Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.