Adaptive Strategy of the Perennial Halophyte Grass Puccinellia tenuiflora to Long-Term Salinity Stress

Salinity stress influences plants throughout their entire life cycle. However, little is known about the response of plants to long-term salinity stress (LSS). In this study, Puccinellia tenuiflora, a perennial halophyte grass, was exposed to 300 mM NaCl for two years (completely randomized experiment design with three biological replicates). We measured the photosynthetic parameters and plant hormones and employed a widely targeted metabolomics approach to quantify metabolites. Our results revealed that LSS induced significant metabolic changes in P. tenuiflora, inhibiting the accumulation of 11 organic acids in the leaves and 24 organic acids in the roots and enhancing the accumulation of 15 flavonoids in the leaves and 11 phenolamides in the roots. The elevated accumulation of the flavonoids and phenolamides increased the ability of P. tenuiflora to scavenge reactive oxygen species. A comparative analysis with short-term salinity stress revealed that the specific responses to long-term salinity stress (LSS) included enhanced flavonoid accumulation and reduced amino acid accumulation, which contributed to the adaptation of P. tenuiflora to LSS. LSS upregulated the levels of abscisic acid in the leaves and ACC (a direct precursor of ethylene) in the roots, while it downregulated the levels of cytokinins and jasmonic acids in both the organs. These tolerance-associated changes in plant hormones would be expected to reprogram the energy allocation among growth, pathogen defense, and salinity stress response. We propose that abscisic acid, ethylene, cytokinins, and jasmonic acids may interact with each other to construct a salinity stress response network during the adaptation of P. tenuiflora to LSS, which mediates salinity stress response and significant metabolic changes. Our results provided novel insights into the plant hormone-regulated metabolic response of the plants under LSS, which can enhance our understanding of plant salinity tolerance.