Jasmonates: Synthesis, Metabolism, Signal Transduction and Action

Claus Wasternack, Palacký University, Olomouc, Czech Republic

Published online: July 2016

DOI: 10.1002/9780470015902.a0020138.pub2

Abstract

Jasmonic acid and other fatty‐acid‐derived compounds called oxylipins are signals in stress responses and development of plants. The receptor complex, signal transduction components as well as repressors and activators in jasmonate‐induced gene expression have been elucidated. Different regulatory levels and cross‐talk with other hormones are responsible for the multiplicity of plant responses to environmental and developmental cues.

Key Concepts

  • Jasmonates are important signalling compounds in plant stress responses and development.
  • Jasmonates are lipid‐derived signals.
  • Active and inactive jasmonates are generated by metabolic conversion.
  • Key components of jasmonate perception and signalling have been elucidated.
  • There is an increasing number of repressors, co‐repressors, adaptors and activators (transcription factors) in JA‐Ile‐induced gene expression

Keywords: jasmonates; biosynthesis; metabolism; signalling; cross‐talk; activators and repressors of transcription; herbivory; development

Figure 1. Metabolic conversion of JA. Methylation to JA‐Me, JA glucosyl ester formation, decarboxylation to cis‐jasmone, hydroxylation to 12‐OH‐JA, sulfation of 12‐OH‐JA, O‐glucosylation of 12‐OH‐JA, conjugation with amino acids, preferentially isoleucine to give JA‐Ile, methylation to JA‐Me‐Ile, 12‐hydroxylation of JA‐Ile, carboxylation of 12‐OH‐JA‐Ile, O‐glucosylation of JA‐Ile and JA‐Ile glucosyl ester formation are indicated, together with the known enzymes involved: JAR1 – jasmonoyl isoleucine synthetase; JA‐Ile‐12‐hydroxylase CYP94B3, 12‐OH‐JA‐Ile carboxylase CYP94C1, amidohydrolases IAR3 and ILL6; JMT, JA methyl transferase; ST2a, 12‐OH‐JA sulfotransferase. The lactone of 12‐OH‐JA‐Ile was added even its detection for plants is missing so far. Biologically inactive compounds are outlined with solid lines (───), partially active compounds are outlined with dashed lines (‐ ‐ ‐) and active compounds are outlined with dotted lines (·····). Modified with permission from Wasternack and Strnad © Elsevier.
Figure 2. Model of JA‐Ile perception via the SCFCOI1–JAZ co‐receptor complex and regulation of JA‐induced gene expression. JA/JA‐Ile perception by the SCFCOI1–JAZ co‐receptor complex leads to JA/JA‐Ile‐induced gene expression. MYC2, which binds to the G‐box of a JA/JA‐Ile‐responsive gene, is repressed by negative regulators such as JAZs. NINJA and TOPLESS (TPL), which act via histone deacetylase6 (HDA6) and HDA19, function as co‐repressors. Jasmonate‐associated VQ motif gene 1 (JAV1) acts in addition to JAZ as a repressor (left‐hand side), whereas JAMs (jasmonate associated MYC2‐LIKE1, JAM2, JAM3) (right‐hand side) compete with MYC2 on binding to the G‐box. JAZs and JAV1 are ubiquitinylated and subjected to proteasomal degradation. MYC2 can then switch on transcription of JA/JA‐Ile‐responsive genes, including early genes such as JAZs and MYC2. MED25, subunit 25 of the mediator complex, mediates transcription. Ub, ubiquitin. E2, Rbx, Cullin, ASK1, and the F‐box protein COI1 are components of the SCF‐complex; ZIM domain (Z), Jas domain (J), EAR domain (E). Modified with permission from Wasternack and Strnad © Elsevier.
Figure 3. Scheme on cross‐talk between JA signalling and ubiquitination (a), between JA and SA (b), between JA and ET (c) and between JA and GA (d). PIFs, phytochrome interacting factors; ERF1, ET response factor1; EIN1, ET insensitive1; ETR, ET receptor; NPR1, nonexpressor of pathogenesis‐related genes; GRX, glutaredoxin; TGA, transcription factor; ICE, inducer of CBF expression‐C‐repeat binding factor1; RGLG, ring domain ligase; cf. legend of Figure for further details.
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References

Brash AR (2009) Mechanistic aspects of CYP74 allene oxide synthases and related cytochrome P450 enzymes. Phytochemistry 70: 1522–1531.

Caarls L, Pieterse CMJ and Van Wees SCM (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Frontiers in Plant Science 6: 170.

De Geyter N, Gholami A, Goormachtig S, et al. (2012) Transcriptional machineries in jasmonate‐elicited plant secondary metabolism. Trends in Plant Science 17: 349–359.

Dobritzsch S, Weyhe M, Schubert R, et al. (2015) Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses. BMC Biology 13: 28.

Farmer EE (2001) Surface‐to‐air signals. Nature 411: 854–856.

Farmer EE (2014) Leaf Defence. Oxford: Oxford University Press.

Fonseca S, Chini A, Hamberg M, et al. (2009) (+)‐7‐Iso‐jasmonoyl‐L‐isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344–350.

Fu ZQ and Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64: 839–863.

Gasperini D, Chauvin A, Acosta IF, et al. (2015a) Axial and radial oxylipin transport. Plant Physiology 169: 2244–2254.

Gasperini D, Chételat A, Acosta IF, et al. (2015b) Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genetics 11: e1005300.

Gimenez‐Ibanez S, Boter M and Solano R (2015) Novel players fine‐tune plant trade‐offs. Essays in Biochemistry 58: 83–100.

Hannapel DJ (2010) A model system of development regulated by the long‐distance transport of mRNA. Journal of Integrative Plant Biology 52: 40–52.

Havko N, Major I, Jewell J, et al. (2016) Control of carbon assimilation and partitioning by jasmonate: an accounting of growth–defense tradeoffs. Plants 5: 7.

Heitz T, Widemann E, Lugan R, et al. (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonoyl‐isoleucine for catabolic turnover. Journal of Biological Chemistry 287: 6296–6306.

Howe GA and Browse J (2007) Jasmonate Synthesis and Action in Higher Plants(eLS). Chichester: John Wiley & Sons Ltd. http://www.els.net. DOI: 10.1002/9780470015902.a0020138.

Huot B, Yao J, Montgomery B, et al (2014) Different shades of JAZ during plant growth and defense. Molecular Plant 7: 1267–1287.

Kazan K and Manners JM (2011) The interplay between light and jasmonate signalling during defence and development. Journal of Experimental Botany 62: 4087–4100.

Koo AJK, Cooke TF and Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl‐L‐isoleucine. Proceedings of the National Academy of Sciences of the United States of America 108: 9298–9303.

Koo AJK and Howe GA (2012) Catabolism and deactivation of the lipid‐derived hormone jasmonoyl‐isoleucine. Frontiers in Plant Science 3: 19.

Larrieu A, Champion A, Legrand J, et al. (2015) A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants. Nature Communications 6. DOI: 10.1038/ncomms7043

Lee D‐S, Nioche P, Hamberg M, et al. (2008) Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455: 363–368.

Mandaokar A, Thines B, Shin B, et al. (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant Journal 46: 984–1008.

Miersch O, Neumerkel J, Dippe M, et al. (2008) Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch‐off in jasmonate signaling. New Phytologist 177: 114–127.

Mousavi SAR, Chauvin A, Pascaud F, et al. (2013) GLUTAMATE RECEPTOR‐LIKE genes mediate leaf‐to‐leaf wound signalling. Nature 500: 422–426.

Nagels Durand A, Pauwels L and Goossens A (2016) The ubiquitin system and jasmonate signaling. Plants 5: 6.

Newie J, Andreou A, Neumann P, et al. (2016) Crystal structure of a lipoxygenase from Cyanothece sp. may reveal novel features for substrate acquisition. Journal of Lipid Research 57: 276–287.

Pieterse CMJ, van der Does D, Zamioudis C, et al. (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28: 489–521.

Pieterse CMJ, Zamioudis C, Berendsen R, et al. (2014) Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology 52: 347–375.

Pozo MJ, López‐Ráez JA, Azcón‐Aguilar C, et al. (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytologist 205: 1431–1436.

Saito H, Oikawa T, Hamamoto S, et al. (2015) The jasmonate‐responsive GTR1 transporter is required for gibberellin‐mediated stamen development in Arabidopsis. Nature Communications 6: 6095.

Schaller A and Stintzi A (2009) Enzymes in jasmonate biosynthesis – structure, function, regulation. Phytochemistry 70: 1532–1538.

Shah J and Zeier J (2013) Long‐distance communication and signal amplification in systemic acquired resistance. Frontiers in Plant Science 4: 30.

Sharma M and Laxmi A (2016) Jasmonates: emerging players in controlling temperature stress tolerance. Frontiers in Plant Science 6: 1129.

Sheard LB, Tan X, Mao H, et al. (2010) Jasmonate perception by inositol‐phosphate‐potentiated COI1‐JAZ co‐receptor. Nature 468: 400–405.

Song S, Qi T, Wasternack C, et al. (2014) Jasmonate signaling. Current Opinion of Plant Biology 21: 112–119.

Staswick PE and Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16: 2117–2127.

Wasternack C and Kombrink E (2010) Jasmonates: structural requirements for lipid‐derived signals active in plant stress responses and development. ACS Chemical Biology 5: 63–77.

Wasternack C and Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111: 1021–1058.

Wasternack C (2014a) Action of jasmonates in plant stress responses and development – applied aspects. Biotechnology Advances 32: 31–39.

Wasternack C (2014b) Jasmonates in plant growth and stress responses. In: Tran L‐S and Pal S (eds) Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications. New York, Heidelberg, Dordrecht, London: Springer.

Wasternack C (2015) How jasmonates earned their laurels: past and present. Journal of Plant Growth Regulation 34: 761–794.

Wasternack C and Strnad M (2015) Jasmonate signaling in plant stress responses and development – active and inactive compounds. New Biotechnology. DOI: 10.1016/j.nbt.2015.11.001.

Westfall CS, Zubieta C and Herrmann J (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336: 1708–1711.

Zhang F, Yao J and Ke J (2015a) Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 525: 269–273.

Further Reading

Acosta IF, Gasperini D, Chételat A, et al. (2013) Role of NINJA in root jasmonate signaling. Proceedings of the National Academy of Sciences of the United States of America 110: 15473–15478.

Davière J‐M and Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Molecular Plant 9: 10–20.

Hilker M, Schwachtje J, Baier M, et al. (2015) Priming and memory of stress responses in organisms lacking a nervous system. Biological Reviews. DOI: 101111/brv.12215.

Poelman EH and Kessler A (2016) Keystone herbivores and the evolution of plant defenses. Trends in Plant Science 21: 477–485. DOI: 10.1016/j.tplants.2016.01.007.

Schuman MC and Baldwin IT (2016) The layers of plant responses to insect herbivores. Annual Review of Entomology 61: 373–394.

Smakowska E, Kong J, Busch W, et al. (2016) Organ‐specific regulation of growth‐defense tradeoffs by plants. Current Opinion in Plant Biology 29: 129–137.

Yan C and Xie D (2015) Jasmonate in plant defence: sentinel or double agent? Plant Biotechnology Journal 13: 1233–1240.

Yang Y, Li L and Qu L‐J (2016) Plant Mediator complex and its critical functions in transcription regulation. Journal of Integrative Plant Biology 58: 106–118.

Yuan Z and Zhang D (2015) Roles of jasmonate signalling in plant inflorescence and flower development. Current Opinion in Plant Biology 27: 44–51.

Zhang X‐C, Millet YA, Cheng Z, et al. (2015b) Jasmonate signalling in Arabidopsis involves SGT1b–HSP70–HSP90 chaperone complexes. Nature Plants 1: 15049.

Zhou M and Memelink J (2016) Jasmonate‐responsive transcription factors regulating plant secondary metabolism. Biotechnology Advances 34: 441–449. DOI: 10.1016/j.biotechadv.2016.02.004.

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Article Title: Jasmonates: Synthesis, Metabolism, Signal Transduction and Action
 
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Wasternack, Claus(Jul 2016) Jasmonates: Synthesis, Metabolism, Signal Transduction and Action. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020138.pub2]