Jasmonate signaling and manipulation by pathogens and insects

Abstract

Plants synthesize jasmonates (JAs) in response to developmental cues or environmental stresses, in order to coordinate plant growth, development or defense against pathogens and herbivores. Perception of pathogen or herbivore attack promotes synthesis of jasmonoyl-L-isoleucine (JA-Ile), which binds to the COI1-JAZ receptor, triggering the degradation of JAZ repressors and induction of transcriptional reprogramming associated with plant defense. Interestingly, some virulent pathogens have evolved various strategies to manipulate JA signaling to facilitate their exploitation of plant hosts. In this review, we focus on recent advances in understanding the mechanism underlying the enigmatic switch between transcriptional repression and hormone-dependent transcriptional activation of JA signaling. We also discuss various strategies used by pathogens and insects to manipulate JA signaling and how interfering with this could be used as a novel means of disease control.

Keywords: Insect defense; jasmonate; plant hormone; plant immunity; plant pathogen; salicylic acid..

Fig. 1.

Model of JAZ-mediated transcriptional repression and JA-Ile perception-mediated transcriptional activation of JA signaling. (A) In the resting stage, JA-responsive gene expression is suppressed by members of the JAZ protein family, which function as transcription repressors by binding and inhibiting MYC transcription factors through: (1) direct inhibition of the interaction between MYCs and the MED25 subunit of the Mediator co-activator complex (Zhang et al., 2015a); and/or (2) recruiting TOPLESS (TPL) corepressors either directly (Shyu et al., 2012) or through the NINJA adaptor (Kazan, 2006; Pauwels et al., 2010; Acosta et al., 2013). TPL in turn recruits histone deacetylases, HDA6 and HDA19, which repress gene expression through chromatin remodeling (Zhou et al., 2005; Long et al., 2006; Wu et al., 2008). JAZ1/3/9 also directly interact with HDA6 (Zhu et al., 2011). Red lines represent transcriptional repression of JA response genes. (B) JA-Ile facilitates the interaction between JAZ and COI1 to form a coreceptor complex (Thines et al., 2007; Katsir et al., 2008; Melotto et al., 2008; Yan et al., 2009; Sheard et al., 2010). This coreceptor complex leads to ubiquitination and proteasome-dependent degradation of JAZ repressors by the SCF^COI1 E3 ubiquitin ligase, resulting in derepression of MYCs (Chini et al., 2007; Thines et al., 2007; Yan et al., 2007). JAZ-free MYCs form homo- or heterodimers and bind to the conserved G-box (not shown) in the promoters of JA responsive genes (Fernández-Calvo et al., 2011). By interacting with MED25 and possibly additional co-activators, MYCs recruit RNA polymerase II and other transcription components (not shown) to transcribe JA-responsive genes (Çevik et al., 2012; Chen et al., 2012). Green arrow represents derepression of JA response genes.

Fig 2.

Crystal structures of the COI1-ASK1 complex with JA-Ile and the Jas ^JAZ1 peptide and the MYC3 (N-terminus) complex with the Jas ^JAZ1 peptide. (A) In the COI1-Jas^JAZ1 complex, COI1 forms a binding pocket for JA-Ile. The Jas^JAZ1 peptide adopts a bipartite structure that contains a N-terminal loop region (magenta) and a C-terminal α-helix (orange). Only parts of the COI1 structure are shown and ASK1 is omitted. (B) JA-Ile interacts with three positive residues in the COI1 ligand-binding pocket: R85, R348 and R409. Hydrogen bond and salt bridge networks are shown by yellow dashes. (C) The hydrogen bond network (yellow dashs) in the inositol phosphate-binding site indicates that InsP₅ is a crucial cofactor for jasmonate perception. R206 of the Jas^JAZ1 peptide directly interacts with the inositol phosphate and the carboxyl group of JA-Ile. R206 also cooperates with three arginine residues, R85, R348 and R409, of COI1 at the bottom of the JA-Ile binding pocket, interacting with both JA-Ile (above) and InsP₅ (below). (D) In the MYC3- Jas^JAZ1 complex, the Jas^JAZ1 peptide, adopting a single, continuous helix, occupies the groove formed by JID and TAD in the MYC3 N-terminus. Images were generated using PyMol software (Schrödinger, 2015) and the PDB files 3OGL (A, B, C) (Sheard et al., 2010) and 4YZ6 (D) (Zhang et al., 2015a).

Fig. 3.

Diagram illustrating plant pathogen hijacking of the core components of JA signaling. Microbial pathogens and insects employ different strategies to hijack JA signaling. In this diagram, only virulence factors that target the core components of JA biosynthesis or signalling are depicted. The insect vector M. quadrilineatus employs phytoplasma AY-WB to suppress JA biosynthesis via downregulation of LOX2 expression (Sugio et al., 2011). The fungus M. oryzae stimulates JA hydroxylation to attenuate JA signalling via the Abm effector (Patkar et al., 2015). The mutualist L. bicolor suppresses the degradation of JAZ protein by the action of the MiSSP7 effector (Plett et al., 2014). The viral protein BCTV L2 suppresses SCF^COI1 activity through CSN5 (Lozano-Duran et al., 2011). The insect vector B. tabaci employs TYLCCNV to suppress MYC2-mediated gene expression through direct interaction between the βC1 effector and MYC2 (Li et al., 2014). Conversely, pathogens can also activate JA signalling for pathogenesis. F. oxysporum produces JA or JA-Ile and activates JA signalling (Cole et al., 2014). The hemibiotrophic bacterium P. syringae secretes COR or the AvrB effector to enhance the interaction between COI1 and JAZ coreceptor proteins (Bender et al., 1999; Katsir et al., 2008; Melotto et al., 2008; Yan et al., 2009; Sheard et al., 2010; Zheng et al., 2012; Zhang et al., 2015b; Zhou et al., 2015). HopZ1a acetylates JAZ proteins and stimulates degradation of JAZ in a COI1-dependent manner (Jiang et al., 2013). HopX1 stimulates JAZ protein degradation in a COI1-independent manner and activates JA signalling (Gimenez-Ibanez et al., 2014).