Integration of metabolite and transcriptome profiles of cultivated and wild rice to unveil gene regulatory networks and key genes determining rice source and sink strength

Targeting source and sink strength for crop yield increase requires a comprehensive genetic and metabolic understanding of desirable source and sink features. We performed comprehensive metabolite and transcriptomic comparisons of the photosynthetic flag leaves and milky-stage developing grains of two cultivated rice varieties (Oryza sativa L. ssp. Indica cv. IR64 and Oryza sativa L. ssp. Japonica cv. Nipponbare) and two wild rice accessions (Oryza rufipogon and Oryza australiensis). The selected wild rice accessions had stronger source strength as evidenced by a higher photosynthesis rate and more abundance of primary metabolites in the photosynthetic leaves than the cultivated varieties. In contrast, cultivated varieties had efficient sink as grains were bigger and accumulated more sugars, amino acids, and fatty acids than the selected wild rice. Transcriptomic analyses identified 9,309 genes for efficient source in wild rice, enriched for biological pathways related to photosynthesis, carbohydrate metabolism, and sucrose transport. 7,062 genes, enriched for starch biosynthesis and lipid metabolism, were associated with the efficient sink strength in the cultivated varieties. Gene co-expression networks showed 267 hub genes for source strength in wild rice that included important genes for photosynthetic reactions and sucrose metabolism. 196 hub genes for sink strength in cultivated rice included genes involved in sucrose, amino acid, and fatty acid metabolism. Gene co-expression modules further identified the candidate transcription regulators, such as zinc finger proteins and NAC for source strength and MYB55/80 and MADS64 for sink strength. Moreover, our analyses suggested a complex interplay of phytohormones regulating rice source and sink strength.