Target of rapamycin signaling orchestrates growth-defense trade-offs in plants

被引:88
作者
De Vleesschauwer, David [1 ]
Filipe, Osvaldo [1 ]
Hoffman, Gena [2 ,3 ]
Seifi, Hamed Soren [1 ]
Haeck, Ashley [4 ]
Canlas, Patrick [2 ,3 ]
Van Bockhaven, Jonas [1 ]
De Waele, Evelien [1 ]
Demeestere, Kristof [4 ]
Ronald, Pamela [2 ,3 ,5 ]
Hofte, Monica [1 ]
机构
[1] Univ Ghent, Fac Biosci Engn, Dept Crop Protect, Lab Phytopathol, Coupure Links 653, B-9000 Ghent, Belgium
[2] Univ Calif Davis, Dept Plant Pathol, Davis, CA 95616 USA
[3] Univ Calif Davis, Genome Ctr, Davis, CA 95616 USA
[4] Univ Ghent, Fac Biosci Engn, Dept Sustainable Organ Chem & Technol, Res Grp EnVOC, Coupure Links 653, B-9000 Ghent, Belgium
[5] Joint Bioenergy Inst, Emeryville, CA 94608 USA
基金
美国国家科学基金会;
关键词
growth-defense trade-offs; jasmonic acid; plant defense; rice (Oryza sativa); salicylic acid; target of rapamycin (TOR); DISEASE RESISTANCE; INNATE IMMUNITY; BALANCING ACT; LIFE-SPAN; TOR; RICE; KINASE; GENE; EXPRESSION; NETWORK;
D O I
10.1111/nph.14785
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Plant defense to microbial pathogens is often accompanied by significant growth inhibition. How plants merge immune system function with normal growth and development is still poorly understood. Here, we investigated the role of target of rapamycin (TOR), an evolutionary conserved serine/threonine kinase, in the plant defense response. We used rice as a model system and applied a combination of chemical, genetic, genomic and cell-based analyses. We demonstrate that ectopic expression of TOR and Raptor (regulatory-associated protein of mTOR), a protein previously demonstrated to interact with TOR in Arabidopsis, positively regulates growth and development in rice. Transcriptome analysis of rice cells treated with the TOR-specific inhibitor rapamycin revealed that TOR not only dictates transcriptional reprogramming of extensive gene sets involved in central and secondary metabolism, cell cycle and transcription, but also suppresses many defense-related genes. TOR overexpression lines displayed increased susceptibility to both bacterial and fungal pathogens, whereas plants with reduced TOR signaling displayed enhanced resistance. Finally, we found that TOR antagonizes the action of the classic defense hormones salicylic acid and jasmonic acid. Together, these results indicate that TOR acts as a molecular switch for the activation of cell proliferation and plant growth at the expense of cellular immunity.
引用
收藏
页码:305 / 319
页数:15
相关论文
共 67 条
[1]   Ectopic expression of Arabidopsis Target of Rapamycin (AtTOR) improves water-use efficiency and yield potential in rice [J].
Bakshi, Achala ;
Moin, Mazahar ;
Kumar, M. Udaya ;
Reddy, Aramati Bindu Madhava ;
Ren, Maozhi ;
Datla, Raju ;
Siddiq, E. A. ;
Kirti, P. B. .
SCIENTIFIC REPORTS, 2017, 7
[2]   The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors [J].
Belkhadir, Youssef ;
Yang, Li ;
Hetzel, Jonathan ;
Dangl, Jeffery L. ;
Chory, Joanne .
TRENDS IN BIOCHEMICAL SCIENCES, 2014, 39 (10) :447-456
[3]   Brassinosteroid's multi-modular interaction with the general stress network customizes stimulus-specific responses in Arabidopsis [J].
Bjornson, Marta ;
Dandekar, Abhaya M. ;
Chory, Joanne ;
Dehesh, Katayoon .
PLANT SCIENCE, 2016, 250 :165-177
[4]   Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana [J].
Caldana, Camila ;
Li, Yan ;
Leisse, Andrea ;
Zhang, Yi ;
Bartholomaeus, Lisa ;
Fernie, Alisdair R. ;
Willmitzer, Lothar ;
Giavalisco, Patrick .
PLANT JOURNAL, 2013, 73 (06) :897-909
[5]   Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs [J].
Campos, Marcelo L. ;
Yoshida, Yuki ;
Major, Ian T. ;
Ferreira, Dalton de Oliveira ;
Weraduwage, Sarathi M. ;
Froehlich, John E. ;
Johnson, Brendan F. ;
Kramer, David M. ;
Jander, Georg ;
Sharkey, Thomas D. ;
Howe, Gregg A. .
NATURE COMMUNICATIONS, 2016, 7
[6]   Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light [J].
Chern, M ;
Fitzgerald, HA ;
Canlas, PE ;
Navarre, DA ;
Ronald, PC .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2005, 18 (06) :511-520
[7]   Connecting Growth and Defense: The Emerging Roles of Brassinosteroids and Gibberellins in Plant Innate Immunity [J].
De Bruyne, Lieselotte ;
Hofte, Monica ;
De Vleesschauwer, David .
MOLECULAR PLANT, 2014, 7 (06) :943-959
[8]   The DELLA Protein SLR1 Integrates and Amplifies Salicylic Acid- and Jasmonic Acid-Dependent Innate Immunity in Rice [J].
De Vleesschauwer, David ;
Seifi, Hamed Soren ;
Filipe, Osvaldo ;
Haeck, Ashley ;
Son Nguyen Huu ;
Demeestere, Kristof ;
Hofte, Monica .
PLANT PHYSIOLOGY, 2016, 170 (03) :1831-1847
[9]   Making sense of hormone-mediated defense networking: from rice to Arabidopsis [J].
De Vleesschauwer, David ;
Xu, Jing ;
Hofte, Minica .
FRONTIERS IN PLANT SCIENCE, 2014, 5 :1-15
[10]   Hormone defense networking in rice: tales from a different world [J].
De Vleesschauwer, David ;
Gheysen, Godelieve ;
Hofte, Monica .
TRENDS IN PLANT SCIENCE, 2013, 18 (10) :555-565