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United States Department of Agriculture

Agricultural Research Service

Research Project: SOYBEAN DISEASE AND PEST MANAGEMENT Title: Arabidopsis TTR1 causes LRR-dependent lethal systemic necrosis, rather than systemic acquired resistance, to Tobacco ringspot virus

Authors
item Nam, Moon -
item Koh, Serry -
item Im, Sung Uk -
item Domier, Leslie
item Jeon, Jae Heung -
item Kim, Hong Gi -
item Lee, Su-Heon -
item Bent, Andrew -
item Moon, Jae Sun -

Submitted to: Molecules and Cells
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 9, 2011
Publication Date: November 1, 2011
Citation: Nam, M., Koh, S., Im, S., Domier, L.L., Jeon, J., Kim, H., Lee, S., Bent, A.F., Moon, J. 2011. Arabidopsis TTR1 causes LRR-dependent lethal systemic necrosis, rather than systemic acquired resistance, to Tobacco ringspot virus. Molecules and Cells. 32:421-429.

Interpretive Summary: Tobacco ringspot virus (TRSV) infects and reduces yields in a broad range of crop plants. The genes involved in production of disease symptoms in TRSV-infected plants were studied in the model plant Arabidopsis thaliana. Most Arabidopsis varieties are tolerant to TRSV infection and infected plants display only mild symptoms, but some Arabidopsis varieties die within two weeks of inoculation with TRSV. In this study, we identified the gene that makes Arabidopsis sensitive to TRSV using a map-based cloning approach. The Arabidopsis gene resembled other genes that confer resistance to plant pathogens, but rather than making plants resistant to infection the gene induced a misdirected defense response that killed the entire plant. We also identified the defect in the gene that is responsible for the malfunction. Furthermore, we showed that the Arabidopsis gene produced the same lethal response to TRSV infection when introduced into tobacco plants. These experiments showed that resistance genes can sometimes interact with viruses to produce more severe disease than is induced by the virus alone. The results of this study will be of interest to scientists who are studying the interactions between pathogens and plant resistance genes.

Technical Abstract: Most Arabidopsis ecotypes display tolerance to the Tobacco ringspot virus (TRSV), but a subset of Arabidopsis ecotypes, including Estland (Est), develop lethal systemic necrosis (LSN), which differs from the localized hypersensitive responses (HRs) or systemic acquired resistance (SAR) characteristic of incompatible reactions. Neither viral replication nor the systemic movement of TRSV was restricted in tolerant or sensitive Arabidopsis ecotypes; therefore, the LSN phenotype shown in the sensitive ecotypes might not be due to viral accumulation. In the present study, we identified the Est TTR1 gene (tolerance to Tobacco ringspot virus 1) encoding a TIR-NBS-LRR protein that controls the ecotype-dependent tolerant/sensitive phenotypes by a map-based cloning method. The tolerant Col-0 ecotype Arabidopsis transformed with the sensitive Est TTR1 allele developed an LSN phenotype upon TRSV infection, suggesting that the Est TTR1 allele is dominant over the tolerant ttr1 allele of Col-0. Multiple sequence alignments of 10 tolerant ecotypes from those of eight sensitive ecotypes showed that 10 LRR amino acid polymorphisms were consistently distributed across the TTR1/ttr1 alleles. Site-directed mutagenesis of these amino acids in the LRR region revealed that two sites, L956S and K1124Q, completely abolished the LSN phenotype. VIGS study revealed that TTR1 is dependent on SGT1, rather than EDS1. The LSN phenotype by TTR1 was shown to be transferred to Nicotiana benthamiana, demonstrating functional conservation of TTR1 across plant families, which are involved in SGT-dependent defense responses, rather than EDS1-dependent signaling pathways.

Last Modified: 12/22/2014
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