Ascorbate-glutathione (AsA-GSH) cycle genes are vital for plant processes like stomatal regulation, nutrient uptake, and stress responses. However, the relationships between the origin and expansion of the AsA-GSH cycle genes and the adaptive evolution of land plants are still unclear. To investigate their evolutionary origins and functional differences, we first used phylogenetic and expression analyses of 2424 AsA-GSH genes (1059 APXs, 364 DHARs, 629 MDHARs, and 372 GRs) derived from 127 green plants to investigate their evolutionary history and functional divergence in green plants. The results highlighted a strong linkage between plant AsA-GSH cycle genes and their adaptation to environmental stress. In grapevine (Vitis vinifera), 16 AsA-GSH genes were identified and analyzed for gene structure, motifs, cis-regulatory elements, and transcription factors network. Gene expression profiling demonstrated their involvement in growth, hormonal regulation, and responses to biotic (Plasmopara viticola infection) and abiotic (cold, heat, salt, and drought) stresses. Functional validation showed that some of these grapevine genes, such as VvAPX6/7/8, VvDHAR1, VvMDHAR2, and VvGR2, are localized in diverse cellular compartments effectively mitigate oxidative stress through ROS scavenging. This study enhances our understanding of the evolutionary dynamics and functional diversification of AsA-GSH cycle genes in green plants, and the stress resilience in grapevine.

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