Unique starch biosynthesis pathways in wild rice revealed by multi-omics analyses

Abstract

Australian wild rice species (AWS) possess unique starch properties characterized by a slow digestibility rate. However, the genomic and transcriptomic variations of starch-synthesis-related genes (SSRGs) influencing starch physiochemical properties in AWS remain unclear. Here, we report comparative analyses of 72 SSRGs in wild species, including two AWS (O. meridionalis and Australian populations of O. rufipogon) and the domesticated rice gene pool. Our findings reveal that most SSRGs are more actively expressed in the early stages of seed development. Transcriptome analysis identified differential splicing patterns, with the starch synthesis pathways in Nipponbare and O. rufipogon being more similar than those in O. meridionalis. Three essential starch genes, GBSSI, SSIIa and BEIIb, were more active and had higher expression in AWS compared to Nipponbare, explaining the higher amylose content, gelatinization temperature, soft gel consistency and high retrogradation in the wild rice. Comparative genomics indicated that Asian domesticated rice evolved from a single ancestral allele of GBSSI (Wx^lv) and SSIIa (ALK^c), but two BEIIb alleles originated from O. rufipogon and O. nivara, the two wild rice species that are considered progenitors of Asian domesticated rice. Additionally, higher expressions of GBSSI, BEI and SSIIIa in O. meridionalis contribute to a slower starch digestibility rate, making its haplotypes valuable for breeding to develop slowly digested starch cultivars. These findings not only provide insight into the evolution of starch gene synthesis during domestication but also pave the way for unlocking desirable gene haplotypes of wild rice to improve starch quality in cultivated rice.