Integrated transcriptomic and metabolomic analysis reveals the salt tolerance mechanisms in Lagerstroemia indica

Lagerstroemia indica, a key summer flower in China, has weak salt tolerance. Understanding its molecular mechanisms is crucial for breeding.

In this study, we investigated the physiological responses and the changes of gene expression and metabolites in L. indica seedlings subjected to varying concentrations of NaCl using integrated transcriptomic and metabolomic approaches. The results showed that increasing NaCl concentrations significantly inhibited root elongation and stem growth. Significant differences were observed in SOD activities, POD activities, and MDA content among treatment groups. Salt stress markedly influenced gene expression and metabolite accumulation, with the 4‰ NaCl treatment group (Li4) exhibiting the highest number of DEGs and DAMs compared to the control (Li0). Transcriptome analysis revealed that pathways including plant hormone signal transduction, MAPK signaling, ribosome function, valine, leucine and isoleucine degradation, photosynthesis, and autophagy were significantly enriched. Weighted Gene Co-Expression Network Analysis (WGCNA) highlighted four key pathways: autophagy-other, peroxisome, valine, leucine and isoleucine degradation, and alanine, aspartate and glutamate metabolism. Metabolomic profiling indicated that salt stress induced the accumulation of specific amino acids (L-tyrosine, L-phenylalanine, L-arginine, e.g.) and secondary metabolites (4-indolecarboxaldehyde, indole-3-acrylic acid, N-benzylcarboxamide, e.g.), while reducing levels of others such as L-threonine, D-sucralose, and MEHP. These compounds may serve as potential biomarkers of salt stress response in L. indica. Association analysis further indicated that biosynthesis of amino acids and ascorbate and aldarate metabolism play key roles in the response of L. indica seedlings to salt stress. Further integrative analysis revealed strong correlations between metabolites and genes. Specifically, L-threonic acid was highly correlated with Lin_chr4_0495 (VTC2), Lin_chr14_0562 (GAE), and XLOC_006237 (VTC2), while D-saccharic acid showed a strong correlation with XLOC_023487 (ARATH).

In this study, we investigated the physiological changes in L. indica seedlings subjected to varying concentrations of NaCl treatment. The relationship between DEGs and DAMs in L. indica was analyzed, and changes in ascorbate and aldarate metabolism were further investigated. Notably, we observed for the first time in L. indica that the accumulation of L-threonic acid exhibits a significant positive correlation with key ascorbate and aldarate metabolism genes, namely VTC2 (Lin_chr4_0495), GAE (Lin_chr14_0562), and VTC2 (XLOC_006237). Additionally, the content of D-saccharic acid was found to be closely associated with the glucose metabolism-related gene ARATH (XLOC_023487). These specific molecular associations advance our understanding of the salt tolerance mechanism from the pathway level to precise metabolic markers and functional genes, thereby providing a direct operational foundation and candidate genes for marker-assisted selection or genetic engineering to improve salt tolerance in L. indica.