A multi-omic resource of sorghum seed tissues for understanding nutrient synthesis and heat stress tolerance

Sorghum is an important C4 monocot crop, serving as a staple food in many arid and semi-arid regions worldwide. It provides essential vitamins, minerals, carbohydrates, fats, oils, and proteins, and ranking as the fifth most important source of nutrition globally. Sorghum seeds are gluten-free and rich in bioactive phenolic compounds, including flavonoids and phenolic acids. Despite its valuable nutritional profile, sorghum faces challenges such as the poor digestibility of kafirins, its predominant protein, deficiencies in essential amino acids, and variability in starch composition, all of which affect its functional properties. Furthermore, rising temperatures and altered precipitation patterns during seed grain filling stage further worsens these challenges. Seed development is a process that is notable for dynamic physiological and biochemical changes. The chemical composition of mature seeds is shaped by complex gene expression networks during seed development. Recent years have seen a surge in transcriptomic analyses investigating seed development in diverse plant species, including Arabidopsis thaliana, Oryza sativa, Triticum, Zea mays, Paeonia, Medicago truncatula, Brassica napus, Hordeum vulgare, and Glycine max. These studies have enabled scientists to identify gene networks associated with nutritional qualities, leading to improvements in seed quality. However, compared to other cereal crops, the genomic resources available for sorghum remain limited, resulting in fewer efforts to enhance its seed quality. To meet the growing global demand for gluten-free and antioxidant-rich sorghum-based foods, improving grain quality—particularly protein content and digestibility—using multi-omics data is essential. Advances in genetic engineering and multi-omics technologies offer valuable insights into the pathways that can be targeted to develop improved sorghum varieties, contributing to food security in the face of climate change. In the current study, we used multi-omics approaches—integrating genomics, transcriptomics, and metabolomics—to enhance sorghum's stress tolerance and nutritional profile. Firstly, a comprehensive seed tissue-specific transcriptomic atlas was developed. We analyzed spatiotemporal transcriptome (45 samples after pollination (1–9 dpa (days post anthesis) for the early whole seed, 6–25 dpa for the endosperm, and 10–25 dpa for the embryo) and metabolome profiles (5, 10, 15, 20, and 25 dpa) during sorghum seed development in the inbred line ‘BTx623’. The results revealed cell wall, embryo, and endosperm-specific genes, along with the regulatory networks associated with starch and protein biosynthesis. This data also identified seed tissue and stage-specific genes and pathways active during seed development under control conditions. Secondly, we investigated the effects of heat stress on sorghum seed development post-pollination, identifying genes and pathways affected heat stress during the grain-filling stage. Results indicated that heat stress during early seed development significantly impacts seed set and size, accelerating seed development at the cost of yield. Lastly, we report a core collection of 206 sorghum mutant lines with altered seed storage proteins. Using wet lab analyses, we evaluated total protein content and the composition of 23 amino acids, including 19 protein-bound and four non-protein amino acids. This work identified mutant lines with diverse profiles of essential and non-essential amino acids. These approaches provide valuable insights into the genetic and molecular mechanisms underlying seed quality and heat stress resilience. Findings from this research will serve as essential resources for the sorghum community and facilitate the breeding of higher-quality sorghum seeds in increasingly hot and dry environments.