SUMOylation of MYB30 enhances salt tolerance by elevating alternative respiration via transcriptionally upregulating AOX1a in Arabidopsis

被引:75
作者
Gong, Qianyuan [1 ]
Li, Sha [1 ]
Zheng, Yuan [2 ]
Duan, Hongqin [1 ]
Xiao, Fei [1 ]
Zhuang, Yufen [1 ]
He, Jiaxian [1 ]
Wu, Guochun [1 ]
Zhao, Shuangshuang [3 ]
Zhou, Huapeng [1 ]
Lin, Honghui [1 ]
机构
[1] Sichuan Univ, Coll Life Sci, Key Lab Bio Resource & Eco Environm, Minist Educ, Chengdu 610064, Peoples R China
[2] Henan Univ, Inst Plant Stress Biol, Dept Biol, State Key Lab Cotton Biol, Kaifeng 475004, Peoples R China
[3] Shandong Normal Univ, Life Sci Coll, Key Lab Plant Stress, Jinan 250014, Peoples R China
基金
中国国家自然科学基金;
关键词
salt tolerance; MYB30; alternative oxidase (AOX); alternative respiration; redox homeostasis; SUMOylation; MITOCHONDRIAL RETROGRADE REGULATION; OXIDATIVE STRESS; SIGNAL-TRANSDUCTION; E3; LIGASE; OXIDASE; GENE; HOMEOSTASIS; ACTIVATION; MECHANISMS; EXPRESSION;
D O I
10.1111/tpj.14689
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Salt stress reduces crop growth and productivity globally. Here we report that a R2R3-MYB transcription factor MYB30 participates in salt tolerance in Arabidopsis. MYB30 can be SUMOylated by SIZ1 in response to salt stress and the lysine (K)283 of MYB30 is essential for its SUMOylation. In contrast to wild-type MYB30, the MYB30(K283R) mutant failed to rescue the salt-sensitive phenotype of the myb30-2 mutant, indicating that SUMOylation of MYB30 is required for the salt-stress response. Through transcriptomic analysis, we identified a MYB30 target, alternative oxidase 1a (AOX1a). MYB30 binds the promoter of AOX1a and upregulates its expression in response to salt stress; however, MYB30(K283R) cannot bind the promoter of AOX1a. The cyanide (CN)-resistant alternative respiration (Alt) mediated by AOX is significantly reduced in the myb30-2 mutant through the loss of function of MYB30. As a result, the redox homeostasis is disrupted in the myb30-2 mutant compared with that in wild-type seedlings (WT) under salt conditions. The artificial elimination of excess reactive oxygen species partially rescues the salt-sensitive phenotype of the myb30-2 mutant, whereas after the exogenous application of SHAM, an inhibitor of AOXs and Alt respiration, the salt tolerance of Col-0 and the complemented plants decreased to a level similar to that observed in myb30-2. Finally, overexpression of AOX1a in myb30-2 confers WT-like salt tolerance compared with that of the myb30-2 mutant. Taken together, our results revealed a functional link between MYB30 and AOX1a, and indicated that SIZ1-mediated SUMOylation of MYB30 enhances salt tolerance by regulating Alt respiration and cellular redox homeostasis via AOX1a in Arabidopsis.
引用
收藏
页码:1157 / 1171
页数:15
相关论文
共 39 条
[1]   Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana [J].
Clifton, R ;
Lister, R ;
Parker, KL ;
Sappl, PG ;
Elhafez, D ;
Millar, AH ;
Day, DA ;
Whelan, J .
PLANT MOLECULAR BIOLOGY, 2005, 58 (02) :193-212
[2]   Alternative oxidases in Arabidopsis: A comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses [J].
Clifton, Rachel ;
Millar, A. Harvey ;
Whelan, James .
BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS, 2006, 1757 (07) :730-741
[3]   A novel myb oncogene homologue in Arabidopsis thaliana related to hypersensitive cell death [J].
Daniel, X ;
Lacomme, C ;
Morel, JB ;
Roby, D .
PLANT JOURNAL, 1999, 20 (01) :57-66
[4]   The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis [J].
De Clercq, Inge ;
Vermeirssen, Vanessa ;
Van Aken, Olivier ;
Vandepoele, Klaas ;
Murcha, Monika W. ;
Law, Simon R. ;
Inze, Annelies ;
Ng, Sophia ;
Ivanova, Aneta ;
Rombaut, Debbie ;
van de Cotte, Brigitte ;
Jaspers, Pinja ;
Van de Peer, Yves ;
Kangasjarvi, Jaakko ;
Whelan, James ;
Van Breusegem, Frank .
PLANT CELL, 2013, 25 (09) :3472-3490
[5]   ROS Generation in Peroxisomes and its Role in Cell Signaling [J].
del Rio, Luis A. ;
Lopez-Huertas, Eduardo .
PLANT AND CELL PHYSIOLOGY, 2016, 57 (07) :1364-1376
[6]   Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants [J].
Gill, Sarvajeet Singh ;
Tuteja, Narendra .
PLANT PHYSIOLOGY AND BIOCHEMISTRY, 2010, 48 (12) :909-930
[7]   Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis [J].
Ho, Lois H. M. ;
Giraud, Estelle ;
Uggalla, Vindya ;
Lister, Ryan ;
Clifton, Rachel ;
Glen, Angela ;
Thirkettle-Watts, Dave ;
Van Aken, Olivier ;
Whelan, James .
PLANT PHYSIOLOGY, 2008, 147 (04) :1858-1873
[8]   MMS21/HPY2 and SIZ1, Two Arabidopsis SUMO E3 Ligases, Have Distinct Functions in Development [J].
Ishida, Takashi ;
Yoshimura, Mika ;
Miura, Kenji ;
Sugimoto, Keiko .
PLOS ONE, 2012, 7 (10)
[9]   The SUMO E3 ligase, AtS1Z1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure [J].
Jin, Jing Bo ;
Jin, Yin Hua ;
Lee, Jiyoung ;
Miura, Kenji ;
Yoo, Chan Yul ;
Kim, Woe-Yeon ;
Van Oosten, Michael ;
Hyun, Youbong ;
Somers, David E. ;
Lee, Ilha ;
Yun, Dae-Jin ;
Bressan, Ray A. ;
Hasegawa, Paul M. .
PLANT JOURNAL, 2008, 53 (03) :530-540
[10]   Redox potential of GSH/GSSG couple: Assay and biological significance [J].
Jones, DP .
PROTEIN SENSORS AND REACTIVE OXYGEN SPECIES, PT B, THIOL ENZYMES AND PROTEINS, 2002, 348 :93-112