Structural insights into alternative splicing-mediated desensitization of jasmonate signaling

Abstract

Jasmonate ZIM-domain (JAZ) transcriptional repressors play a key role in regulating jasmonate (JA) signaling in plants. Below a threshold concentration of jasmonoyl isoleucine (JA-Ile), the active form of JA, the C-terminal Jas motif of JAZ proteins binds MYC transcription factors to repress JA signaling. With increasing JA-Ile concentration, the Jas motif binds to JA-Ile and the COI1 subunit of the SCF COI1 E3 ligase, which mediates ubiquitination and proteasomal degradation of JAZ repressors, resulting in derepression of MYC transcription factors. JA signaling subsequently becomes desensitized, in part by feedback induction of JAZ splice variants that lack the C-terminal Jas motif but include an N-terminal cryptic MYC-interaction domain (CMID). The CMID sequence is dissimilar to the Jas motif and is incapable of recruiting SCF COI1 , allowing CMID-containing JAZ splice variants to accumulate in the presence of JA and to re-repress MYC transcription factors as an integral part of reestablishing signal homeostasis. The mechanism by which the CMID represses MYC transcription factors remains elusive. Here we describe the crystal structure of the MYC3-CMID JAZ10 complex. In contrast to the Jas motif, which forms a single continuous helix when bound to MYC3, the CMID adopts a loop-helix-loop-helix architecture with modular interactions with both the Jas-binding groove and the backside of the Jasinteraction domain of MYC3. This clamp-like interaction allows the CMID to bind MYC3 tightly and block access of MED25 (a subunit of the Mediator coactivator complex) to the MYC3 transcriptional activation domain, shedding light on the enigmatic mechanism by which JAZ splice variants desensitize JA signaling.signaling | plant hormone | plant defense | plant pathogen | plant insect

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

“…The expression of JAZ genes is also known to be subsequently activated, which in part results in desensitization of JA signaling through alterative splicing variants of JAZs (28)(29)(30). This alternative splicingmediated desensitization of JA signaling requires the N-terminal cryptic MYC-interaction domain (CMID) of JAZ, which somehow keeps JA signaling from becoming unregulated (28,31,32). There are at least two mechanisms required for JAZ repressor activity.…”

Regulation of growth–defense balance by the JASMONATE ZIM‐DOMAIN (JAZ)‐MYC transcriptional module

“…Second, binding of the Jas motif of JAZ to the N terminus of MYC restricts access of MYC to the MED25 coactivator subunit of the mediator complex (C ß evik et al, 2012;Chen et al, 2012;Zhang et al, 2015). A subset of JAZ repressors, including alternative splice variants of JAZ10, contain a cryptic MYC-interaction domain (CMID) that tightly binds MYC and represses target gene expression (Chung & Howe, 2009;Chung et al, 2010;Moreno et al, 2013;Goossens et al, 2015;Zhang et al, 2017). Transcription of JA-responsive genes is activated upon accumulation of jasmonoyl-L-isoleucine (JA-Ile), the production of which is tightly controlled by environmental and developmental cues (Staswick & Tiryaki, 2004;Suza & Staswick, 2008;).…”

The OsJAZ1 degron modulates jasmonate signaling sensitivity during rice development

“…In the Arabidopsis genome, there are 12 JAZ genes belonging to the family of TIFY proteins, which are characterized by two conserved motifs (Chini et al, 2016;Howe et al, 2018;Pauwels and Goossens, 2011): a TIF[F/Y]XG motif [also called the zinc-finger protein expressed in the inflorescence meristem (ZIM) motif ] in the central portion of the protein (Pauwels et al, 2010;Thireault et al, 2015); and a JA-associated (Jas) motif that is particularly important for controlling SCF COI1 -dependent stability, TF interactions and nuclear localization of the JAZ proteins (Chini et al, 2007;Howe, 2018;Melotto et al, 2008;Sheard et al, 2010;Thines et al, 2007;Withers et al, 2012;Yan et al, 2007). Some JAZ proteins also contain cryptic MYC-interaction domain/N-terminal (CMID/NT) motifs that are involved in interactions with other proteins (Goossens et al, 2015;Hou et al, 2010;Moreno et al, 2013;Zhai et al, 2015;Zhang et al, 2017), and ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motifs that repress TF activity (Shyu et al, 2012).…”