Genome-Wide Analysis of Nelumbo nucifera UXS Family Genes: Mediating Dwarfing and Aquatic Salinity Tolerance

Nelumbo nucifera (Lotus) is an economically important aquatic crop frequently challenged by abiotic stresses. The plant cell wall, a primary interface with the environment, undergoes dynamic remodeling to balance structural integrity with adaptation. UDP-glucuronic acid decarboxylase (UXS), a key enzyme synthesizing the nucleotide sugar precursor UDP-xylose, exists in distinct membrane-bound (e.g., Golgi) and cytosolic forms, channeling substrates into compartmentalized polysaccharide biosynthesis pathways and positioning the UXS family as a crucial regulator linking cell wall metabolism to plant adaptation. Here, we systematically characterized the NnUXS gene family in lotus through genome-wide identification, evolutionary synteny analysis, and functional validation. Integrated bioinformatic analysis revealed their physicochemical properties, motif patterns, and regulatory cis-elements, suggesting potential roles in growth and salt stress responses. Among the family, NnUXS3 was prioritized due to its preferentially upregulated in small plant architecture (SPA) varieties, its early induction under salt stress (0.5 days, 200 mM NaCl), and its highest predicted binding affinity for UDP-GlcA (−8.9 kcal/mol). Subsequent functional validation confirmed its dual role: heterologous overexpression in tobacco reduced plant height (47.22%) and leaf area (67.61%), while transient overexpression in lotus enhanced salt tolerance and shortened the petioles. This enhanced tolerance was achieved by upregulating key genes involved in polysaccharide biosynthesis (NnCSLC4, NnXTH22, NnCESA1) and antioxidant defense (NnSOD, NnPOD). Our findings establish NnUXS3 as a key mediator in balancing plant architecture and abiotic stress resilience. This work not only identifies a valuable genetic target for lotus breeding but also provides insights into the growth-stress trade-off, highlighting the importance of UXS subcellular localization in tailoring cell wall remodeling for environmental adaptation.