Region-specific carbon metabolism underlies floridean starch accumulation in rhizoid-like filament cells of Pyropia yezoensis.

BACKGROUND

Pyropia yezoensis thalli exhibit pronounced cellular differentiation throughout their growth and development. In particular, basal rhizoid-like filament cells (R-region cells) differ significantly from other thallus cells in cell morphology, photosynthetic physiology and carbon metabolism. Previous studies have shown that abundant floridean starch granules accumulate in R-region cells, whereas only few floridean starch granules are present in neighbouring vegetative cells (V-region cells). However, the specific mechanism underlying floridean starch accumulation in R-region cells remains unclear.

RESULTS

In this study, basal cells of the P. yezoensis thallus were first divided, according to cell morphology, structural features and functional differences, into lower R-region cells and upper V-region cells. Anthrone colorimetric quantification, iodine staining and transmission electron microscopy collectively confirmed that floridean starch content was significantly higher in basal R-region cells than in upper V-region cells. By combining physiological measurements with integrated transcriptomic and metabolomic analyses, we further provided mechanistic insights into floridean starch accumulation in R-region cells. First, compared with V-region cells, R-region cells showed a significantly lower growth rate and globally reduced energy metabolic activity, features that are consistent with reduced carbon consumption and may contribute to the net accumulation of floridean starch. Second, on this basis, R-region cells promoted the directed allocation of carbon skeletons towards starch biosynthesis through enhanced expression of UGP (UDP-glucose pyrophosphorylase) genes and increased UGPase activity, thereby increasing UDP-glucose availability for floridean starch synthesis, while downregulating the expression of genes encoding starch-degradation-related enzymes. These coordinated changes promoted starch synthesis and suppressed starch degradation, jointly contributing to the efficient accumulation of floridean starch in R-region cells.

CONCLUSIONS

Based on the cellular differentiation characteristics of the P. yezoensis thallus, this study compares cells from distinct thallus regions and provides integrated physiological, biochemical, transcriptomic and metabolomic evidence that region-specific carbon metabolism is associated with floridean starch accumulation in R-region cells. These findings not only provide a theoretical basis for understanding thallus cell differentiation and carbon metabolism in P. yezoensis, but also advance our understanding of how differentiated cells in red algal thalli coordinate regional function with carbon storage.