Dicer‐like2b suppresses the wiry leaf phenotype in tomato induced by tobacco mosaic virus

• Published in: The Plant journal : for cell and molecular biology 2023-12, Vol.116 (6), p.1737-1747
• Main Authors: Ma, Liqun, Zhang, Xi, Deng, Zhiqi, Zhang, Peiyu, Wang, Tian, Li, Ran, Li, Jinyan, Cheng, Ke, Wang, Jubin, Ma, Nan, Qu, Guiqin, Zhu, Benzhong, Fu, Daqi, Luo, Yunbo, Li, Feng, Zhu, Hongliang
• Format: Article
• Language: English
• Subjects: Bioinformatics; dicer; Genotype & phenotype; Leaves; miRNA; Mutants; Phenotypes; Plant virus diseases; Plant viruses; Primordia; RNA viruses; RNA-mediated interference; siRNA; Solanum lycopersicum; tasiRNA; Tobacco; Tobamovirus; tomato; Tomatoes; virus; Viruses; wiry leaf
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.16462

SUMMARY Dicer‐like (DCL) proteins are principal components of RNA silencing, a major defense mechanism against plant virus infections. However, their functions in suppressing virus‐induced disease phenotypes remain largely unknown. Here, we identified a role for tomato (Solanum lycopersicum) DCL2b in regulating the wiry leaf phenotype during defense against tobacco mosaic virus (TMV). Knocking out SlyDCL2b promoted TMV accumulation in the leaf primordium, resulting in a wiry phenotype in distal leaves. Biochemical and bioinformatics analyses showed that 22‐nt virus‐derived small interfering RNAs (vsiRNAs) accumulated less abundantly in slydcl2b mutants than in wild‐type plants, suggesting that SlyDCL2b‐dependent 22‐nt vsiRNAs are required to exclude virus from leaf primordia. Moreover, the wiry leaf phenotype was accompanied by upregulation of Auxin Response Factors (ARFs), resulting from a reduction in trans‐acting siRNAs targeting ARFs (tasiARFs) in TMV‐infected slydcl2b mutants. Loss of tasiARF production in the slydcl2b mutant was in turn caused by inhibition of miRNA390b function. Importantly, silencing SlyARF3 and SlyARF4 largely restored the wiry phenotype in TMV‐infected slydcl2b mutants. Our work exemplifies the complex relationship between RNA viruses and the endogenous RNA silencing machinery, whereby SlyDCL2b protects the normal development of newly emerging organs by excluding virus from these regions and thus maintaining developmental silencing. Significance Statement Dicer‐like2b protects tomato leaf primordia from tobacco mosaic virus infection and maintains the balance between trans‐acting small interfering RNAs and auxin response factors.