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Jasmonate signalling in barley
Jasmonate signalling in barley In a recent review, Wastemack and Parthier’ discussed a model, originating from Farmer and Ryan’, for jasmonate-signalled gene expression in tomato. In order to broaden the discussion of jasmonate signal transduction, and to highlight differences between experimental systems, we would like to present a model for jasmonate signalling and activation of jasmonate-responsive genes (jrgs) in barley. Jasmonic acid and its methyl ester have been shown to have a variety of physiological effects in different species, including involvement in developmental processe?, defence in response to insects“.’ and, possibly, responses to pathogens, wounding and desiccation’. In the Farmer and Ryan model’, environmental stimuli are perceived at receptors on the plasma membrane and trigger the biosynthesis of jasmonate, which is then recognized by an intracellular receptor. A signal cascade then leads to the activation ofjrgs, and their products are responsible for the physiological response. Elevation of the amount of endogenous jasmonate in potato by overexpression of a chloroplast allene oxide synthase failed to induce the jrg pin2, probably because of
Fig. 1. Northern blot analyses of the expression of jasmonate-responsive genes (jrgs). Barley leaf segments were floated on 90 pM abscisic acid (ABA), water, 45 pM jasmonic acid methyl ester (JAME) or sorbitol (1 M); 20 pg of total RNA was used from each treatment. The blots were hybridized to the cDNA probes “.” indicated.
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1998, Vol. 3, No. 1
Fig. 2. Model of jasmonate signal transduction in barley. Exogenously applied jasmonic acid methyl ester (JAME) may be either taken up or recognized by a plasma membrane-localized receptor (pR). Endogenous jasmonic acid (JA) may interact with a cytoplasmic receptor (CR) and activate a signal cascade different from the one initiated by pR. Individual sets of JAresponsive genes (jugs) are induced consecutively. jrgl and genes encoding the JA-induced proteins JIP23, JIP37 and JIP66 (collectively labelled JIP) are triggered by endogenous and exogenous JA, whereas jrg5, jrgl0 and jrgl2, encoding a caffeic acid methyltransferase (COMT), a chalcone synthase homologue (CHS) and a protein of unknown function, respectively, are induced by exogenous JAME. Exogenously supplied abscisic acid (ABA) induces expression of those jrgs encoding JIP23, JIP37 and JIP66. Sorbitol will increase the endogenous content of both JA and ABA; the JIPs (e.g. JIP23) are induced by endogenous JA but not byendogenous ABA.
jasmonate sequestratior+. In contrast, flotation of barley leaf segments on sorbitol solution increased both the amount of endogenous jasmonate and subsequent expression ofjrgl and genes encoding the jasmonate-induced proteins JIP23, JIP37 and JIP66 (Fig. 1; Ref. 7). However, other osmotica (2-desoxyglucose or O-methylglucose) of identical osmolality failed to induce jrgs, indicating that it was not osmotic stress that was involved’. Otherjrgs do not respond to the endogenous jasmonate triggered by sorbitol treatment, but are induced after application of jasmonate’ (Fig. 1). All these genes show a similar dose response for methyl jasmonate’, and thus jasmonate sensitivity cannot be the cause of the differential expression pattern. One model to explain the observations is that exogenous jasmonate is recognized by a plasma membrane receptor (as with the perception of ethylene”‘) and that endogenous jasmonate is recognized by an intracellular, probably cytoplasmic. receptor (Fig. 2). Each signal-transduction cascade will lead to the expression of distinctjrgs. Although certain jrgs respond only to exogenous jasmonate (jrg.5, jrgl0 and jrgl2; Fig. l), it is difficult to assess whether others respond exclusively to the endogenous compound. The observed response pattern of jrgs cannot simply be explained by sequestration of jasmonate within subcellular compartments, because some of the genes are induced by endogenous Coovrioht
0 1998
Elsevier
and exogenous jasmonate Cjrgl and genes encoding JIP23, JIP37 and JIP66), whereas others are induced only by exogenous jasmonate (jrg5, jrgl0 and jrgl2). Also, tissue-specific expression of the jrgs requires either distinct signal-transduction pathways for jasmonate or tissue-specific jasmonate biosynthesis. As an alternative to the existence of two jasmonate-signalling pathways, it could be that there is an additional signal that is required for the expression of jrgs by endogenous jasmonate or that an inhibitor prevents the expression of certain jrgs. Likewise the absence of pin2 expression, despite a high amount of endogenous jasmonate, suggests a requirement for additional cues such as mechanical damage or water stres8. In addition to the differential recognition of exogenous and endogenous jasmonate signals, the situation in barley is further complicated by an increase in the concentration of endogenous abscisic acid (ABA) after sorbitol treatment’. Exogenous ABA induces the expression of several jrgs [JIP6, JIP23, JIP37 and JIP66 (but not jrgl, jrg5, jrgl0 or jrgIZ)]“, but endogenous ABA does not”. Therefore, it appears unlikely that the ABA signal is mediated through a jasmonate signal cascade, as in tomato’, and instead must act independently. The observation that exogenous ABA induces specific jrgs might be caused by the existence Science
Ltd. All riahts
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correspondence of ABA- andjasmonate-responsive elements in the same promoter, or the presence of individual ABA- or jasmonate-regulated genes within genefamilies. In our preferred model (Fig. 2), ABA signalling is independentof jasmonate signalling, and the induction ofjqs is caused by the presence of gene families, some members of which are individually induced by either ABA or jasmonate. Jasmonate signalling is mediatedthrough two pathways, one sensing extracellular jasmonate and the other sensing intracellular jasmonate. Marian Lijbler* and Justin lnstitut fijr Pflanzenbiochemie, D-06120 Halle, Germany
Lee Weinberg
References 1 Wastemack, C. and Ptihier, B. (1997) Jasmonate-signalled plant gene expression, Plant
Sci. 2.302-307
Annu.
Rev. Plant
Physiol.
Plant
Mol.
Biol.
48,
355-381 4 Howe, G.A. et al. (1996) An octadecanoid pathway mutant (X.5) of tomato is compromised in signaling for defense against insect attack, Plant
Gel/ 8, 2067-2077
5 McCann, M. et al. (1997) Jasmonate is essential for insect defense in Arabidopsis, Proc. Natl. Acad.
3,
*Author for correspondence (tel+49 345 5582 253; fax +49 345 5582 166; e-mail mloeblerQipb.uni-halle.de).
Trends
2 Farmer, E.E. and Ryan, C.A. (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors, Planr Cell 4, 129-134 3 Creelman, R.A. and Mullet, J.E. (1997) Biosynthesis and action of jasmonates in plants,
Sci. Ii. S. A. 94, 5473-5471
6 Harms, K. et al. (1995) Expression of a flax allene oxide synthase cDNA leads to increased endogenous jasmonic acid (JA) levels in transgenic potato plants but not to a corresponding activation of JA-responding genes, Plant Cell 7, 1645-1654 7 Lehmann. J. et al. (1995) Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments, Planta 197, 156-l 62
Forthcoming articles in Trends in Plant Science Glutamate synthase and nitrogen assimilation, S.J. Temple, C. P. Vance and J.S. Gantt Ozone: an abiotic elicitor of plant defence reactions, H. Sandermann, Jr, D. Ernst, W. Heller and C. Langebalfels Improving stress tolerance in plants by gene transfer, N. Holmbergand L. Billow
8 Lee, J. ef al. (1997) Methyl jasmonate induces an O-methyl-transferase in barley, Plant Cell Physiol. 38, 85 l-862 9 Kramell, R. et al. (1997) Amino acid conjugates of jasmonic acid induce jasmonate-responsive gene expression in barley (Ho&urn m&are L.) leaves, FEBS Len. 414. 197-202 10 Ecker. J.R. (1995) The ethylene signal transduction pathway in plants, Science 268, 667-675 11 Lee, J., Patthier. B. and LBbler. M. (1996) Jasmonate signalling can be uncoupled from ABA signalling in barley: identification of jasmonate-regulated transcripts that are not induced by ABA, Planta 199, 625-632 12 Wasternack, C. et al. (1994) Relationship between jasmonate and ABA in JIP gene expression of barley (Hordeurn vulgare cv. Salome), Russ. J. Plant Physiol. 4 1, 6046 12 13 Andresen, I. et al. (1992) The identification of a leaf thionin as one of the main jasmonateinduced proteins of barley (Hordeurn vulgare), Plant Mol. Biol. 19, 193-204
Letters to Trends in Plant Science Correspondence in Trends in P/ant Science may address topics raised in very recent issues of the magazine, or other matters of general current interest to plant scientists. Letters should be sent, together with a disk copy (preferably Word for Mac) to the Editor (or e-mail your text to [email protected]). The decision to publish rests with the Editor, and the author(s) of any Trends in Plant Science article criticized in a Letter will nomally be invited to reply.
The protein translocation apparatus of chloroplast envelopes, L. Heins, 1. Collinsonand J. Sol/
January 1998, Vol. 3, No. 1
9
Fig. 1. Northern blot analyses of the expression of jasmonate-responsive genes (jrgs). Barley leaf segments were floated on 90 pM abscisic acid (ABA), water, 45 pM jasmonic acid methyl ester (JAME) or sorbitol (1 M); 20 pg of total RNA was used from each treatment. The blots were hybridized to the cDNA probes “.” indicated.
8
January
1998, Vol. 3, No. 1
Fig. 2. Model of jasmonate signal transduction in barley. Exogenously applied jasmonic acid methyl ester (JAME) may be either taken up or recognized by a plasma membrane-localized receptor (pR). Endogenous jasmonic acid (JA) may interact with a cytoplasmic receptor (CR) and activate a signal cascade different from the one initiated by pR. Individual sets of JAresponsive genes (jugs) are induced consecutively. jrgl and genes encoding the JA-induced proteins JIP23, JIP37 and JIP66 (collectively labelled JIP) are triggered by endogenous and exogenous JA, whereas jrg5, jrgl0 and jrgl2, encoding a caffeic acid methyltransferase (COMT), a chalcone synthase homologue (CHS) and a protein of unknown function, respectively, are induced by exogenous JAME. Exogenously supplied abscisic acid (ABA) induces expression of those jrgs encoding JIP23, JIP37 and JIP66. Sorbitol will increase the endogenous content of both JA and ABA; the JIPs (e.g. JIP23) are induced by endogenous JA but not byendogenous ABA.
jasmonate sequestratior+. In contrast, flotation of barley leaf segments on sorbitol solution increased both the amount of endogenous jasmonate and subsequent expression ofjrgl and genes encoding the jasmonate-induced proteins JIP23, JIP37 and JIP66 (Fig. 1; Ref. 7). However, other osmotica (2-desoxyglucose or O-methylglucose) of identical osmolality failed to induce jrgs, indicating that it was not osmotic stress that was involved’. Otherjrgs do not respond to the endogenous jasmonate triggered by sorbitol treatment, but are induced after application of jasmonate’ (Fig. 1). All these genes show a similar dose response for methyl jasmonate’, and thus jasmonate sensitivity cannot be the cause of the differential expression pattern. One model to explain the observations is that exogenous jasmonate is recognized by a plasma membrane receptor (as with the perception of ethylene”‘) and that endogenous jasmonate is recognized by an intracellular, probably cytoplasmic. receptor (Fig. 2). Each signal-transduction cascade will lead to the expression of distinctjrgs. Although certain jrgs respond only to exogenous jasmonate (jrg.5, jrgl0 and jrgl2; Fig. l), it is difficult to assess whether others respond exclusively to the endogenous compound. The observed response pattern of jrgs cannot simply be explained by sequestration of jasmonate within subcellular compartments, because some of the genes are induced by endogenous Coovrioht
0 1998
Elsevier
and exogenous jasmonate Cjrgl and genes encoding JIP23, JIP37 and JIP66), whereas others are induced only by exogenous jasmonate (jrg5, jrgl0 and jrgl2). Also, tissue-specific expression of the jrgs requires either distinct signal-transduction pathways for jasmonate or tissue-specific jasmonate biosynthesis. As an alternative to the existence of two jasmonate-signalling pathways, it could be that there is an additional signal that is required for the expression of jrgs by endogenous jasmonate or that an inhibitor prevents the expression of certain jrgs. Likewise the absence of pin2 expression, despite a high amount of endogenous jasmonate, suggests a requirement for additional cues such as mechanical damage or water stres8. In addition to the differential recognition of exogenous and endogenous jasmonate signals, the situation in barley is further complicated by an increase in the concentration of endogenous abscisic acid (ABA) after sorbitol treatment’. Exogenous ABA induces the expression of several jrgs [JIP6, JIP23, JIP37 and JIP66 (but not jrgl, jrg5, jrgl0 or jrgIZ)]“, but endogenous ABA does not”. Therefore, it appears unlikely that the ABA signal is mediated through a jasmonate signal cascade, as in tomato’, and instead must act independently. The observation that exogenous ABA induces specific jrgs might be caused by the existence Science
Ltd. All riahts
resewed.
1360 - 13W9WH9.00
correspondence of ABA- andjasmonate-responsive elements in the same promoter, or the presence of individual ABA- or jasmonate-regulated genes within genefamilies. In our preferred model (Fig. 2), ABA signalling is independentof jasmonate signalling, and the induction ofjqs is caused by the presence of gene families, some members of which are individually induced by either ABA or jasmonate. Jasmonate signalling is mediatedthrough two pathways, one sensing extracellular jasmonate and the other sensing intracellular jasmonate. Marian Lijbler* and Justin lnstitut fijr Pflanzenbiochemie, D-06120 Halle, Germany
Lee Weinberg
References 1 Wastemack, C. and Ptihier, B. (1997) Jasmonate-signalled plant gene expression, Plant
Sci. 2.302-307
Annu.
Rev. Plant
Physiol.
Plant
Mol.
Biol.
48,
355-381 4 Howe, G.A. et al. (1996) An octadecanoid pathway mutant (X.5) of tomato is compromised in signaling for defense against insect attack, Plant
Gel/ 8, 2067-2077
5 McCann, M. et al. (1997) Jasmonate is essential for insect defense in Arabidopsis, Proc. Natl. Acad.
3,
*Author for correspondence (tel+49 345 5582 253; fax +49 345 5582 166; e-mail mloeblerQipb.uni-halle.de).
Trends
2 Farmer, E.E. and Ryan, C.A. (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors, Planr Cell 4, 129-134 3 Creelman, R.A. and Mullet, J.E. (1997) Biosynthesis and action of jasmonates in plants,
Sci. Ii. S. A. 94, 5473-5471
6 Harms, K. et al. (1995) Expression of a flax allene oxide synthase cDNA leads to increased endogenous jasmonic acid (JA) levels in transgenic potato plants but not to a corresponding activation of JA-responding genes, Plant Cell 7, 1645-1654 7 Lehmann. J. et al. (1995) Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments, Planta 197, 156-l 62
Forthcoming articles in Trends in Plant Science Glutamate synthase and nitrogen assimilation, S.J. Temple, C. P. Vance and J.S. Gantt Ozone: an abiotic elicitor of plant defence reactions, H. Sandermann, Jr, D. Ernst, W. Heller and C. Langebalfels Improving stress tolerance in plants by gene transfer, N. Holmbergand L. Billow
8 Lee, J. ef al. (1997) Methyl jasmonate induces an O-methyl-transferase in barley, Plant Cell Physiol. 38, 85 l-862 9 Kramell, R. et al. (1997) Amino acid conjugates of jasmonic acid induce jasmonate-responsive gene expression in barley (Ho&urn m&are L.) leaves, FEBS Len. 414. 197-202 10 Ecker. J.R. (1995) The ethylene signal transduction pathway in plants, Science 268, 667-675 11 Lee, J., Patthier. B. and LBbler. M. (1996) Jasmonate signalling can be uncoupled from ABA signalling in barley: identification of jasmonate-regulated transcripts that are not induced by ABA, Planta 199, 625-632 12 Wasternack, C. et al. (1994) Relationship between jasmonate and ABA in JIP gene expression of barley (Hordeurn vulgare cv. Salome), Russ. J. Plant Physiol. 4 1, 6046 12 13 Andresen, I. et al. (1992) The identification of a leaf thionin as one of the main jasmonateinduced proteins of barley (Hordeurn vulgare), Plant Mol. Biol. 19, 193-204
Letters to Trends in Plant Science Correspondence in Trends in P/ant Science may address topics raised in very recent issues of the magazine, or other matters of general current interest to plant scientists. Letters should be sent, together with a disk copy (preferably Word for Mac) to the Editor (or e-mail your text to [email protected]). The decision to publish rests with the Editor, and the author(s) of any Trends in Plant Science article criticized in a Letter will nomally be invited to reply.
The protein translocation apparatus of chloroplast envelopes, L. Heins, 1. Collinsonand J. Sol/
January 1998, Vol. 3, No. 1
9