Portal de Periódicos da CAPES

Many ways to repress! JAZ’s agony of choices

2021; Elsevier BV; Volume: 14; Issue: 5 Linguagem: Inglês

10.1016/j.molp.2021.04.010

1674-2052

Mark Zander,

Plant Virus Research Studies

The major plant hormone jasmonic acid (JA) controls a wide range of important biological processes; in particular stress responses and male reproductive development (Wasternack and Song, 2017Wasternack C. Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription.J. Exp. Bot. 2017; 68: 1303-1321PubMed Google Scholar). Local de novo biosynthesis as well aslong-distance transport of JA and subsequent perception of its conjugate jasmonoyl-isoleucine (JA-Ile) leads to the activation of a large transcriptional regulatory network with thousands of genes transcriptionally reprogrammed (Wasternack and Song, 2017Wasternack C. Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription.J. Exp. Bot. 2017; 68: 1303-1321PubMed Google Scholar; Aerts et al., 2021Aerts N. Pereira Mendes M. Van Wees S.C.M. Multiple levels of crosstalk in hormone networks regulating plant defense.Plant J. 2021; 105: 489-504Crossref PubMed Scopus (40) Google Scholar). Key regulators of this JA-initiated transcriptional network are the JAZ (JASMONATE-ZIM DOMAIN) proteins that directly repress the master transcription factors (TFs) MYC2 to MYC5 and other TFs (Wasternack and Song, 2017Wasternack C. Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription.J. Exp. Bot. 2017; 68: 1303-1321PubMed Google Scholar). JAZ proteins form the JA co-receptor complex together with the F-box protein COI1 (CORONATINE INSENSITIVE1), which is part of the Skp-Cullin-F-box-E3 ubiquitin ligase complex (SCFCOI1) that upon JA-Ile perception induces the ubiquitination and proteasomal degradation of JAZ proteins (Wasternack and Song, 2017Wasternack C. Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription.J. Exp. Bot. 2017; 68: 1303-1321PubMed Google Scholar). Consequently, previously JAZ-bound TFs are liberated in a JA dose-dependent manner with increasing levels of free JA-Ile gradually leading to more liberated TFs. Non-repressed TFs, such as MYC2, stimulate their own expression to rapidly initiate and amplify the JA-induced transcriptional response by targeting major components of the JA signaling pathway along with other secondary TFs (Aerts et al., 2021Aerts N. Pereira Mendes M. Van Wees S.C.M. Multiple levels of crosstalk in hormone networks regulating plant defense.Plant J. 2021; 105: 489-504Crossref PubMed Scopus (40) Google Scholar). At its target genes, MYC2 associates with the Mediator subunit MED25, HAC1 (HISTONE ACETYLTRANSFERASE OF THE CBP FAMILY1), and the plant Gro/Tup1 family protein LUH (LEUNIG_HOMOLOG) to orchestrate MYC2-dependent gene activation (Zhai et al., 2020Zhai Q. Deng L. Li C. Mediator subunit MED25: at the nexus of jasmonate signaling.Curr. Opin. Plant Biol. 2020; 57: 78-86Crossref PubMed Scopus (9) Google Scholar). To prevent TF-induced transcriptional gene activation, JAZs use multiple strategies. Here, I discuss this versatile repressive repertoire of JAZ proteins, especially in light of new findings by Li et al., 2021Li Z. Luo X. Ou Y. et al.JASMONATE-ZIM DOMAIN proteins 1 engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis.Mol. Plant. 2021; 14 (In this issue)https://doi.org/10.1016/j.molp.2021.03.001Abstract Full Text Full Text PDF Scopus (7) Google Scholar revealing a JAZ-mediated repression mechanism that operates through the direct engagement of PRC2 (Polycomb Repressive Complex 2). In cells with low levels of JA-Ile, TFs such as MYC2 are not very abundant and probably reside on the DNA directly interacting with JAZ repressors. JAZs can either recruit the transcriptional Groucho (Gro)/Tup1 family corepressor TPL (TOPLESS) and TPL-related (TPR) directly through their own EAR motif (JAZ8 and JAZ13) or indirectly through the interaction with the EAR domain-containing protein NINJA (NOVEL INTERACTOR OF JAZ) to MYC2 target genes (Wasternack and Song, 2017Wasternack C. Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription.J. Exp. Bot. 2017; 68: 1303-1321PubMed Google Scholar). A recent study also identified EAR motif-Containing Adaptor Protein as a direct JAZ6 and JAZ8 interactor that recruits TPR2 (Li et al., 2020Li C. Shi L. Wang Y. Li W. Chen B. Zhu L. Fu Y. Arabidopsis ECAP is a new adaptor protein that connects JAZ repressors with the TPR2 co-repressor to suppress jasmonate-responsive anthocyanin accumulation.Mol. Plant. 2020; 13: 246-265Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar). TPL and TPRs associate with histone deacetylases (HDACs), such as HDA6 and HDA19 in Arabidopsis, to reduce gene body acetylation in JA-responsive genes, thereby repressing gene expression (Figure 1) (Zhu et al., 2011Zhu Z. An F. Feng Y. Li P. Xue L. Mu A. Jiang Z. Kim J.M. To T.K. Li W. et al.Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2011; 108: 12539-12544Crossref PubMed Scopus (442) Google Scholar; Liu et al., 2014Liu X. Yang S. Zhao M. Luo M. Yu C.W. Chen C.Y. Tai R. Wu K. Transcriptional repression by histone deacetylases in plants.Mol. Plant. 2014; 7: 764-772Abstract Full Text Full Text PDF PubMed Scopus (146) Google Scholar). In addition to the TPL-mediated chromatin-based repression of JAZs, Zhang et al., 2015Zhang F. Yao J. Ke J. Zhang L. Lam V.Q. Xin X.F. Zhou X.E. Chen J. Brunzelle J. Griffin P.R. et al.Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling.Nature. 2015; 525: 269-273Crossref PubMed Scopus (165) Google Scholar discovered a JAZ-triggered MED25 outcompetition mechanism. A key regulatory prerequisite of JA-induced gene activation is the complex formation between TF and MED25 (Zhai et al., 2020Zhai Q. Deng L. Li C. Mediator subunit MED25: at the nexus of jasmonate signaling.Curr. Opin. Plant Biol. 2020; 57: 78-86Crossref PubMed Scopus (9) Google Scholar). Strikingly, the activator interaction domain of MED25 and the Jas domain of JAZs bind to the same region of MYC3 (Zhang et al., 2015Zhang F. Yao J. Ke J. Zhang L. Lam V.Q. Xin X.F. Zhou X.E. Chen J. Brunzelle J. Griffin P.R. et al.Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling.Nature. 2015; 525: 269-273Crossref PubMed Scopus (165) Google Scholar). Co-expression and competition assays revealed that JAZs outcompete MED25 for MYC3 interaction thus providing an elegant mode of JAZ-mediated repression by simply preventing the formation of a transcriptional activation complex (Figure 1) (Zhang et al., 2015Zhang F. Yao J. Ke J. Zhang L. Lam V.Q. Xin X.F. Zhou X.E. Chen J. Brunzelle J. Griffin P.R. et al.Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling.Nature. 2015; 525: 269-273Crossref PubMed Scopus (165) Google Scholar). This modus can also better explain the observed repressive capacities of JAZs in transient reporter assays using protoplasts since an often-overlooked aspect of these assays are differences in biological context between a chromosome-located versus a plasmid-located regulatory region. A recent large-scale study analyzing human enhancer regions revealed large differences between chromosomal and episomal reporter activity (Inoue et al., 2017Inoue F. Kircher M. Martin B. Cooper G.M. Witten D.M. McManus M.T. Ahituv N. Shendure J. A systematic comparison reveals substantial differences in chromosomal versus episomal encoding of enhancer activity.Genome Res. 2017; 27: 38-52Crossref PubMed Scopus (111) Google Scholar). Results from transient assays that investigate chromatin-based mechanisms should therefore be interpreted cautiously. PRC2 controls and catalyzes the genome-wide trimethylation of histone H3 lysine 27 (H3K27me3) (Lanzuolo and Orlando, 2012Lanzuolo C. Orlando V. Memories from the polycomb group proteins.Annu. Rev. Genet. 2012; 46: 561-589Crossref PubMed Scopus (130) Google Scholar). In Arabidopsis, H3K27me3 maintenance is conferred by one of the H3K27me3 readers LHP1 (LIKE HETEROCHOMATIN PROTEIN 1), which interacts with EMF1 (EMBRYONIC FLOWER 1) to repress transcription at target (Wang et al., 2014Wang Y. Gu X. Yuan W. Schmitz R.J. He Y. Photoperiodic control of the floral transition through a distinct polycomb repressive complex.Dev. Cell. 2014; 28: 727-736Abstract Full Text Full Text PDF PubMed Scopus (90) Google Scholar). In a recent study, Li et al., 2021Li Z. Luo X. Ou Y. et al.JASMONATE-ZIM DOMAIN proteins 1 engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis.Mol. Plant. 2021; 14 (In this issue)https://doi.org/10.1016/j.molp.2021.03.001Abstract Full Text Full Text PDF Scopus (7) Google Scholar discovered that seven (JAZ1, JAZ3, JAZ4, JAZ6, JAZ8, JAZ9, and JAZ10) out of the 13 Arabidopsis JAZ proteins, as well as the adaptor protein NINJA, can interact with the H3K27me3 reader LHP1 and the PRC2 structural core subunit EMF2 (EMBRYONIC FLOWER 2) in yeast and in planta. To investigate the biological significance of these interactions, the authors chose proper stamen development as their phenotypical readout since mutants defective in JA biosynthesis or JA perception, such as the coi1 mutant, show no anther dehiscence and no viable pollen. The general assumption is that coi1 mutant phenotypes are the consequence of non-degradable JAZ repressors that continuously repress gene expression. Introduction of the lhp1 and clf mutation into the coi1 mutant background led to a partial suppression of its anther dehiscence and pollen viability phenotype. The partial suppression was also observed in lhp1 and clf mutants that were crossed with mutants that express a dominant-negative version of JAZ1 (JAZ1ΔJas) suggesting that the PRC2 complex is partially responsible for JAZ-mediated gene repression in stamen development. Next, the authors focused on the expression of three master TFs, DYT1, AMS, and MS1 that control both phases of anther and pollen development: microsporogenesis (early development) and microgametogenesis (late development). Their expression is de-repressed in lhp1 and clf mutants and repressed in JAZ1ΔJas mutants (DYT1 early phase, AMS and MS1 late phase). In addition, JAZ1ΔJas-mediated transcriptional suppression of DYT1, AMS, and MS1 expression is partially relieved in JAZ1ΔJas lhp1 and JAZ1ΔJas clf double mutants. By using chromatin immunoprecipitation (ChIP)–qPCR, Li et al., 2021Li Z. Luo X. Ou Y. et al.JASMONATE-ZIM DOMAIN proteins 1 engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis.Mol. Plant. 2021; 14 (In this issue)https://doi.org/10.1016/j.molp.2021.03.001Abstract Full Text Full Text PDF Scopus (7) Google Scholar observed an enrichment of GFP-tagged CLF at the DYT1, AMS, and MS1 genes, which was reduced upon JA treatment. H3K27me3 occupancy at these loci followed a similar trend. In contrast, CLF ChIP analysis in JAZ1ΔJas mutants revealed the opposite scenario, with an increased CLF binding compared with CLF binding in the wild type, again highlighting the new function of JAZs in engaging PRC2 to facilitate gene repression (Figure 1). The TFs, which are repressed by the JAZ/PRC2/LHP1 module are unknown at this point, and also whether H3K27me3 demethylases are involved in the repression relief is not known. To test how globally this JAZ-PRC2/LHP1 repressive module operates, Li et al., 2021Li Z. Luo X. Ou Y. et al.JASMONATE-ZIM DOMAIN proteins 1 engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis.Mol. Plant. 2021; 14 (In this issue)https://doi.org/10.1016/j.molp.2021.03.001Abstract Full Text Full Text PDF Scopus (7) Google Scholar conducted LHP1 ChIP sequencing in seedlings and found that 177 genes out of 1222 JA-induced genes are bound by LHP1. Interestingly, LHP1 occupancy was reduced upon JA application, indicating that the relief of JAZ-PRC2/LHP1-mediated repression is required for full JA-induced activation of these genes. The molecular determinants for the individual modes of repression, including their dynamics, are unclear at this point but a mixture of stress, developmental, tissue, and locus-specific contexts can be envisioned. Future research is needed to shed more light on this intriguing repressive repertoire of JAZs. No conflict of interest declared.