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

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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 re- duction 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 wound- ing 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 1360 - 1385/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(99)01498-3 December 1999, Vol. 4, No. 12 503 trends in plant science perspectives (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
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