Two Transcriptional Factors Antagonistically Fine-Tune MIR1863a to Balance Resistance and Yield Traits in Rice.

Immune activation usually trades off growth, leading to yield loss. Genes that coordinate resistance and yield are urgently required for crop improvement. MicroRNAs (miRNAs) provide rich candidates for coordinating resistance with yield. Here, we demonstrated that mutation of MIR1863a enhances blast disease resistance without yield loss accompanying increased panicle number. However, overexpression and mutation of MIR1863a both lead to compromised yield traits such as seed setting rate. The expression of MIR1863a was antagonistically regulated by two transcription factors, MADS51 and ESR1. MADS51 activates, whereas ESR1 suppresses MIR1863a in leaves and panicles during the growth period and upon pathogen invasion, thus avoiding a penalty in yield caused by excessive resistance. Consistent with the phenotype of mir1863a lines, mutation of MADS51 boosts blast disease resistance without yield loss. Moreover, the haplotypes of MADS51 and ESR1, which exhibit differential activity on the MIR1863a promoter, correlate with disease phenotypes in diverse Japonica and Indica rice accessions, implying a subspecies-specific evolution of these 'transcriptional factor-MIR1863a' models. Taken together, our results revealed a fine-tuning mechanism controlling an miRNA amounts to balance disease resistance and yield, advancing our understanding of the regulation of the resistance-yield trade-off.