Phenotypic and physiological responses of three Poa species under different soil moisture gradients and the molecular regulatory mechanisms of drought resistance

Background Under the influence of global climate change, drought events have become increasingly frequent on the Qinghai-Tibet Plateau, which constrains the utilization of native forages from the genus Poa and hampers the ecological restoration of alpine grasslands. Methods To reveal the drought adaptation patterns and the molecular mechanisms underlying the differentiation of drought resistance among various Poa germplasms, this study conducted a gradient water experiment on Poa pratensis 'Qinghai', Poa crymophila 'Qinghai', and Poa pratensis var. anceps Gaud. cv. 'Qinghai', measuring growth morphology, photosynthetic pigments, osmoregulatory substances, reactive oxygen species levels, and antioxidant enzyme activities. A comprehensive membership function method was employed for a comprehensive evaluation of drought tolerance at the seedling stage. Furthermore, a joint analysis of transcriptomics and proteomics was conducted on Poa species exhibiting significant differences in drought tolerance. Results With increasing drought stress intensity, the growth indicators and chlorophyll content of the three Poa species first increased and then decreased, with optimal performance under T50 treatment, suggesting that moderate water deficit can promote plant growth. There were significant germplasm differences in the response patterns of the osmoregulation system, reactive oxygen metabolism, and antioxidant defense system. Comprehensive evaluation yielded a drought tolerance ranking of Poa pratensis 'Qinghai' > Poa crymophila 'Qinghai' > Poa pratensis var. anceps Gaud. cv. 'Qinghai'. Omics analysis revealed that the strongly drought-tolerant Poa pratensis 'Qinghai' maintained photosynthetic homeostasis by regulating only 44 differentially expressed genes in photosynthetic pathways and 4 differentially expressed proteins, whereas the weakly drought-tolerant Poa pratensis var. anceps Gaud. cv. 'Qinghai' required the mobilization of 197 differentially expressed genes and 14 differentially expressed proteins for a compensatory response. Multi-omics enrichment analysis indicated that the photosynthesis pathway serves as the central pathway in Poa species 's response to drought stress. Drought conditions resulted in a widespread downregulation of related genes, including the PSII reaction center components (PsbP, PsbS, PsbW, PsbY, Psb28), the PSI reaction center components (PsaF, PsaN), and the F-type ATP synthase (alpha). Conversely, significant germplasm-specific expression differences were observed in the PSII reaction center component PsbR, the PSI subunit PsaE, the photosynthetic electron transport gene PetH, and the F-type ATP synthase delta. Conclusions Mild water deficit can stimulate the growth of Poa forage, while severe drought inhibits photosynthesis by damaging photosystem function, disrupting electron transport, and impairing photophosphorylation. The transcription and translation of photosynthetic pathways are synergistically coordinated in robust drought-tolerant germplasm, whereas these two regulatory processes are antagonistic in weak drought-tolerant germplasm, resulting in an imbalance in energy metabolism homeostasis. This study elucidates the drought adaptation strategies of alpine Poa species, providing a theoretical basis for the restoration of alpine grasslands and the breeding of drought-tolerant Poa forages.