Integrated transcriptomic and metabolomic analyses reveal the molecular mechanisms of sugar accumulation and yield trade-off in sugar beet.

BACKGROUND

The negative correlation between taproot yield and sugar content remains a persistent challenge in sugar beet (Beta vulgaris L.) breeding. This trade-off reflects the competitive partitioning of finite assimilated carbon between structural growth and vacuolar storage. However, the transcriptional and metabolic mechanisms underlying this shift remain poorly characterized.

METHODS

We integrated transcriptomic and widely-targeted metabolomic data across five developmental stages of taproots from two lines with contrasting phenotypes: a high-sugar/low-yield line (Group K) and a low-sugar/high-yield line (Group D).

RESULTS

Our analysis revealed that high sucrose accumulation is driven by minimized metabolic consumption rather than enhanced biosynthesis. While the high-yield line (Group D) sustained elevated expression of sucrose synthesis genes (SPS, SPP) alongside elevated expression through the tricarboxylic acid (TCA) cycle (CS, ACLY, MDH2) and nitrogen assimilation (GLUL, GAD) to fuel continuous cambial expansion, the high-sugar line (Group K) showed progressive attenuation of these primary metabolic pathways during maturation. Consequently, Group K exhibited depleted pools of citrate, malate, and glutamine, but highly accumulated sucrose and osmoprotectants like trehalose and raffinose. Weighted Gene Co-expression Network Analysis (WGCNA) identified a core co-expression module strongly correlated with the high-sugar trait. Within this module, transcription factors AP2, bHLH78, REM16, SRS3, and TIFY4b were identified as hub genes, suggesting possible regulatory roles in the suppression of growth-associated carbon consumption.

CONCLUSIONS

The yield-sugar trade-off in sugar beet appears to reflect differential carbon allocation between primary metabolic pathways and sucrose storage, associated with distinct transcriptional programs in the two lines. The identified transcription factor hubs may participate in regulating the balance between growth-associated carbon use and storage metabolism. These findings provide candidate molecular targets for future studies aimed at simultaneously improving yield and sugar content in sugar beet.