Exploring phenotypic plasticity in rice seed metabolism to unveil genetic factors addressing triple burden nutrition targets

Abstract

The world is grappling with a triple burden of malnutrition, characterized by the simultaneous rise in non-communicable diseases, undernutrition, and hidden hunger, especially in low- and middle-income countries with significant income inequality. Coincidentally, a significant portion of the population affected by these health-threatening conditions relies heavily on rice as a staple food. This underscores the vital role that rice can play in addressing the global malnutrition crisis and combating diet-related conditions. We systematically explored the diverse gene bank collections for phenotypic plasticity in seed metabolism for multi-nutritional properties and low glycemic index (GI) properties. We performed comprehensive genomics and metabolomics complemented with modeling analyses emphasizing the importance of OsSBEIIb along with additional candidate genes whose variations allowed us to produce target rice lines with lower GI and high PC (14-16%) in a high-yielding background. By integrating genetic techniques with classification models, this comprehensive approach identified candidate genes on chromosome 2 (qGI2.1/qAC2.1 spanning the region from 18.62 Mb to 19.95 Mb), exerting influence on low GI and high amylose. Notably, the phenotypic variant with high value was associated with the recessive allele of the starch branching enzyme 2b (sbeIIb). The genome-edited sbeIIb line confirmed low GI phenotype in milled rice grains. Comprehensive metabolomic analysis further revealed a metabolic shift in superior rice lines, favoring peptides and specific flavonoids, while high glycemic index rice lines showed an enrichment of certain triglycerides. The metabolite genome-wide association study (mGWAS) conducted on the whole grain rice collection revealed genetic variants influencing various metabolic traits during seed development and maturation. Further analysis linked genetic variants on chromosome 7 (6.06–6.43 Mb region) with complex epistatic interactions affecting multiple nutritional targets, including carbohydrate starch quality, glycemic index, antioxidant catechin levels, and grain pigmentation. This multi-omics approach identified rare gene bank accessions carrying variants in bHLH and IPT5 genes, associated with low glycemic index, increased catechin and total flavonoid content, and enhanced antioxidant activity. These accessions also exhibited strong anti-cancer properties in cell line assays. The metabolomic-driven insights from this study provide valuable information for breeding rice varieties with low glycemic index, improved nutritional profiles, and potential health benefits. Deploying this genetic knowledge we have introgressed low GI and high protein traits into multiple mega-varieties exhibiting high yielding attributes without compromising texture. These healthier rice varieties have been scaled in India and Philippines to more than 400 hectares and a dedicated processing plant being set up to scale the low GI and high protein milled rice and low GI food products for domestic and international markets.