Virus resistance induced by NB-LRR proteins involves Argonaute4-dependent translational control

被引:96
作者
Bhattacharjee, Saikat [1 ]
Zamora, Alejandro [1 ]
Azhar, Muhammad Tehseen [1 ]
Sacco, Melanie A. [1 ]
Lambert, Lester H. [1 ]
Moffett, Peter [1 ]
机构
[1] Boyce Thompson Inst Plant Res, Ithaca, NY 14850 USA
基金
美国国家科学基金会;
关键词
NBS-LRR; plant disease resistance; RNA silencing; Argonaute; translational control; TOBACCO MOSAIC-VIRUS; DISEASE RESISTANCE; NICOTIANA-BENTHAMIANA; ARABIDOPSIS-THALIANA; CONFER RESISTANCE; COAT PROTEIN; HYPERSENSITIVE RESPONSE; PSEUDOMONAS-SYRINGAE; MEDIATED RESISTANCE; SIRNA ACCUMULATION;
D O I
10.1111/j.1365-313X.2009.03832.x
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
P>Active resistance to viruses is afforded by plant disease resistance (R) genes, which encode proteins with nucleotide-binding (NB) and leucine-rich repeat (LRR) domains. Upon recognition of pathogen-derived elicitors, these NB-LRR proteins are thought to initiate a number of signaling pathways that lead to pathogen restriction. However, little is known about the molecular mechanisms that ultimately curtail virus accumulation. Here, we show that the co-expression of a plant NB-LRR protein with its cognate elicitor results in an antiviral response that inhibits the translation of virus-encoded proteins in Nicotiana benthamiana. This antiviral response is dependent on viral cis elements, and, upon activation of the NB-LRR protein, viral transcripts accumulate but do not associate with ribosomes. The induced inhibition of viral transcript translation and NB-LRR-mediated virus resistance were compromised by the downregulation of Argonaute4-like genes. Argonaute proteins have been implicated in small RNA-mediated RNA degradation, and in degradation-independent translational control. Our results suggest that the engagement of Argonaute proteins in the specific translational control of viral transcripts is a key factor in virus resistance mediated by NB-LRR proteins.
引用
收藏
页码:940 / 951
页数:12
相关论文
共 58 条
[1]   ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis [J].
Agorio, Astrid ;
Vera, Pablo .
PLANT CELL, 2007, 19 (11) :3778-3790
[2]   The polerovirus silencing suppressor PO targets ARGONAUTE proteins for degradation [J].
Baumberger, Nicolas ;
Tsai, Ching-Hsui ;
Lie, Miranda ;
Havecker, Ericka ;
Baulcombe, David C. .
CURRENT BIOLOGY, 2007, 17 (18) :1609-1614
[3]   The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato [J].
Bendahmane, A ;
Kohm, BA ;
Dedi, C ;
Baulcombe, DC .
PLANT JOURNAL, 1995, 8 (06) :933-941
[4]   Agrobacterium transient expression system as a tool for the isolation of disease resistance genes:: application to the Rx2 locus in potato [J].
Bendahmane, A ;
Querci, M ;
Kanyuka, K ;
Baulcombe, DC .
PLANT JOURNAL, 2000, 21 (01) :73-81
[5]   Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato [J].
Bendahmane, A ;
Farnham, G ;
Moffett, P ;
Baulcombe, DC .
PLANT JOURNAL, 2002, 32 (02) :195-204
[6]   The Rx gene from potato controls separate virus resistance and cell death responses [J].
Bendahmane, A ;
Kanyuka, K ;
Baulcombe, DC .
PLANT CELL, 1999, 11 (05) :781-791
[7]   The polerovirus F box protein PO targets ARGONAUTE1 to suppress RNA silencing [J].
Bortolamiol, Diane ;
Pazhouhandeh, Maghsoud ;
Marrocco, Katia ;
Genschik, Pascal ;
Ziegler-Graff, Veronique .
CURRENT BIOLOGY, 2007, 17 (18) :1615-1621
[8]   Widespread translational inhibition by plant miRNAs and siRNAs [J].
Brodersen, Peter ;
Sakvarelidze-Achard, Lali ;
Bruun-Rasmussen, Marianne ;
Dunoyer, Patrice ;
Yamamoto, Yoshiharu Y. ;
Sieburth, Leslie ;
Voinnet, Olivier .
SCIENCE, 2008, 320 (5880) :1185-1190
[9]   The plant gene CCD1 selectively blocks cell death during the hypersensitive response to cauliflower mosaic virus infection [J].
Cawly, J ;
Cole, AB ;
Király, L ;
Qiu, WP ;
Schoelz, JE .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2005, 18 (03) :212-219
[10]   Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens [J].
Cooley, MB ;
Pathirana, S ;
Wu, HJ ;
Kachroo, P ;
Klessig, DF .
PLANT CELL, 2000, 12 (05) :663-676