Organ-specific transcriptional and metabolic adaptations of potato plants to limited phosphate availability prior and after tuberization

Abstract

While plants adapt to fluctuating phosphorus (P) availability in soils by enhancing phosphate acquisition or optimizing internal P-utilization, the spatiotemporal dynamics of these responses, particularly in crops, remain poorly understood. This study systematically investigated how and when potato organs respond to fluctuating P availability across different developmental stages using transcriptomic, metabolomic, and physiological analyses of leaves, roots, and tubers. Transcriptomic data revealed dynamic, organ- and stage-specific responses to P-deficiency, with the highest number of differentially expressed genes in leaves before tuberization and in roots during tuberization. P-deficiency led to a marked accumulation of proline in tubers and nitrogen-rich amino acids, particularly glutamine and asparagine, in roots and leaves. Carbohydrate metabolism exhibited severity- and time-dependent changes: severe P-deficiency triggered earlier, stronger, but transient carbohydrate accumulation, whereas medium P-deficiency led to a gradual and sustained increase in leaves and roots. Hexose phosphates and organic acids accumulated in roots under P-stress, especially severe P-stress, during early vegetative growth, followed by a marked reduction during tuberization. During tuber filling, severe P-deficiency reduced sucrose and starch in roots, decreased leaf starch but increased leaf sucrose, likely due to impaired translocation, and a decrease in tuber sucrose alongside increased starch due to reduced degradation. Under medium P-deficiency, sucrose and starch remained stable in leaves and tubers but declined in roots, reflecting a moderate shift in carbon allocation that maintained tuber development at the expense of root metabolism. These findings highlight the spatiotemporal regulation of metabolic and molecular responses to P-deficiency in potato and provide insights for improving nutrient use efficiency and stress resilience in crops.