ScDREBA5 Enhances Cold Tolerance by Regulating Photosynthetic and Antioxidant Genes in the Desert Moss Syntrichia caninervis

Extreme cold events, becoming more frequent, affect plant growth and development. Much is known about C-repeat binding transcription factor (CBF)-dependent cold-signaling pathways in plants. However, the CBF-independent regulatory pathway in angiosperms is unclear, and the cold-signaling pathways in non-angiosperms lacking CBFs, such as the extremely cold-tolerant desert moss Syntrichia caninervis, are largely unknown. In this study, we determined that fully hydrated S. caninervis without cold acclimation could tolerate a low-temperature of -16°C. Transcriptome analysis of S. caninervis under 4°C and -4°C treatments revealed that sugar and energy metabolism, lipid metabolism and antioxidant activity were altered in response to cold stress, and surprisingly, most photosynthesis-related genes were upregulated under cold treatment. Transcription factors analysis revealed that A-5 DREB genes, which share a common origin with CBFs, are the hubs in the freezing-stress response of S. caninervis, in which ScDREBA5 was upregulated ~1000-fold. Overexpressing ScDREBA5 significantly enhanced freezing tolerance in both S. caninervis and Physcomitrium patens by upregulating genes involved in photosynthetic and antioxidant pathways. This is the first study to uncover the mechanism regulating the cold-stress response in S. caninervis. Our findings increase our understanding of different cold-stress response strategies in non-angiosperms and provide valuable genetic resources for breeding cold-tolerant crops.