SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes

被引:118
作者
Deng, Heng [1 ]
Chen, Yao [1 ]
Liu, Ziyu [1 ]
Liu, Zhaoqiao [1 ]
Shu, Peng [1 ]
Wang, Ruochen [1 ]
Hao, Yanwei [2 ]
Su, Dan [1 ]
Pirrello, Julien [3 ]
Liu, Yongsheng [1 ]
Li, Zhengguo [4 ]
Grierson, Don [5 ]
Giovannoni, James J. [6 ,7 ]
Bouzayen, Mondher [3 ]
Liu, Mingchun [1 ]
机构
[1] Sichuan Univ, Coll Life Sci, Key Lab Bioresource & Ecoenvironm, Minist Educ, Chengdu 610065, Sichuan, Peoples R China
[2] South China Agr Univ, Coll Hort, Guangzhou 510642, Peoples R China
[3] Univ Toulouse, GBF Lab, INRA, F-31320 Castanet Tolosan, France
[4] Chongqing Univ, Sch Life Sci, Key Lab Plant Hormones & Dev Regulat Chongqing, Chongqing, Peoples R China
[5] Univ Nottingham, Sch Biosci, Loughborough LE12 5RD, Leics, England
[6] Cornell Univ, Boyce Thompson Inst, Ithaca, NY 14853 USA
[7] USDA ARS, Robert W Holley Ctr Agr & Hlth, Ithaca, NY 14853 USA
基金
中国国家自然科学基金; 国家重点研发计划;
关键词
ETHYLENE RESPONSE FACTORS; ERF TRANSCRIPTION FACTOR; ABSCISIC-ACID; SALT STRESS; MOTIF; ARABIDOPSIS; EXPRESSION; RESISTANCE; BINDING; METHYLOMES;
D O I
10.1093/plcell/koac025
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Ethylene response factors (ERFs) are downstream components of ethylene-signaling pathways known to play critical roles in ethylene-controlled climacteric fruit ripening, yet little is known about the molecular mechanism underlying their mode of action. Here, we demonstrate that SlERF.F12, a member of the ERF.F subfamily containing Ethylene-responsive element-binding factor-associated Amphiphilic Repression (EAR) motifs, negatively regulates the onset of tomato (Solanum lycopersicum) fruit ripening by recruiting the co-repressor TOPLESS 2 (TPL2) and the histone deacetylases (HDAs) HDA1/HDA3 to repress the transcription of ripening-related genes. The SlERF.F12-mediated transcriptional repression of key ripening-related genes 1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2 (ACS2), ACS4, POLYGALACTURONASE 2a, and PECTATE LYASE is dependent on the presence of its C-terminal EAR motif. We show that SlERF.F12 interacts with the co-repressor TPL2 via the C-terminal EAR motif and recruits HDAs SlHDA1 and SlHDA3 to form a tripartite complex in vivo that actively represses transcription of ripening genes by decreasing the level of the permissive histone acetylation marks H3K9Ac and H3K27Ac at their promoter regions. These findings provide new insights into the ripening regulatory network and uncover a direct link between repressor ERFs and histone modifiers in modulating the transition to ripening of climacteric fruit. The SlERF.F12-TPL2-HDA1/3 complex represses fruit ripening initiation by promoting histone deacetylation in the promoter regions of ripening-related genes.
引用
收藏
页码:1250 / 1272
页数:23
相关论文
共 83 条
[1]   Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening [J].
Alexander, L ;
Grierson, D .
JOURNAL OF EXPERIMENTAL BOTANY, 2002, 53 (377) :2039-2055
[2]   The significance of digital gene expression profiles [J].
Audic, S ;
Claverie, JM .
GENOME RESEARCH, 1997, 7 (10) :986-995
[3]   Molecular mechanisms of ethylene signaling in Arabidopsis [J].
Benavente, LM ;
Alonso, JM .
MOLECULAR BIOSYSTEMS, 2006, 2 (3-4) :165-173
[4]   POST-HARVEST RIPENING OF AVOCADOS [J].
BURG, SP ;
BURG, EA .
NATURE, 1962, 194 (4826) :398-&
[5]   Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress [J].
Cao, Yifei ;
Song, Fengming ;
Goodman, Robert M. ;
Zheng, Zhong .
JOURNAL OF PLANT PHYSIOLOGY, 2006, 163 (11) :1167-1178
[6]   The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis [J].
Causier, Barry ;
Ashworth, Mary ;
Guo, Wenjia ;
Davies, Brendan .
PLANT PHYSIOLOGY, 2012, 158 (01) :423-438
[7]   The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control [J].
Dong, Chun-Juan ;
Liu, Jin-Yuan .
BMC PLANT BIOLOGY, 2010, 10
[8]   Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean [J].
Dong, Lidong ;
Cheng, Yingxin ;
Wu, Junjiang ;
Cheng, Qun ;
Li, Wenbin ;
Fan, Sujie ;
Jiang, Liangyu ;
Xu, Zhaolong ;
Kong, Fanjiang ;
Zhang, Dayong ;
Xu, Pengfei ;
Zhang, Shuzhen .
JOURNAL OF EXPERIMENTAL BOTANY, 2015, 66 (09) :2635-2647
[9]   Isolation and characterization of a bread wheat salinity responsive ERF transcription factor [J].
Dong, Wei ;
Ai, Xinghui ;
Xu, Fei ;
Quan, Taiyong ;
Liu, Shuwei ;
Xia, Guangmin .
GENE, 2012, 511 (01) :38-45
[10]   Rapid phenotyping of the tomato fruit model, Micro-Tom, with a portable VIS-NIR spectrometer [J].
Ecarnot, Martin ;
Baczyk, Paulina ;
Tessarotto, Lydie ;
Chervin, Christian .
PLANT PHYSIOLOGY AND BIOCHEMISTRY, 2013, 70 :159-163