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

Abstract

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.

Trehalose 6-phosphate signalling and impact on crop yield

“…SWEET transporters may be important downstream targets for the regulation of sucrose allocation [19]. Wide ranging traits in four food security cereals are associated with T6P as seen through transgenic modification in maize and rice [13,24], natural genetic variation in wheat [43,45], rice [26] and sorghum [40] and chemical intervention with T6P precursors in wheat [42].…”

“…In this instance over expression of the TPP gene with a MADS6 promoter active during the flowering period in the phloem of female reproductive tissue, particularly companion cells, reduced T6P levels in pith tissue (Figure 2; [19]). This was associated with up-regulation of sucrose efflux regulators, SWEETs, which could explain enhanced sucrose bZIP and TPP produce differential T6P signal and sucrose accumulation in sweet sorghum stems (high T6P) and down-regulated stem sucrose, starch and cell wall metabolism (low T6P in grain sorghum [40]. Overexpression of a rice TPP gene in maize alters sucrose flow within maize cob in favour of kernels [19].…”

“…Sorghum, grown in tropical and sub-tropical regions, is the fifth most important cereal worldwide after maize, rice, wheat and barley. Li et al [40] published an important study that showed that T6P/SnRK1 could play a key role in the diverse assimilate partitioning patterns of sweet and grain sorghum ( Figure 2). Sweet sorghum is taller than grain sorghum and accumulates large amounts of sugar in the stem which gives it uses as a bioenergy crop.…”

Profiling Alternative 3′ Untranslated Regions in Sorghum using RNA-seq Data

“…The RNA-seq dataset (NCBI accession PRJNA413691) used for 3 UTR analysis was generated previously by us to study genes and networks associated with soluble sugar accumulation in internodes (internodes 2, 3, and 4, numbered from top to bottom) at four post-stem elongation stages from three sorghum genotypes, Rio, BTx406, and R9188 (Li et al, 2019a). The three genotypes contrast in the phenotypes of stem sugar accumulation: Rio accumulates high contents of sugar in stems during the post-flowering stages (∼20% Brix in the stemextracted juice), while BTx406 has a low stem sugar content (<10% Brix), with R9188 having an intermediate stem sugar content especially during the post-flowering stages (Li et al, 2019a). R9188 is an introgression line developed from the BTx406/Rio cross followed by one backcross to sweet sorghum Rio and contains the early flowering and dwarf loci introgressed from grain sorghum BTx406 (Ritter et al, 2004).…”

“…Its primary applications are to measure the gene expression levels and to calculate differential gene expression (DGE). Like in model species and major crops, RNA-seq has recently been widely employed in sorghum research and advanced our understanding in many aspects of sorghum including development (Davidson et al, 2012;Kebrom et al, 2017;Turco et al, 2017;Leiboff and Hake, 2019), accumulation of sugar/biomass (McKinley et al, 2016(McKinley et al, , 2018Mizuno et al, 2016Mizuno et al, , 2018Zhang L. M. et al, 2018Li et al, 2019aZhang et al, 2019;Hennet et al, 2020), stress responses and tolerance (Dugas et al, 2011;Gelli et al, 2014;Sui et al, 2015;Fracasso et al, 2016;Yang et al, 2018;Varoquaux et al, 2019), senescence (Johnson et al, 2015;Wu et al, 2016a), and regulation of miRNA and long non-coding RNA (Calvino et al, 2011;Sun et al, 2020).…”