Multi-omics analyses reveal mechanism for high resistant starch formation in an indica rice SSIIIa mutant

Soluble starch synthase IIIa (SSIIIa) is a key enzyme involved in amylopectin biosynthesis in rice, and deficiency of SSIIIa results in high content of resistant starch, which is benefit to human health. However, little is known about metabolic differences and carbon re-allocation in the seeds of the indica rice ss3a mutant. We found that SSIIIa deficiency impaired the storage of starch, but increased the soluble sugars, free amino acids and lipids. By multi-omic analyses, we found inactivation of SSIIIa triggered carbon repartitioning by downregulating sucrose synthase, grain incomplete filling 1, fructokinase and hexokinase (HK), and promoted the accumulation of soluble sugars. Meanwhile, the downregulation of HK and upregulation of plastidic phosphoglucomutase reduced the carbon flow through glycolysis and promoted glycogenesis. The downregulation of OsbZIP58 and the deleterious effect on ribosome formation might result in the reduction of storage protein synthesis and increased free amino acids content in ss3a. The higher levels of amylose and lipids could form more amylose-lipid complexes (starch phospholipids), resulting in a higher resistant starch content. Taken together, our study unraveled a functional cross talk between starch, protein and lipids in rice endosperm during seed development of ss3a, providing new insights for formation of high resistant starch in rice.