A critical role of autophagy in plant resistance to necrotrophic fungal pathogens

被引:241
作者
Lai, Zhibing [1 ]
Wang, Fei [1 ]
Zheng, Zuyu [1 ]
Fan, Baofang [1 ]
Chen, Zhixiang [1 ]
机构
[1] Purdue Univ, Dept Bot & Plant Pathol, W Lafayette, IN 47907 USA
基金
美国国家科学基金会;
关键词
autophagy; necrotrophic pathogen; plant disease resistance; Botrytis cinerea; Alternaria brassicicola; WRKY33; INNATE IMMUNE-RESPONSE; CELL-DEATH; ARABIDOPSIS-THALIANA; BOTRYTIS-CINEREA; SALICYLIC-ACID; SACCHAROMYCES-CEREVISIAE; TRANSCRIPTION FACTOR; POLLEN GERMINATION; MICROBIAL PATHOGENS; DEFENSE RESPONSES;
D O I
10.1111/j.1365-313X.2011.04553.x
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Autophagy is a pathway for degradation of cytoplasmic components. In plants, autophagy plays an important role in nutrient recycling during nitrogen or carbon starvation, and in responses to abiotic stress. Autophagy also regulates age- and immunity-related programmed cell death, which is important in plant defense against biotrophic pathogens. Here we show that autophagy plays a critical role in plant resistance to necrotrophic pathogens. ATG18a, a critical autophagy protein in Arabidopsis, interacts with WRKY33, a transcription factor that is required for resistance to necrotrophic pathogens. Expression of autophagy genes and formation of autophagosomes are induced in Arabidopsis by the necrotrophic fungal pathogen Botrytis cinerea. Induction of ATG18a and autophagy by B. cinerea was compromised in the wrky33 mutant, which is highly susceptible to necrotrophic pathogens. Arabidopsis mutants defective in autophagy exhibit enhanced susceptibility to the necrotrophic fungal pathogens B. cinerea and Alternaria brassicicola based on increased pathogen growth in the mutants. The hypersusceptibility of the autophagy mutants was associated with reduced expression of the jasmonate-regulated PFD1.2 gene, accelerated development of senescence-like chlorotic symptoms, and increased protein degradation in infected plant tissues. These results strongly suggest that autophagy cooperates with jasmonate-and WRKY33-mediated signaling pathways in the regulation of plant defense responses to necrotrophic pathogens.
引用
收藏
页码:953 / 968
页数:16
相关论文
共 65 条
[11]   Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors [J].
Dove, SK ;
Piper, RC ;
McEwen, RK ;
Yu, JW ;
King, MC ;
Hughes, DC ;
Thuring, J ;
Holmes, AB ;
Cooke, FT ;
Michell, RH ;
Parker, PJ ;
Lemmon, MA .
EMBO JOURNAL, 2004, 23 (09) :1922-1933
[12]   Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4 [J].
Ferrari, S ;
Plotnikova, JM ;
De Lorenzo, G ;
Ausubel, FM .
PLANT JOURNAL, 2003, 35 (02) :193-205
[13]   An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination [J].
Fujiki, Yuki ;
Yoshimoto, Kohki ;
Ohsumi, Yoshinori .
PLANT PHYSIOLOGY, 2007, 143 (03) :1132-1139
[14]   Functional analysis of the Saccharomyces cerevisiae YFR021w/YGR223c/YPL100w ORF family suggests relations to mitochondrial/peroxisomal functions and amino acid signalling pathways [J].
Georgakopoulos, T ;
Koutroubas, G ;
Vakonakis, I ;
Tzermia, M ;
Prokova, V ;
Voutsina, A ;
Alexandraki, D .
YEAST, 2001, 18 (12) :1155-1171
[16]   The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea [J].
Govrin, EM ;
Levine, A .
CURRENT BIOLOGY, 2000, 10 (13) :751-757
[17]   Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris [J].
Guan, J ;
Stromhaug, PE ;
George, MD ;
Habibzadegah-Tari, P ;
Bevan, A ;
Dunn, WA ;
Klionsky, DJ .
MOLECULAR BIOLOGY OF THE CELL, 2001, 12 (12) :3821-3838
[18]   EXPLOITING THE TRIPLE RESPONSE OF ARABIDOPSIS TO IDENTIFY ETHYLENE-RELATED MUTANTS [J].
GUZMAN, P ;
ECKER, JR .
PLANT CELL, 1990, 2 (06) :513-523
[19]   Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene [J].
Hanaoka, H ;
Noda, T ;
Shirano, Y ;
Kato, T ;
Hayashi, H ;
Shibata, D ;
Tabata, S ;
Ohsumi, Y .
PLANT PHYSIOLOGY, 2002, 129 (03) :1181-1193
[20]   Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana [J].
Harrison-Lowe, Nicola J. ;
Olsen, Laura J. .
AUTOPHAGY, 2008, 4 (03) :339-348