solano, R. and Ecker, J.R. (1998) Ethylene gas: 29 Bhalla, U. and Iyengar, R. (1999) Emergent Université de Fribourg, Switzerland. perception, signaling and response, Curr. Biol. 1, properties of networks of biological signalling (tel ϩ41 26 300 8810; 393–398 pathways, Science 283, 381–387 fax ϩ41 26 300 9740; 13 Zhou, L. et al. (1998) Glucose and ethylene 30 Bray, D. (1995) Protein molecules as e-mail signal transduction crosstalk revealed by an computational elements in living cells, Nature [email protected]; [email protected]). Arabidopsis glucose-insensitive mutant, Proc. 376, 307–312 Natl. Acad. Sci. U. S. A. 95, 10294–10299 14 Genoud, T. et al. (1998) An Arabidopsis mutant hypersensitive to red and far-red light signals, Plant Cell 10, 889–904 15 Casal, J.J. and Boccalandro, H. (1995) Co-action between phytochrome B and HY4 in Arabidopsis thaliana, Planta 197, 213–218 Trends in Plant Science Perspectives 16 Ahmad, M. and Cashmore, A.R. (1997) The blue-light receptor cryptochrome 1 shows Perspectives articles are your opportunity to express personal views on topics of functional dependence on phytochrome A or interest to plant scientists. The range of appropriate subject matter covers the breadth phytochrome B in Arabidopsis thaliana, Plant J. 11, 421–427 of plant biology: historical, philosophical or political aspects; potential links between 17 Casal, J.J. and Mazzella, M.A. (1998) hitherto disparate fields; or simply a new view on a subject of current importance. Conditional synergism between cryptochrome 1 Specific issues might include: the allocation of funding; commercial exploitation of data; and phytochrome B is shown by the analysis of the gene sequencing projects; genetic engineering; the impact of the internet; education phyA, phyB, and hy4 simple, double, and triple mutants in Arabidopsis, Plant Physiol. 118, issues; or public perception of science. Current developments in other disciplines may 19–25 also be relevant. 18 Neff, M.M. and Chory, J. (1998) Genetic Although Perspective articles are more opinionated in tone, they remain subject to interactions between phytochrome A, phytochrome B, and cryptochrome 1 during stringent peer-review to ensure clarity and accuracy. The decision to publish rests with Arabidopsis development, Plant Physiol. 118, the Editor. If you wish to write for the Perspectives section, please contact 27–36 the Editor before embarking on your manuscript, with a 200-word proposal and a list 19 Ahmad, M. et al. (1998) The CRY1 blue light photoreceptor of Arabidopsis interacts of key recent references ([email protected]). with phytochrome A in vitro, Mol. Cell 1, 939–948

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