A Pyrophosphate-Based Energy Economy Enables Sucrose Storage in the Oxygen-Limited Sugarcane Culm

Bulky plant storage organs frequently experience restricted internal oxygen diffusion, yet how such tissues remain metabolically active while accumulating large quantities of storage carbohydrate remains unresolved. In sugarcane, the culm accumulates exceptionally high sucrose concentrations despite sustained respiration, suggesting that storage metabolism operates under specific energetic constraints. We estimated growth and maintenance respiration along developing sugarcane internodes using a composition-based carbon accounting framework across stages representing rapid elongation and mature storage. Growth respiration peaked in elongating internodes (3–6), whereas maintenance respiration increased progressively with maturation and dominated in mature storage tissue (internodes 10–12), demonstrating that mature internodes remain metabolically active despite cessation of structural growth. Despite this sustained metabolic demand, mature tissue accumulates sucrose rather than depleting it. Modelled internal oxygen limitation reduced ATP yield per unit substrate without suppressing metabolic activity. Under severe oxygen limitation the carbohydrate requirement for maintenance metabolism more than doubled in mature internodes, indicating that storage tissue operates with reduced energetic efficiency. We therefore propose that the sugarcane culm operates a pyrophosphate-supported metabolic configuration in which ATP demand is minimised and carbon is conserved. In this framework oxygen limitation alters the energetic currency of metabolism rather than suppressing metabolic activity, allowing cellular maintenance to continue without proportional consumption of stored sucrose. This interpretation is consistent with previously observed extensive recycling between triose-phosphates and hexose-phosphates during sucrose accumulation, suggesting that this cycling represents an ATP-conserving metabolic strategy rather than futile metabolism. These results indicate that sucrose storage in sugarcane reflects an alternative energy economy of an oxygenlimited storage organ, linking respiratory energetics, hypoxia and carbon partitioning in a C₄ crop.