Origin and evolution of signaling pathways responsible for ascorbic acid synthesis and catabolism during plant terrestrialization

Abstract

This study comprehensively reveals the origin and evolution mechanisms of ascorbic acid (AsA) synthesis and breakdown pathways during plants' transition from water to land. By analyzing genomic data from 21 key plant species and transcriptomic data from the One thousand plants transcription project, we found that the L-galactose pathway emerged in green algae, with variations in the HIT domain of the rate-limiting enzyme GGP driving adaptive divergence between lower and higher plants. The galacturonic acid pathway integrated with the L-galactose pathway through the emergence of GalUR in bryophytes. The myo-inositol pathway became complete in bryophytes, and its refinement likely promoted dehydration adaptation via oxidative protection. The AsA recycling pathway (APX/MDHAR/DHAR) originated in red algae, while the appearance of AO enzymes is significantly related to rising oxygen levels during land colonization. Statistical analysis of 218 plant species shows that AsA content increases significantly with evolution, in line with heightened light and oxygen stress. This study explains the dynamic evolution of the AsA metabolic network during plant terrestrialization, highlighting how key gene families (e.g., GGP, GalUR, GLOase) undergo functional and structural domain divergence to boost antioxidant capacity and thus facilitate adaptation to terrestrial life. These findings offer a theoretical basis for improving crop stress resistance.