Identification and analysis of microRNAs responsible for brown planthopper resistance in BPH14/BPH15 pyramiding rice

Background Rice farming faces a serious challenge from the brown planthopper (BPH), with the pyramiding of BPH14 and BPH15 genes delivering effective protection in elite rice strains. However, the molecular basis behind this resistance is still unclear. Results The study investigated miRNA levels in BPH14/BPH15 pyramiding line (B1415) and their recurrent parent (RP) under BPH infestation employing high-throughput sequencing and revealed 136 differentially expressed miRNAs (DEMs) among 550 known miRNAs. An integrated analysis highlighted that 587 miRNA-mRNA pairs linking 95 DEMs to 537 targeted genes were enriched in phenylpropanoid and lignin metabolism, circadian rhythms, and amino acid metabolism. The candidate DEMs, miR172d-3p, and miR396 family members were identified as negative regulators to decrease their target genes Os06g0708700 (encoding a nodulin-like protein) and Os11g0129700 (encoding an AP2 domain transcription factor), suggesting their key roles in rice against BPH. Conclusions Our investigation provides the first insights into miRNA-mediated defense mechanisms in the B1415. Identifying miRNAs and their target mRNAs in BPH resistance opens a new avenue for rice breeding programs, offering potential targets for improving pest resistance. Understanding these molecular interactions paves the way for developing more resistant rice cultivars, thereby contributing to sustainable rice production and food security. Overall design: To uncover miRNAs responsible for BPH resistance in B1415, we conducted small RNA sequencing and characterized small RNAs in the B1415 and RP plants infested by BPH at onset (B1415_0, RP_0), early infestation stage (B1415_early, RP_early), and late infestation stage (B1415_late, RP_late), revealing key miRNA-mRNA regulatory networks contributing to B1415's BPH resistance. The pyramiding line containing both BPH14/BPH15 genes (B1415) was created using the indica cartivar 'Wushansimiao' as the recurrent parent (RP).