The role of different innate and environmental factors in Tm-22-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-22 gene confers resistance to some tobamoviruses by recognizing viral movement proteins. However, Tm-22-mediated resistance against ToMMV is not well known. Here, we found that ToMMV could infect wild-type but not Tm-22 transgenic Nicotiana benthamiana plants and could also infect tomato cultivar Moneymaker but not resistant cultivar Jili with homozygous Tm-22. Chimeric viral ToMMVToBRFV−MP with swapped ToMMV MP to MP of tomato brown rugose fruit virus could systemically infect Tm-22 transgenic N. benthamiana and tomato cultivars Jili plants. Further, transient expression of ToMMV MP in the leaves of Tm-22 transgenic N. benthamiana plants induced hypersensitive response-associated cell death, suggesting that the MP of ToMMV was the avirulent factor for the Tm-22 resistance gene. ToMMV could infect Tm-22-containing cultivar Jinpeng 1 but not Chaobei. Sequence analysis revealed that cultivars Chaobei and Jinpeng 1 were heterozygous, where Chaobei consists of Tm-22 and Tm-2 genes, while Jinpeng 1 consists of Tm-22 and tm-2 genes. Transient co-expression assays showed that both Tm-22 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-22 and heterozygous tomato containing Tm-22 and Tm-2 may exhibit more durable resistance to ToMMV than heterozygous tomato carrying Tm-22 and tm-2. Further, Tm-22 transgenic N. benthamiana and tomato cultivar Jili plants with silenced Tm-22 gene were susceptible to ToMMV. Also, silencing type-I J-domain MIP1 gene compromised Tm-22-mediated resistance to ToMMV in Tm-22 transgenic N. benthamiana and tomato cultivar Jili. Moreover, we found that viral RNA could accumulate in the systemic leaves of Tm-22 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-22 confers resistance to ToMMV by recognizing MP, and the resistance is regulated by the allele combinations, accumulation levels of Tm-22, MIP1, and the temperature.

Plant Immunity against Tobamoviruses

“…The homozygous tomato harboring Tm-2 2 and the heterozygous tomato containing Tm-2 2 and Tm-2, but not the heterozygous tomato containing Tm-2 2 and Tm-2, exhibit resistance to ToMMV. Tm-2 2 -mediated resistance is compromised at 35 • C, but not at 30 • C or lower temperatures [55]. Previous studies showed that the C-terminal 30-amino acid deletion of viral MP compromised Tm-2 2 -mediated resistance [54].…”

Plant Immunity against Tobamoviruses

“…The homozygous tomato harboring Tm-2 2 and the heterozygous tomato containing Tm-2 2 and Tm-2 , but not the heterozygous tomato containing Tm-2 2 and Tm-2 , exhibit resistance to ToMMV. Tm-2 2 -mediated resistance is compromised at 35 °C, but not at 30 °C or lower temperatures [ 55 ]. Previous studies showed that the C-terminal 30-amino acid deletion of viral MP compromised Tm-2 2 -mediated resistance [ 54 ].…”

“…Tm-2 and Tm-2 2 confer resistance to tobamoviruses, including TMV and ToMV, by recognizing the viral MP [42,[52][53][54]. Tm-2 2 also displays resistance to tomato mottle mosaic virus (ToMMV) by recognizing the MP, and the resistance is regulated by the allele combinations and the temperature [55]. The homozygous tomato harboring Tm-2 2 and the heterozygous tomato containing Tm-2 2 and Tm-2, but not the heterozygous tomato containing Tm-2 2 and Tm-2, exhibit resistance to ToMMV.…”