Jasmonic Acid Signalling

Abstract

Jasmonic acid (JA) is an important plant hormone involved in the regulation of plant development and stress responses. A central feature of JA signalling is the repression of JA responses by the JASMONATE ZIM‐DOMAIN (JAZ) protein family. JAZ proteins function to inhibit the activity of transcription factors responsible for driving the expression of JA‐responsive target genes. This is achieved by recruitment of transcriptional repressors and chromatin remodelling proteins. Perception by a COI1‐JAZ coreceptor of the main bioactive molecule in JA signalling, jasmonoyl‐l‐isoleucine, results in JAZ protein degradation and release of JA responses from suppression. Specificity in JA signalling is generated by a combination of JAZ protein diversity, cell specificity of JA‐responsive transcription factors and interactions with other plant hormone signalling pathways.

Key Concepts

  • (+)‐7‐iso‐jasmonoyl‐l‐isoleucine (JA‐Ile) is the main biologically active compound responsible for jasmonic acid (JA) signalling in higher plants.
  • JASMONATE ZIM‐DOMAIN (JAZ) proteins function as the central regulators of jasmonate signalling.
  • JAZ proteins recruit transcriptional repressors to inhibit the activity of transcription factors that positively regulate JA responses.
  • The F‐box protein COI1 functions along with JAZ proteins as a JA‐Ile coreceptor that controls JA‐dependent JAZ protein degradation.
  • Specificity in JA signalling is conferred by context‐specific interactions between JAZ proteins and their targets, and by interactions between JA and other signalling pathways.
  • There are two major pathways for jasmonate‐dependent plant defence responses, which are controlled by antagonistic master‐regulator transcription factors.
  • Herbivores, pathogens and symbiotic microorganisms can manipulate jasmonate signalling for their own benefit.
  • Interactions between JAZ and DELLA proteins mediate trade‐offs between growth and defence.
  • Jasmonates likely function as long‐distance defence signals within, and possibly even between, plants.
  • Other bioactive jasmonates include 12‐oxo‐phytodienoic acid (OPDA) and cis‐jasmone.

Keywords: jasmonic acid; JAZ proteins; signalling; disease resistance; herbivore resistance; plant hormones

Figure 1. Mechanism for activation of JA responses by degradation of JAZ proteins. In the absence of JA, transcriptional activation of JA‐response genes is suppressed by JAZ proteins (top). Suppression is mediated through the recruitment of repressors of the TPL family and chromatin remodellers. COI1, a component of the SCFCOI1 ubiquitin E3 ligase complex, and JAZ proteins act as coreceptors for bioactive jasmonates, such that elevated JA levels promote COI1–JAZ protein interaction, ubiquitination (U) of JAZ proteins and their consequent destruction in the 26S proteasome (middle). The removal of JAZ proteins releases JA‐responsive transcription factors (TF), which are free to recruit RNA polymerase II (Pol II) via MED25 (bottom) and initiate gene expression. Forward arrows indicate positive regulation, while barred lines indicate negative regulation.
Figure 2. Encoding specificity in JA signalling: different outcomes of JA production depend on cellular and environmental context. Different JAZ protein isoforms in the same cell (cell 1), which may have different properties in terms of interactions with COI1 and/or transcriptional repressors, bind selectively to JA‐response transcription factors (TF1 and TF2). Hence, the characteristics of the final JA response are determined by the balance of two individual responses, which in turn depend on the properties of the individual JAZ proteins and their specific targets in the cell. In cell 2, the same JAZ protein (JAZ1) that is present in cell 1 controls JA responses, but in cell 2, it interacts with a different, tissue‐specific, transcription factor (TF3), such that the same JAZ protein regulates a different JA response in the two cell types. A fourth transcription factor (TF4) that is also present in cell 2 is regulated by a hormone (H), and when activated, interacts with TF3 to provide combinatorial control of an alternative group of target genes, generating a different JA‐dependent response. Forward arrows indicate positive regulation, while barred lines indicate negative regulation.
Figure 3. JA regulates antagonistic resistance responses to herbivory and disease. Attack by herbivores or necrotrophic pathogens leads to elevated JA levels, but different JA‐dependent defence responses are induced depending on the identity of the attacker. JA, via JAZ proteins, regulates the activity of both MYC family transcription factors, which drive herbivore resistance responses (MYC branch), and the EIN3/EIL1 transcription factors, which promote herbivore resistance (ERF branch). Herbivory tends to cause elevated ABA levels alongside JA, which favours the activation of the MYC branch, because ABA cooperatively promotes activity of the MYC transcription factors, MYC2, MYC3 and MYC4. Besides positively regulating herbivore resistance, MYC2 inhibits the ERF branch by negatively regulating the ethylene‐dependent transcription factors, EIN3 and EIL1. The ERF branch, on the other hand, is preferentially activated when JA is accompanied by elevated levels of ethylene (ET). Ethylene‐ and JA‐induced EIN3 and EIL1 simultaneously repress MYC2 activity and promote expression of ERF1 and ORA59, which in turn activate disease resistance response genes. Forward arrows indicate positive regulation, while barred lines indicate negative regulation.
Figure 4. The balance between JAZ and DELLA proteins regulates the trade‐off between defence and growth. Direct interactions between JAZ and DELLA proteins render them unavailable for repression of their respective target proteins. (a) Under stress‐free conditions, JA levels are low, resulting in stabilisation of JAZ proteins, whereas GA levels are sufficiently high that there is turnover of DELLA proteins, increasing the pool of free JAZ proteins available to suppress defence responses. (b) In the presence of herbivores or disease, JA levels rapidly rise, resulting in JAZ protein degradation, activation of defence and repression of growth via DELLA‐mediated inhibition of PHYTOCHROME‐INTERACTING FACTORS (PIFs). (c) When potential competitor plants are sensed by phytochrome (Phy), JAZ protein stability is increased but DELLA proteins are destabilised, suppressing defence and enabling growth even at elevated levels of JA.
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Roberts, Michael R(Jan 2016) Jasmonic Acid Signalling. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023721]