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Review
. 2013 Jun;111(6):1021-58.
doi: 10.1093/aob/mct067. Epub 2013 Apr 4.

Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany

C Wasternack  1 , B Hause
Affiliations
Review

Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany

C Wasternack et al. Ann Bot. 2013 Jun.

Abstract

Background: Jasmonates are important regulators in plant responses to biotic and abiotic stresses as well as in development. Synthesized from lipid-constituents, the initially formed jasmonic acid is converted to different metabolites including the conjugate with isoleucine. Important new components of jasmonate signalling including its receptor were identified, providing deeper insight into the role of jasmonate signalling pathways in stress responses and development.

Scope: The present review is an update of the review on jasmonates published in this journal in 2007. New data of the last five years are described with emphasis on metabolites of jasmonates, on jasmonate perception and signalling, on cross-talk to other plant hormones and on jasmonate signalling in response to herbivores and pathogens, in symbiotic interactions, in flower development, in root growth and in light perception.

Conclusions: The last few years have seen breakthroughs in the identification of JASMONATE ZIM DOMAIN (JAZ) proteins and their interactors such as transcription factors and co-repressors, and the crystallization of the jasmonate receptor as well as of the enzyme conjugating jasmonate to amino acids. Now, the complex nature of networks of jasmonate signalling in stress responses and development including hormone cross-talk can be addressed.

Keywords: COI1; JA in development; JA signalling; JAZ; Jasmonic acid; SCF; enzymes in biosynthesis and metabolism; light regulation; oxylipins; perception; responses to herbivores and pathogens; symbiotic interaction.

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Figures

Fig. 1.
Fig. 1.
Synthesis of jasmonic acid (JA)/JA-Ile from α-linolenic acid generated from galactolipids. Enzymes which have been crystallized are given in yellow boxes. Steps impaired in mutants of Arabidopsis (green) or tomato (red) are indicated. acx1, acyl-CoA-oxidase1; AOC, allene oxide cyclase; AOS, allene oxide synthase; coi1, coronatine insensitive1; dad1, delayed anther dehiscence1; 13-HPOT, (13S)-hydroperoxyoctadecatrienoic acid; jai1, jasmonic acid insensitive1; JAR1, JA-amino acid synthetase; α-LeA, α-linolenic acid; 13-LOX, 13-lipoxygenase; myc2, bHLHzip transcription factor MYC2; OPR3, OPDA reductase3; OPC-8, 3-oxo-2-( 2-pentenyl)-cyclopentane-1-octanoic acid; cis-(+)-OPDA; cis-(+)-12-oxophytodienoic acid; PLA1, phospholipase A1.
Fig. 2.
Fig. 2.
Metabolic fate of jasmonic acid (JA) and JA-Ile. Enzymes which have been cloned are given in grey. JAR1, JA-amino acid synthetase; JMT, JA methyl transferase; ST2A, sulfotransferase 2A.
Fig. 3.
Fig. 3.
Jasmonic acid (JA) perception via the COI1–JAZ co-receptor complex – mechanisms in JA-induced gene expression. In the resting state (left, low JA-Ile level), the binding of MYC2 to a G-box within the promoter of a JA-responsive gene does not activate transcription due to binding of the repressors Jasmonate ZIM domain proteins (JAZs) to MYC2. The co-repressors Novel Interactor of JAZ (NINJA) bound to JAZs, and TOPLESS (TPL) repress transcription via HISTONE DEACETYLASE 6 (HDA6) and HDA19. Upon stimulation (right, high JA-Ile level), JAZs are recruited by COI1 and subjected to ubiquitinylation and subsequent degradation by the 26S proteasome. Subsequently, MYC2 can activate transcription of early JA-responsive genes such as those encoding JAZ and MYC2. Transcription is mediated by the subunit 25 of Mediator complex (MED25; see section 4). ASK1, Arabidopsis SKP1 (S-phase kinase-associated protein 1) homologue; CUL, CULLIN; E2, ubiquitin-conjugating enzyme; MYC2, bHLHzip transcription factor; RBX, RING-H2 protein; SCF-complex, complex consisting of Skp1, Cullin-1 and F-box protein; Ub, ubiquitin.
Fig. 4.
Fig. 4.
The domain structure of MYC2, Jasmonate ZIM domain proteins (JAZ) and Novel Interactor of JAZ (NINJA) (A) and a hypothetical scheme of interaction between MYC2, JAZ, NINJA and TOPLESS (TPL) (B). Data adapted from Pauwels and Goossens (2011). B, conserved protein domain of NINJA; bHLH, DNA binding domain of MYC2; C, conserved protein domain of NINJA mediating binding to ZIM of JAZ; EAR, ethylene-responsive element binding factor-associated amphiphilic repression motif of NINJA-mediating binding to TPL; Jas, domain of JAZ for binding to COI1, MYC and other TFs; JID, JAZ-interacting domain of MYC2; NT, binding domain of JAZ to other TFs; TAC, domain of MYC2 for homo- and heteromerization; ZIM, domain of JAZ for binding to NINJA and for homo- and heteromerization.
Fig. 5.
Fig. 5.
The cross-talk between jasmonate (JA), ethylene (ET) and abscisic acid (ABA) triggered in response to herbivorous insects and necrotrophic pathogens (adapted from Pieterse et al., 2012). Attack by herbivorous insects induces JA- and ABA-dependent signalling pathways, whereas infections by necrotrophic pathogens induce JA- and ET-dependent signalling pathways. Both branches are antagonistically regulated. Solid lines, known interactions; dashed lines, hypothetical interactions; green arrows, positive effects; blue inhibition lines, negative effects. Compounds are given in rectangles, transcriptional regulators in circles, regulated genes in purple. ERF1, ethylene response factor 1; ORA59, octadecanoid-responsive Arabidopsis AP2/ERF-domain protein 59; PYL4, PYR1-like protein 4 (ABA receptor); other acronyms are given in Fig. 3.
Fig. 6.
Fig. 6.
Cross-talk between jasmonic acid (JA)- and gibberellic acid (GA)-signalling pathways in stamen maturation and during growth and defence processes. In stamen, DELLA negatively affects the expression of genes encoding JA biosynthetic enzymes. An increase in GA will result in the removal of DELLA leading to enhanced synthesis of JA/JA-Ile. In turn, this induces the expression of MYB21/24, which is crucial for stamen maturation. In vegetative tissues, the DELLA-TF DELLA RGA-like (RGL) competes with MYC2 for binding to JAZ. With an increasing level of JA/JA-Ile, MYC2 is released and mediates the transcription of not only JA-regulated genes involved in defence but also encoding RGL. An increase in RGL will amplify the defence response by recruiting Jasmonate ZIM domain protein (JAZ) followed by release of MYC2. In contrast, accumulation of GA will lead to degradation of RGL, thereby releasing JAZ to inhibit MYC2. In parallel, GA activates the growth response via phytochrome interacting factor (PIF); other acronyms are given in Fig. 1.
Fig. 7.
Fig. 7.
Effects of arbuscular mycorrhization (AM) and root nodule symbiosis (RNS) on endogenous levels of jasmonates as well as the effects of modulated JA levels on AM and RNS in Medicago truncatula. Endogenous jasmonate levels are increased and remain unaffected in roots of AM and RNS plants, respectively. The application of jasmonic acid (JA) or wound-induced rise in JA results in enhanced AM, but no effects on RNS. Similarly, reduced JA levels in transformed ALLENE OXIDE CYCLASE (AOC)-RNAi roots suppress AM, but do not affect RNS.
Fig. 8.
Fig. 8.
The role of jasmonic acid (JA)/JA-Ile in plant development. JA induces root growth inhibition by stimulating auxin biosynthesis via anthranilate synthase α1 (ASA1) and inhibiting the expression of genes encoding the TFs PLETHORA 1 (PLT1) and PLT2, which ensure the maintenance and activity of stem cells in the root. In tuber formation, jasmonates [JA, tuberonic acid (TA) and TA glucoside (TAG)] might act directly after their rise following activity of LIPOXYGENASE 1 (LOX1). However, most importantly levels of gibberellic acid (GA) are regulated by the combined action of the TFs BEL1-like 5 (BEL5) and POTATO HOMEOBOX 1 (POTH1) at the promoters of GA-20 oxidase-encoding genes. In trichome initialization, JA/JA-Ile act via the COI1 co-receptor complex to activate the trichome-specific TFs MYB75 and GLABRA 3 (GL3), leading to formation of defence proteins as well as terpenoids. Role of jasmonates in flower development is depicted for Arabidopsis thaliana. The TF AGAMOUS activates the phospholipase A1 DAD1, but also auxin induces rise in JA/JA-Ile via the function of the TFs AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8. Jasmonates induce COI1-dependently expression of MYB21 and MYB24, leading to proper stamen development, whereas expression of the TF BIGPETALp (BPEp) restricts petal growth. In senescence, jasmonates act on different levels. On the one hand, chlorophyllase is activated, which leads to chlorophyll breakdown, and RUBISCO activase is inhibited, which switches off photosynthesis. On the other hand, specific TFs, such as WRKY53, WRKY54, WRKY70 and ANAC092/ORE1, are induced, leading to expression of senescence-related genes.
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