LAUSR

Significance Plants, like animals, have complex disease resistance systems in which receptors interact directly or indirectly with effectors of disease produced by pests and pathogens. To minimize the fitness cost of these systems to the plant, there are miRNAs that target the mRNAs of a family of receptor proteins required for disease resistance. Target site mimics of these miRNAs confer enhanced quantitative resistance in tomato against an oomycete and a bacterium. These findings are consistent with a role of the receptor proteins in quantitative disease resistance and show how blocking these miRNAs could be a useful approach in crop protection. Nucleotide binding site leucine-rich repeat (NLR) proteins of the plant innate immune system are negatively regulated by the miR482/2118 family miRNAs that are in a distinct 22-nt class of miRNAs with a double mode of action. First, they cleave the target RNA, as with the canonical 21-nt miRNAs, and second, they trigger secondary siRNA production using the target RNA as a template. Here, we address the extent to which the miR482/2118 family affects expression of NLR mRNAs and disease resistance. We show that structural differences of miR482/2118 family members in tomato (Solanum lycopersicum) are functionally significant. The predicted target of the miR482 subfamily is a conserved motif in multiple NLR mRNAs, whereas for miR2118b, it is a noncoding RNA target formed by rearrangement of several different NLR genes. From RNA sequencing and degradome data in lines expressing short tandem target mimic (STTM) RNAs of miR482/2118, we confirm the different targets of these miRNAs. The effect on NLR mRNA accumulation is slight, but nevertheless, the tomato STTM lines display enhanced resistance to infection with the oomycete and bacterial pathogens. These data implicate an RNA cascade of miRNAs and secondary siRNAs in the regulation of NLR RNAs and show that the encoded NLR proteins have a role in quantitative disease resistance in addition to dominant gene resistance that has been well characterized elsewhere. We also illustrate the use of STTM RNA in a biotechnological approach for enhancing quantitative disease resistance in highly bred cultivars.