Seashore paspalum (Paspalum vaginatum) is a halophytic, warm-season grass which is closely related to various grain crops. Gene duplication plays an important role in plant evolution, conferring significant plant adaptation at the genomic level. Here, we identified 2,542 tandem duplicated genes (TDGs) in the P. vaginatum genome and estimated the divergence time of pairs of TDGs based on synonymous substitution rates (Ks). Expression of P. vaginatum TDGs resulted in enrichment in many GO terms and KEGG pathways when compared to four other closely-related species. The GO terms included: “ion transmembrane transporter activity,” “anion transmembrane transporter activity” and “cation transmembrane transport,” and KEGG pathways included “ABC transport.” RNA-seq analysis of TDGs showed tissue-specific expression under salt stress, and we speculated that P. vaginatum leaves became adapted to salt stress in the earlier whole-genome duplication (WGD; ~83.3 million years ago; Ma), whereas the entire P. vaginatum plant acquired a large number of TDGs related to salt stress in the second WGD (~23.3 Ma). These results can be used as a reference resource to accelerate salt-resistance research in other grasses and crops.

Soil salinization is a growing issue that limits agriculture globally. Understanding the mechanism underlying salt tolerance in halophytic grasses can provide new insights into engineering plant salinity tolerance in glycophytic plants. Seashore paspalum (Paspalum vaginatum Sw.) is a halophytic turfgrass and genomic model system for salt tolerance research in cereals and other grasses. However, the salt tolerance mechanism of this grass largely unknown. To explore the correlation between Na+ accumulation and salt tolerance in different tissues, we utilized two P. vaginatum accessions that exhibit contrasting tolerance to salinity. To accomplish this, we employed various analytical techniques including ICP-MS-based ion analysis, lipidomic profiling analysis, enzyme assays, and integrated transcriptomic and metabolomic analysis. Under high salinity, salt-tolerant P. vaginatum plants exhibited better growth and Na+ uptake compared to salt-sensitive plants. Salt-tolerant plants accumulated heightened Na+ accumulation in their roots, leading to increased production of root-sourced H2O2, which in turn activated the antioxidant systems. In salt-tolerant plants, metabolome profiling revealed tissue-specific metabolic changes, with increased amino acids, phenolic acids, and polyols in roots, and increased amino acids, flavonoids, and alkaloids in leaves. High salinity induced lipidome adaptation in roots, enhancing lipid metabolism in salt-tolerant plants. Moreover, through integrated analysis, the importance of amino acid metabolism in conferring salt tolerance was highlighted. This study significantly enhances our current understanding of salt-tolerant mechanisms in halophyte grass, thereby offering valuable insights for breeding and genetically engineering salt tolerance in glycophytic plants.

Background and aims Soil salinization is a growing problem for agriculture worldwide. To elucidate the mechanism underlying the salt tolerance of halophytes can offer a new angle for developing salt−tolerant crops. Seashore paspalum (Paspalum vaginatum Sw.) is a halophytic turfgrass and genomic model system for salt tolerance research in cereals and other grasses. However, knowledge regarding the tolerance mechanism of this halophyte remains largely unknown. Methods The two P.vaginatum accessions with contrasting salinity tolerance were employed to investigate the relationship between Na+ accumulation, lipid metabolism, antioxidant response and tissue−dependent salt tolerance using ICP−MS−based ion analysis, lipidomic profiling analysis, enzyme assay and integrated transcriptomic and metabolomic analysis, respectively. Gene−metabolite network analysis was carried to identify the significant TF genes and metabolites associated with salt tolerance in P.vaginatum plants. Results We found that salt−tolerant P.vaginatum built up tissue−specific strategies accompanied with Na+ accumulation in response to salt stress. Antioxidant system and amino acid metabolism were curial to maintain high salinity tolerance in leaves of P. vaginatum plants. On the contrary, lipid upregulation is the important components of the salt−tolerant mechanism in roots of P. vaginatum. Furthermore, 109 TF genes were identified to be linked to salt tolerance, conferring to salinity tolerance in this halophytic grass. Conclusions Our results expand our understanding of the underlying salt tolerance of seashore halophyte grass for the breeding and genetic engineering of salt tolerance in crop plants.

Salinization is increasingly a major factor limiting production worldwide. Revealing the mechanism of salt tolerance could help to create salt-tolerant crops and improve their yields. We reported a chromosome-scale genome sequence of the halophyte turfgrass Paspalum vaginatum, and provided structural evidence that it shared a common ancestor with Z. mays and S. bicolor. A total of 107 P. vaginatum germplasms were divided into two groups (China and foreign group) based on the re-sequenced data, and the grouping findings were consistent with the geographical origin. Genome-wide association study (GWAS) of visually scored wilting degree and withering rates identified highly significant QTL on chromosome 6. Combination with RNA-seq, we identified a significantly up-regulated gene under salt stress, which encodes 'High-affinity K+ Transporter 7' (PvHKT7), as strong candidates underlying the QTL. Overexpression of this gene in Arabidopsis thaliana significantly enhanced salt tolerance by increasing K+ absorption. This study adds new insights into salt-stress adaptation of P. vaginatum and serve as a resource for salt-tolerant improvement of grain crops.