A Brassica miRNA Regulates Plant Growth and Immunity through Distinct Modes of Action

In plants,high disease resistance often results in a reduction of yield.Therefore,breeding crops with balanced yield and disease resistance has become a major challenge.Recently,microRNA(miRNA)-mediated R gene turnover has been shown to be a protective mechanism used by plants to prevent autoimmunity in the absence of pathogens.However,whether these miRNAs play a role in plant growth and how miRNA-mediated R gene turnover responds to pathogen infection have rarely been explored.Here,we found that a Brassica miRNA,miR1885,targets both an immune receptor gene and a development-related gene for negative regulation through distinct modes of action.MiR1885 directly silences the TIR-NBS-LRR class of R gene BraTNL1 but represses the expression of the photosynthesis-related gene BraCP24 by targeting the Trans-Acting Silencing(TAS)gene BraTIR1 for trans-acting small interfering RNAs(tasiRNAs)-mediated silencing.We found that,under natural conditions,miR1885 was kept at low levels to maintain normal development and basal immunity but peaked during the floral transition to promote flowering.Interestingly,upon Turnip mosaic virus(TuMV)infection,miR1885-dependent trans-acting silencing of BraCP24 was enhanced to speed up the floral transition,whereas miR1885-mediated R gene turnover was overcome by TuMV-induced BraTNL1 expression,reflecting precise regulation of the arms race between plants and pathogens.Collectively,our results demonstrate that a single Brassica miRNA dynamically regulates both innate immunity and plant growth and responds to viral infection,revealing that Brassica plants have developed a sophisticated mechanism in modulating the interplay between growth,immunity,and pathogen infection.