title: Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes.
abstract: Degreening caused by rapid chlorophyll (Chl) degradation is a characteristic event during green organ senescence or maturation. Pheophorbide a oxygenase gene (PAO) encodes a key enzyme of Chl degradation, yet its transcriptional regulation remains largely unknown. Using yeast one-hybrid screening, coupled with in vitro and in vivo assays, we revealed that Arabidopsis MYC2/3/4 basic helix-loop-helix proteins directly bind to PAO promoter. Overexpression of the MYCs significantly enhanced the transcriptional activity of PAO promoter in Arabidopsis protoplasts, and methyl jasmonate (MeJA) treatment greatly induced PAO expression in wild-type Arabidopsis plants, but the induction was abolished in myc2 myc3 myc4. In addition, MYC2/3/4 proteins could promote the expression of another Chl catabolic enzyme gene, NYC1, as well as a key regulatory gene of Chl degradation, NYE1/SGR1, by directly binding to their promoters. More importantly, the myc2 myc3 myc4 triple mutant showed a severe stay-green phenotype, whereas the lines overexpressing the MYCs showed accelerated leaf yellowing upon MeJA treatment. These results suggest that MYC2/3/4 proteins may mediate jasmonic acid (JA)-induced Chl degradation by directly activating these Chl catabolic genes (CCGs). Three NAC family proteins, ANAC019/055/072, downstream from MYC2/3/4 proteins, could also directly promote the expression of a similar set of CCGs (NYE1/SGR1, NYE2/SGR2 and NYC1) during Chl degradation. In particular, anac019 anac055 anac072 triple mutant displayed a severe stay-green phenotype after MeJA treatment. Finally, we revealed that MYC2 and ANAC019 may interact with each other and synergistically enhance NYE1 expression. Together, our study reveals a hierarchical and coordinated regulatory network of JA-induced Chl degradation.
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Xiaoyu
authors.initials: X
authors.lastname: Zhu
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Junyi
authors.initials: J
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Zuokun
authors.initials: Z
authors.lastname: Xie
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Jiong
authors.initials: J
authors.lastname: Gao
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Guodong
authors.initials: G
authors.lastname: Ren
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Shan
authors.initials: S
authors.lastname: Gao
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
authors.forename: Xin
authors.initials: X
authors.lastname: Zhou
authors.affiliation: State Key Laboratory of Genetic Engineering and Fudan Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.|Shanghai Key Laboratory of Bio-Energy Crops, Shanghai University, Shanghai, 200444, China.
authors.forename: Benke
authors.initials: B
authors.lastname: Kuai
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D051778:Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / Q000235:genetics / Q000378:metabolism; D002734:Chlorophyll / Q000235:genetics* / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D010105:Oxygenases / Q000235:genetics / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism*; D018515:Plant Leaves / Q000502:physiology; D030821:Plants, Genetically Modified; D011401:Promoter Regions, Genetic; D015534:Trans-Activators / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D051778:Basic Helix-Loop-Helix Leucine Zipper Transcription Factors; D002734:Chlorophyll; D003517:Cyclopentanes; D010105:Oxygenases; D054883:Oxylipins; D015534:Trans-Activators; D014157:Transcription Factors; C493659:NAC019 protein, Arabidopsis; C493660:ANAC055 protein, Arabidopsis; C493661:ANAC072 protein, Arabidopsis; C473611:MYC2 protein, Arabidopsis; C473612:MYC3 protein, Arabidopsis; C473613:MYC4 protein, Arabidopsis; C011006:jasmonic acid; C112915:pheide a oxygenase
keywords: ANAC019/055/072; Arabidopsis; MYC2/3/4; chlorophyll degradation; jasmonic acid signaling