The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus

Abstract Tomato mottle mosaic virus (ToMMV) poses a threat to production and quality of tomato fruits. The Tm-2 2 gene confers resistance to some tobamoviruses by recognizing viral movement proteins. However, Tm-2 2 -mediated resistance against ToMMV is not well known. Here, we found that ToMMV coul...

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Main Authors: Carlos Kwesi Tettey, Xiu-Qi Mu, Hua-Yu Ma, Xin-Yang Chen, Chao Geng, Yan-Ping Tian, Zhi-Yong Yan, Xiang-Dong Li
Format: Article
Language:English
Published: BMC 2023-03-01
Series:Phytopathology Research
Subjects:
Online Access:https://doi.org/10.1186/s42483-023-00162-4
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author Carlos Kwesi Tettey
Xiu-Qi Mu
Hua-Yu Ma
Xin-Yang Chen
Chao Geng
Yan-Ping Tian
Zhi-Yong Yan
Xiang-Dong Li
author_facet Carlos Kwesi Tettey
Xiu-Qi Mu
Hua-Yu Ma
Xin-Yang Chen
Chao Geng
Yan-Ping Tian
Zhi-Yong Yan
Xiang-Dong Li
author_sort Carlos Kwesi Tettey
collection DOAJ
description Abstract Tomato mottle mosaic virus (ToMMV) poses a threat to production and quality of tomato fruits. The Tm-2 2 gene confers resistance to some tobamoviruses by recognizing viral movement proteins. However, Tm-2 2 -mediated resistance against ToMMV is not well known. Here, we found that ToMMV could infect wild-type but not Tm-2 2 transgenic Nicotiana benthamiana plants and could also infect tomato cultivar Moneymaker but not resistant cultivar Jili with homozygous Tm-2 2 . Chimeric viral ToMMVToBRFV−MP with swapped ToMMV MP to MP of tomato brown rugose fruit virus could systemically infect Tm-2 2 transgenic N. benthamiana and tomato cultivars Jili plants. Further, transient expression of ToMMV MP in the leaves of Tm-2 2 transgenic N. benthamiana plants induced hypersensitive response-associated cell death, suggesting that the MP of ToMMV was the avirulent factor for the Tm-2 2 resistance gene. ToMMV could infect Tm-2 2 -containing cultivar Jinpeng 1 but not Chaobei. Sequence analysis revealed that cultivars Chaobei and Jinpeng 1 were heterozygous, where Chaobei consists of Tm-2 2 and Tm-2 genes, while Jinpeng 1 consists of Tm-2 2 and tm-2 genes. Transient co-expression assays showed that both Tm-2 2 and Tm-2 but not tm-2 could recognize ToMMV MP and induce hypersensitivity response-associated cell death in N. benthamiana leaves, suggesting that homozygous tomato harboring Tm-2 2 and heterozygous tomato containing Tm-2 2 and Tm-2 may exhibit more durable resistance to ToMMV than heterozygous tomato carrying Tm-2 2 and tm-2. Further, Tm-2 2 transgenic N. benthamiana and tomato cultivar Jili plants with silenced Tm-2 2 gene were susceptible to ToMMV. Also, silencing type-I J-domain MIP1 gene compromised Tm-2 2 -mediated resistance to ToMMV in Tm-2 2 transgenic N. benthamiana and tomato cultivar Jili. Moreover, we found that viral RNA could accumulate in the systemic leaves of Tm-2 2 transgenic N. benthamiana plants and tomato cultivar Jili at 35°C, but not at 20, 25, or 30°C. Altogether, our findings reveal that the Tm-2 2 confers resistance to ToMMV by recognizing MP, and the resistance is regulated by the allele combinations, accumulation levels of Tm-2 2 , MIP1, and the temperature.
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spelling doaj.art-a990009f1dee47f7a099f0346a032c862023-03-22T10:34:07ZengBMCPhytopathology Research2524-41672023-03-015111310.1186/s42483-023-00162-4The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virusCarlos Kwesi Tettey0Xiu-Qi Mu1Hua-Yu Ma2Xin-Yang Chen3Chao Geng4Yan-Ping Tian5Zhi-Yong Yan6Xiang-Dong Li7Shandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural UniversityAbstract Tomato mottle mosaic virus (ToMMV) poses a threat to production and quality of tomato fruits. The Tm-2 2 gene confers resistance to some tobamoviruses by recognizing viral movement proteins. However, Tm-2 2 -mediated resistance against ToMMV is not well known. Here, we found that ToMMV could infect wild-type but not Tm-2 2 transgenic Nicotiana benthamiana plants and could also infect tomato cultivar Moneymaker but not resistant cultivar Jili with homozygous Tm-2 2 . Chimeric viral ToMMVToBRFV−MP with swapped ToMMV MP to MP of tomato brown rugose fruit virus could systemically infect Tm-2 2 transgenic N. benthamiana and tomato cultivars Jili plants. Further, transient expression of ToMMV MP in the leaves of Tm-2 2 transgenic N. benthamiana plants induced hypersensitive response-associated cell death, suggesting that the MP of ToMMV was the avirulent factor for the Tm-2 2 resistance gene. ToMMV could infect Tm-2 2 -containing cultivar Jinpeng 1 but not Chaobei. Sequence analysis revealed that cultivars Chaobei and Jinpeng 1 were heterozygous, where Chaobei consists of Tm-2 2 and Tm-2 genes, while Jinpeng 1 consists of Tm-2 2 and tm-2 genes. Transient co-expression assays showed that both Tm-2 2 and Tm-2 but not tm-2 could recognize ToMMV MP and induce hypersensitivity response-associated cell death in N. benthamiana leaves, suggesting that homozygous tomato harboring Tm-2 2 and heterozygous tomato containing Tm-2 2 and Tm-2 may exhibit more durable resistance to ToMMV than heterozygous tomato carrying Tm-2 2 and tm-2. Further, Tm-2 2 transgenic N. benthamiana and tomato cultivar Jili plants with silenced Tm-2 2 gene were susceptible to ToMMV. Also, silencing type-I J-domain MIP1 gene compromised Tm-2 2 -mediated resistance to ToMMV in Tm-2 2 transgenic N. benthamiana and tomato cultivar Jili. Moreover, we found that viral RNA could accumulate in the systemic leaves of Tm-2 2 transgenic N. benthamiana plants and tomato cultivar Jili at 35°C, but not at 20, 25, or 30°C. Altogether, our findings reveal that the Tm-2 2 confers resistance to ToMMV by recognizing MP, and the resistance is regulated by the allele combinations, accumulation levels of Tm-2 2 , MIP1, and the temperature.https://doi.org/10.1186/s42483-023-00162-4Tomato mottle mosaic virusTm-2 2MIP1Movement proteinTm-2 2 allele compositionTemperature
spellingShingle Carlos Kwesi Tettey
Xiu-Qi Mu
Hua-Yu Ma
Xin-Yang Chen
Chao Geng
Yan-Ping Tian
Zhi-Yong Yan
Xiang-Dong Li
The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
Phytopathology Research
Tomato mottle mosaic virus
Tm-2 2
MIP1
Movement protein
Tm-2 2 allele composition
Temperature
title The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
title_full The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
title_fullStr The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
title_full_unstemmed The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
title_short The role of different innate and environmental factors in Tm-2 2 -mediated resistance to tomato mottle mosaic virus
title_sort role of different innate and environmental factors in tm 2 2 mediated resistance to tomato mottle mosaic virus
topic Tomato mottle mosaic virus
Tm-2 2
MIP1
Movement protein
Tm-2 2 allele composition
Temperature
url https://doi.org/10.1186/s42483-023-00162-4
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