To immunity and beyond: the central role of jasmonate signalling in beneficial root-microbe-environment interactions

Abstract

Jasmonates (JAs) have traditionally been studied for their defensive roles against wounding and detrimental organisms, but they are also crucial hormones for plant-microbe beneficial interactions. Here, we review the most recent advances in this overlooked field. We cover the evolutionary divergences of JA biosynthesis and signalling across various plant lineages and present the molecular mechanisms of action through which beneficial microbes interact with the host JA signalling pathway as well as environmental integration. Special emphasis is given to the cutting-edge tools to study the spatial compartmentalization and cell and tissue specialization of JA signalling. This review underscores the role of the JA signalling pathway, with the MYELOCYTOMATOSIS2 transcription factor as a potential integrator of biotic and environmental cues, and highlights its significance in mutualistic interactions.

Keywords: defence; environmental integration; evolution; jasmonates; mutualism; plant–microbe interactions; rhizobiome; spatial compartmentalization.

Fig. 1

Jasmonate signalling as an integrator of environmental cues and plant–microbe interactions in roots. Diagram summarizing the novel insights about the role of jasmonates (JAs) as integrators of root–microbe–environment interactions. A schematic representation of a plant is shown at the centre of the image. Red arrows indicate the crosstalk between JAs' signalling with diverse stimuli and plant processes. Yellow lightings represent environmental stresses. Simplified schemes of JAs biosynthesis and signalling are shown in green boxes. (a) While key components of JA signalling are strongly conserved across species, divergence in JA biosynthesis and the ligand specificity of COI1 reflect evolutionary adaptations of the JA signalling pathway, which may influence how plants perceive and respond to their dynamic surroundings. 12‐OPDA, 12‐oxo‐phytodienoic acid; dn‐OPDAs, dinor‐oxo‐phytodienoic acids; α‐LeA, alpha linoleic acid. (b) Different microbes from diverse guilds present evolutionarily divergent effectors that converge in a parallel mechanism of action that stabilizes JASMONATE ZIM DOMAIN proteins and repress JAs‐responsive genes to ensure microbial colonization. (c) MYELOCYTOMATOSIS2 (MYC2) is the master regulator of JA‐responsive genes, controlling defence and mutualism genes while it also promotes certain mutualistic interactions through distinct mechanisms in root nodule symbiosis (RNS) and ectomycorrhiza (ECM). Most representative genes involved in MYC2's defence/mutualism coordination in RNS are depicted with blue circles, while those described in ECM are in red. CHI, chitinase; DNF1, defective in nitrogen fixation 1; IPD3, interacting protein of DMI3, also known as CYCLOPS; NCR, nodule‐specific cysteine‐rich peptide; NIN, nodule inception; NRT, nitrogen transporter; PCWDE, plant cell wall degrading enzymes; PDF1.2, plant defensin 1.2; PI, protease inhibitor; PR, pathogenesis related; TPS, terpene synthase. (d) Finally, MYC2 also promotes mycorrhiza‐induced resistance in arbuscular mycorrhiza. (e) Microbiomes isolated from warm environments enhance the synthesis of 12‐OPDA and dn‐OPDAs, which are related to enhanced thermotolerance in Bryophytes in a CORONATINE INSENSITIVE 1‐independent manner. (f) MYC2 transcription factor integrates environmental cues, such as light or nutrients, which are capable of reshaping JA signalling and affecting growth‐defence trade‐offs in response to microbial interaction.

Fig. 2

Current and future perspectives on jasmonate (JA) signalling multilayered regulation, spatial compartmentalization and PRIMER cell state concept in mutualistic interactions. Multiple layers of gene and protein regulation may act to fine‐tune JA responses in fluctuating environments. (a) JA core signalling hub COI1‐JAZ‐MYC2 regulates JA‐responsive genes through JA‐Ile‐mediated ubiquitination (Ub) of JAZ corepressor and activation of MYC2 transcription factor. (b) JA alters H3K4me3 and H2A.Z methylation landscape, whereas host hypomethylation impairs ectomycorrhizal interaction. (c) Post‐translational modifications, such as ubiquitination (Ub), phosphorylation (P), SUMOylation (SUMO) and arginine methylation (R‐met), have been reported to influence key JA signalling proteins. (d) Spatial compartmentalization of JA signalling may allow plants to mount strong but localized defence responses while maintaining overall growth. (e) A novel ‘PRIMER’ cell state initiating defence responses has been recently described in plants. Future studies could investigate whether this novel state also occurs in ‘mutualistic competent’ cells and whether it involves shared or distinct molecular mechanisms. COI1, CORONATINE INSENSITIVE 1; JAZ, JASMONATE ZIM DOMAIN; MYC2, MYELOCYTOMATOSIS2.