Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

被引:284
作者
Nolan, Trevor M. [1 ]
Brennan, Benjamin [1 ]
Yang, Mengran [2 ]
Chen, Jiani [1 ]
Zhang, Mingcai [3 ]
Li, Zhaohu [3 ]
Wang, Xuelu [2 ]
Bassham, Diane C. [1 ]
Walley, Justin [4 ]
Yin, Yanhai [1 ]
机构
[1] Iowa State Univ, Dept Genet Dev & Cell Biol, Ames, IA 50011 USA
[2] Huazhong Agr Univ, Coll Life Sci & Technol, Wuhan 430070, Peoples R China
[3] China Agr Univ, Dept Agron, Beijing 100193, Peoples R China
[4] Iowa State Univ, Dept Plant Pathol & Microbiol, Ames, IA 50011 USA
基金
美国国家科学基金会;
关键词
REGULATED GENE-EXPRESSION; BRASSINOSTEROID SIGNAL-TRANSDUCTION; BINDING-PROTEIN; DROUGHT STRESS; 26S PROTEASOME; ARABIDOPSIS; DEGRADATION; FAMILY; BIN2; BZR1;
D O I
10.1016/j.devcel.2017.03.013
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Plants encounter a variety of stresses and must fine-tune their growth and stress-response programs to best suit their environment. BES1 functions as a master regulator in the brassinosteroid (BR) pathway that promotes plant growth. Here, we show that BES1 interacts with the ubiquitin receptor protein DSK2 and is targeted to the autophagy pathway during stress via the interaction of DSK2 with ATG8, a ubiquitin-like protein directing autophagosome formation and cargo recruitment. Additionally, DSK2 is phosphorylated by the GSK3-like kinase BIN2, a negative regulator in the BR pathway. BIN2 phosphorylation of DSK2 flanking its ATG8 interacting motifs (AIMs) promotes DSK2-ATG8 interaction, thereby targeting BES1 for degradation. Accordingly, loss-of-function dsk2 mutants accumulate BES1, have altered global gene expression profiles, and have compromised stress responses. Our results thus reveal that plants coordinate growth and stress responses by integrating BR and autophagy pathways and identify the molecular basis of this crosstalk.
引用
收藏
页码:33 / +
页数:21
相关论文
共 79 条
[1]   Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor [J].
Asami, T ;
Min, YK ;
Nagata, N ;
Yamagishi, K ;
Takatsuto, S ;
Fujioka, S ;
Murofushi, N ;
Yamaguchi, I ;
Yoshida, S .
PLANT PHYSIOLOGY, 2000, 123 (01) :93-99
[2]   The tumor necrosis factor receptor-associated factor (TRAF)-like family protein SEVEN IN ABSENTIA 2 (SINA2) promotes drought tolerance in an ABA-dependent manner in Arabidopsis [J].
Bao, Yan ;
Wang, Cuiting ;
Jiang, Chunmei ;
Pan, Jing ;
Zhang, Guobin ;
Liu, Hua ;
Zhang, Hongxia .
NEW PHYTOLOGIST, 2014, 202 (01) :174-187
[3]   The molecular circuitry of brassinosteroid signaling [J].
Belkhadir, Youssef ;
Jaillais, Yvon .
NEW PHYTOLOGIST, 2015, 206 (02) :522-540
[4]   CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING [J].
BENJAMINI, Y ;
HOCHBERG, Y .
JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) :289-300
[5]   Modification Site Localization Scoring: Strategies and Performance [J].
Chalkley, Robert J. ;
Clauser, Karl R. .
MOLECULAR & CELLULAR PROTEOMICS, 2012, 11 (05) :3-14
[6]   Expression profiling of the whole Arabidopsis Shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction [J].
Charrier, B ;
Champion, A ;
Henry, Y ;
Kreis, M .
PLANT PHYSIOLOGY, 2002, 130 (02) :577-590
[7]   ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci [J].
Chung, Taijoon ;
Phillips, Allison R. ;
Vierstra, Richard D. .
PLANT JOURNAL, 2010, 62 (03) :483-493
[8]   The Selective Autophagy Receptor p62 Forms a Flexible Filamentous Helical Scaffold [J].
Ciuffa, Rodolfo ;
Lamark, Trond ;
Tarafder, Abul K. ;
Guesdon, Audrey ;
Rybina, Sofia ;
Hagen, Wim J. H. ;
Johansen, Terje ;
Sachse, Carsten .
CELL REPORTS, 2015, 11 (05) :748-758
[9]   The Agony of Choice: How Plants Balance Growth and Survival under Water-Limiting Conditions [J].
Claeys, Hannes ;
Inze, Dirk .
PLANT PHYSIOLOGY, 2013, 162 (04) :1768-1779
[10]   Floral dip:: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana [J].
Clough, SJ ;
Bent, AF .
PLANT JOURNAL, 1998, 16 (06) :735-743