The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development

Abstract

Plants have evolved sophisticated systems for adaptation to their natural habitat. In response to developmental and environmental cues, plants produce and perceive jasmonate (JA) signals, which induce degradation of JASMONATE-ZIM-Domain (JAZ) proteins and derepress the JAZ-repressed transcription factors to regulate diverse aspects of defense responses and developmental processes. Here, we identified the bHLH subgroup IIId transcription factors (bHLH3, bHLH13, bHLH14 and bHLH17) as novel targets of JAZs. These bHLH subgroup IIId transcription factors act as transcription repressors and function redundantly to negatively regulate JA responses. The quadruple mutant bhlh3 bhlh13 bhlh14 bhlh17 showed severe sensitivity to JA-inhibited root growth and JA-induced anthocyanin accumulation, and exhibited obvious increase in JA-regulated plant defense against pathogen infection and insect attack. Transgenic plants overexpressing bHLH13 or bHLH17 displayed reduced JA responses. Furthermore, these bHLH factors functioned as transcription repressors to antagonize the transcription activators, such as MYC2 and the WD-repeat/bHLH/MYB complex, through binding to their target sequences. Coordinated regulation of JA responses by transcription activators and repressors would benefit plants by allowing fine regulation of defense and development, and survival in their frequently changing environment.

Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling inArabidopsis

“…The b-glucuronidase (GUS) gene driven by four copies of GAL4 DNA binding sites [GAL4(4x)-D1-3(4x)] was used as a reporter, whereas the LUC gene under the control of 35S promoter was used as the internal control ( Figure 8A). Similar with previous observations (Pauwels et al, 2010;Song et al, 2013b), expression of GAL4DB-MYC2 clearly increased the GUS/LUC ratio ( Figure 8B). However, coexpression of EIN3 or EIL1 with GAL4BD-MYC2 obviously reduced the GUS/LUC ratio ( Figure 8B), suggesting that EIN3 and EIL1 attenuate the transcriptional activation function of MYC2.…”

“…Detached leave from 3-week-old plant were inoculated with 5 mL spores of Botrytis cinerea (SCL2-4, isolated from tomato in 2011, Shanghai) (Song et al, 2013b) (10 5 spores/mL) suspended in potato dextrose broth (with potato dextrose broth alone as the control), placed in Petri dishes with 0.8% agar, and covered with lids. The lesion diameter from eight leaves for each genotype exhibiting disease symptoms was measured 2 d after inoculation.…”

“…Upon perception of JA signal (Fonseca et al, 2009;Yan et al, 2009;Sheard et al, 2010), the F-box protein CORO-NATINE INSENSITIVE1 (COI1) (Xie et al, 1998;Yan et al, 2009) recruits the JASMONATE ZIM-DOMAIN (JAZ) proteins (Chini et al, 2007;Thines et al, 2007;Yan et al, 2007) for degradation, which leads to the release of various downstream factors, including MYC2/JASMONATE INSENSITIVE1 (JIN1), MYC3, and MYC4 (Cheng et al, 2011;Fernández-Calvo et al, 2011;Niu et al, 2011), as well as WD-repeat/bHLH/MYB complex , MYB21, MYB24, and MYB57 (Mandaokar et al, 2006;Song et al, 2011) and the IIId bHLH factors (Nakata et al, 2013;Song et al, 2013b), which regulate diverse JA-mediated functions. These functions include root growth (Dathe et al, 1981;Chen et al, 2011), apical hook formation (Turner et al, 2002), flowering (Robson et al, 2010), stamen development (McConn and Browse, 1996;Song et al, 2011Song et al, , 2013a, leaf senescence (Ueda and Kato, 1980;Shan et al, 2011), secondary metabolism (De Geyter et al, 2012;Schweizer et al, 2013), drought responses (Seo et al, 2011), wounding responses (Mason and Mullet, 1990;Acosta et al, 2013;Mousavi et al, 2013), and defense against pathogen infection Vijayan et al, 1998;Melotto et al, 2006;Rowe et al, 2010;Yang et al, 2012;Zheng et al, 2012) and insect attack (McConn et al, 1997;…”

Quantitative analysis of the tomato nuclear proteome during Phytophthora capsici infection unveils regulators of immunity

“…These include transcription factors (TFs) such as a WRKY‐like TF (Solyc09g014990.2.1), which increased in abundance during infection, and a helix‐loop‐helix TF (Solyc01g096370.2.1) whose levels dropped during infection. The WRKY‐like TF is homologous to WRKY33 from Arabidopsis thaliana, which is a key defence‐associated transcriptional regulator (Zheng et al ., 2006), while helix‐loop‐helix TFs have been shown to regulate plant defence (Song et al ., 2013; Woldemariam et al ., 2013). In addition, RNA helicases, proteins that regulate RNA structure, metabolism and gene expression (Li et al ., 2008), were found to decrease in abundance during infection.…”

Cotton WRKY1 Mediates the Plant Defense-to-Development Transition during Infection of Cotton byVerticillium dahliaeby ActivatingJASMONATE ZIM-DOMAIN1Expression

“…Jasmonate (JA) is a fatty acid-derived plant hormone that is perceived by an F-box protein, CORONATINE INSENSITIVE1 (COI1), a component of the SKIP-CULLIN-F-box-type (SCF) E3 ubiquitin ligase complex (Katsir et al, 2008;Yan et al, 2009;Sheard et al, 2010). JASMONATE ZIM-DOMAIN (JAZ) family proteins are transcriptional repressors that negatively regulate JA signaling via direct interaction with several transcription factors, such as basic helix-loop-helix (bHLH) subgroup IIIe transcription factors (myelocytomatosis viral oncogene2 [MYC2], MYC3, and MYC4) and myeloblastosis (MYB) transcription factors (MYB21, MYB24, and MYB57; Cheng et al, 2009Cheng et al, , 2011Fernández-Calvo et al, 2011;Niu et al, 2011;Qi et al, 2011;Song et al, 2011Song et al, , 2013. In the presence of JA, JAZ proteins are targeted by the SCF COI1 complex for ubiquitination and degradation, which consequently relieves the repression and rapid activation of JA responses (Chini et al, 2007;Thines et al, 2007;Howe, 2010).…”