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The tomato encode four functional  DCL  families, of which  DCL2  is poorly studied. Here, we generated loss-of-function mutants for a tomato  DCL2  gene,  dcl2b , and we identified its major role in defending against tomato mosaic virus in relation to both natural and manual infections. Genome-wide small RNA expression profiling revealed that  DCL2b  was required for the processing 22-nt small RNAs, including a few species of miRNAs. Interestingly, these  DCL2b -dependent 22-nt miRNAs functioned similarly to the  DCL1 -produced 22-nt miRNAs in  Arabidopsis  and could serve as triggers to generate a class of secondary siRNAs. In particular, the majority of secondary siRNAs were derived from plant defense genes when the plants were challenged with viruses. We also examined differentially expressed genes in  dcl2b  through RNA-seq and observed that numerous genes were associated with mitochondrial metabolism and hormone signaling under virus-free conditions. Notably, when the loss-of-function  dcl2b  mutant was challenged with tomato mosaic virus, a group of defense response genes was activated, whereas the genes related to lipid metabolism were suppressed. Together, our findings provided new insights into the roles of tomato  DCL2b  in small RNA biogenesis and in antiviral defense.

Tomato DCL2b is required for the biosynthesis of 22-nt small RNAs, the resulting secondary siRNAs, and the host defense against ToMV