Translational landscape provides insight into the molecular mechanism of heterosis in inter-subspecific hybrid rice

Abstract

Heterosis has been widely applied in crop breeding and has significantly improved grain yield worldwide. Many studies have attempted to elucidate heterosis from various perspectives; however, its genetic basis—especially at the translational level—remains elusive. In this study, we performed RNA-seq and ribosome profiling on the inter-subspecific hybrid rice ZY19 (Oryza sativa L. subsp. indica Kato × O. sativa L. subsp. japonica Kato) and its parental lines to examine genome-wide translational dynamics. Differential gene expression between the hybrid and its parents revealed a strong discordance between transcriptional and translational levels, and translational regulation appeared to buffer the transcriptional differences. Although additive and non-additive gene expression patterns shifted during translation, additive expression remained the predominant pattern at the translational level in the hybrid. Moreover, a high proportion of single-parent expression genes also exhibited additive expression. In the hybrid, allele-specific expression (ASE) was differentially regulated in transcription and translation. Notably, cis and trans-regulation tended to function independently in transcription, whereas they were more likely to act together in translation. Finally, we investigated the effects of various regulatory mechanisms and elements on translation and found that genes with more alternative splicing (AS) events had a lower translational efficiency (TE) than genes with fewer AS events. In addition, translation was repressed by the upstream open reading frames (uORFs), downstream open reading frames (dORFs), N⁶-methyladenosines (m⁶As) and microRNAs (miRNAs). Overall, our study provides new insights into the molecular mechanisms of heterosis in inter-subspecific hybrid rice.