Synergistic Response Mechanism and Gene Regulatory Network of Arundo donax Leaf Under Multiple Stresses

Arundo donax exhibits strong comprehensive stress resistance and high levels of crude protein and crude fiber, making it an ideal perennial forage crop. It adapts to various abiotic stresses and serves as a new model for studying plant stress response mechanisms. A. donax frequently encounters diverse environmental stresses during agricultural production, including drought, waterlogging, and temperature extremes. However, the response mechanisms of A. donax to multiple stresses remains elusive. By analyzing publicly available transcriptome data, we identified 9089, 19,272, and 8585 differentially expressed genes (DEGs) and 742 DEGs shared in the leaves of A. donax under drought, waterlogging, and cold conditions. The data showed that A. donax exhibits differential activation patterns in endogenous hormone signaling (jasmonate/gibberellin), energy metabolism (UDP-glucosyltransferase), and nitrogen metabolism pathways (acyltransferase) under these stresses. DEGs involved in the nitrogen metabolism and phenylpropanoid metabolism pathways were significantly enriched, while the gene expression patterns of these pathways varied among the drought, waterlogging, and cold stress conditions. Different stresses could affect the nitrogen accumulation in A. donax leaves. In addition, pairwise DEG comparisons indicated active roles of antioxidant defense and photosynthetic system in multiple stress responses. Physiological measurements validated these transcriptional changes: the activities of antioxidant enzymes (catalase (CAT), superoxide dismutase (SOD), and peroxidase (POD)) increased significantly, minimizing oxidative damage. Meanwhile, the photosynthetic pigments content also decreased in response to the three stresses. Soluble sugars, pyruvate, malate, and citrate, which are involved in energy metabolism in the leaves of A. donax, accumulated to sustain themaintenance of the plant’s own energy metabolism. In conclusion, our study revealed the transcriptome-based regulatory network related with synergistic response mechanisms of A. donax leaves under multiple stress conditions.