Unraveling the Contribution of Sucrose Metabolism Enzyme Family to Salt Tolerance in Rosa chinensis: A Genome-Wide Perspective

Salt stress severely inhibits plant growth and agricultural production by disrupting the balance of water and ions. To counteract this abiotic challenge, plants have evolved sophisticated mechanisms to modulate carbon allocation, prominently through the transcriptional regulation of sucrose metabolism-related genes (SMGs). This study focuses on the globally important horticultural crop, the rose (Rosa chinensis ‘Old Blush’), and provides the first systematic analysis of the RcSMG gene family. Using bioinformatics, 25 RcSMGs were identified, including 4 sucrose phosphate synthase (SPS), 6 sucrose synthase (SUS) and 15 invertase (INV) members. Phylogenetic analysis classified these SMGs into four distinct clades (SUS, SPS, CWINV, and NINV), with the INV family being the largest and the SPS family showing striking conservation across all four species. Evolutionary and collinearity analyses revealed that the SPS family is highly conserved, whereas the INV subfamily has undergone lineage-specific expansion. Protein analysis showed that all RcSMGs are hydrophilic. SPS proteins were found to be relatively unstable, while SUS and most INV members were stable. Further analysis of a protein–protein interaction (PPI) network showed that SPS proteins interact with enzymes in the metabolic pathway both upstream and downstream, forming a tightly regulated sucrose metabolism network. Transcriptome and promoter analyses revealed that RcSMGs exhibit tissue-specific expression patterns. The enrichment of diverse stress-responsive cis-regulatory elements in their promoter regions strongly implies a broad functional role in abiotic-stress adaptation, a hypothesis corroborated by transcriptome profiling under various stress conditions. Crucially, virus-induced gene silencing (VIGS) assays demonstrated that RcSUS3 and RcSPS1 positively regulate salt tolerance, while RcCWINV1 and RcVINV3 may act as negative regulators. In summary, this work provides the foundational framework for understanding the evolution, structure, and transcriptional regulation of the RcSMG family in roses. These findings highlight the important role of sucrose metabolism in stress resilience and provide a valuable basis for future molecular breeding to enhance stress resistance in horticultural crops.