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Mol. Cells 2011; 32(5): 421-429

Published online November 1, 2011

https://doi.org/10.1007/s10059-011-0101-z

© The Korean Society for Molecular and Cellular Biology

Arabidopsis TTR1 Causes LRR-Dependent Lethal Systemic Necrosis, rather than Systemic Acquired Resistance, to Tobacco Ringspot Virus

Moon Nam1,6,7, Serry Koh1,7, Sung Uk Kim1, Leslie L. Domier2, Jae Heung Jeon1, Hong Gi Kim3, Su-Heon Lee4, Andrew F. Bent5, and Jae Sun Moon1,*

1Green Bio-materials Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon 305-333, Korea, 2Department of Crop Sciences, USDA-ARS, Soybean/Maize Germplasm, Pathology, and Genetics Research Unit, Urbana, IL 61801, USA, 3Department of Agricultural Biology, Chungnam National University, Daejeon 305-764, Korea, 4Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration, Suwon 441-707, Korea, 5Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706, USA, 6 Present address: Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration, Suwon 441-707, Korea, 7These authors contributed equally to this work.

Correspondence to : *Correspondence: jsmoon@kribb.re.kr

Received: May 8, 2011; Revised: September 3, 2011; Accepted: September 3, 2011

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 a 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.

Keywords Arabidopsis, lethal systemic necrosis, TIR-NBS-LRR, tobacco ringspot virus, tolerance to tobacco ringspot virus 1

Article

Research Article

Mol. Cells 2011; 32(5): 421-429

Published online November 30, 2011 https://doi.org/10.1007/s10059-011-0101-z

Copyright © The Korean Society for Molecular and Cellular Biology.

Arabidopsis TTR1 Causes LRR-Dependent Lethal Systemic Necrosis, rather than Systemic Acquired Resistance, to Tobacco Ringspot Virus

Moon Nam1,6,7, Serry Koh1,7, Sung Uk Kim1, Leslie L. Domier2, Jae Heung Jeon1, Hong Gi Kim3, Su-Heon Lee4, Andrew F. Bent5, and Jae Sun Moon1,*

1Green Bio-materials Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon 305-333, Korea, 2Department of Crop Sciences, USDA-ARS, Soybean/Maize Germplasm, Pathology, and Genetics Research Unit, Urbana, IL 61801, USA, 3Department of Agricultural Biology, Chungnam National University, Daejeon 305-764, Korea, 4Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration, Suwon 441-707, Korea, 5Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706, USA, 6 Present address: Crop Protection Division, National Academy of Agricultural Science, Rural Development Administration, Suwon 441-707, Korea, 7These authors contributed equally to this work.

Correspondence to:*Correspondence: jsmoon@kribb.re.kr

Received: May 8, 2011; Revised: September 3, 2011; Accepted: September 3, 2011

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 a 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.

Keywords: Arabidopsis, lethal systemic necrosis, TIR-NBS-LRR, tobacco ringspot virus, tolerance to tobacco ringspot virus 1

Mol. Cells
Sep 30, 2023 Vol.46 No.9, pp. 527~572
COVER PICTURE
Chronic obstructive pulmonary disease (COPD) is marked by airspace enlargement (emphysema) and small airway fibrosis, leading to airflow obstruction and eventual respiratory failure. Shown is a microphotograph of hematoxylin and eosin (H&E)-stained histological sections of the enlarged alveoli as an indicator of emphysema. Piao et al. (pp. 558-572) demonstrate that recombinant human hyaluronan and proteoglycan link protein 1 (rhHAPLN1) significantly reduces the extended airspaces of the emphysematous alveoli by increasing the levels of TGF-β receptor I and SIRT1/6, as a previously unrecognized mechanism in human alveolar epithelial cells, and consequently mitigates COPD.

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