Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> 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, <i>Puccinellia tenuiflora</i>, a perennial halophyte grass, was exposed to 300 mM NaCl for two years (completely...

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Main Authors: Lei Han, Zhanwu Gao, Luhao Li, Changyou Li, Houxing Yan, Binbin Xiao, Yimeng Ma, Huan Wang, Chunwu Yang, Hongwei Xun
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/23/3445
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author Lei Han
Zhanwu Gao
Luhao Li
Changyou Li
Houxing Yan
Binbin Xiao
Yimeng Ma
Huan Wang
Chunwu Yang
Hongwei Xun
author_facet Lei Han
Zhanwu Gao
Luhao Li
Changyou Li
Houxing Yan
Binbin Xiao
Yimeng Ma
Huan Wang
Chunwu Yang
Hongwei Xun
author_sort Lei Han
collection DOAJ
description 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, <i>Puccinellia tenuiflora</i>, 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 <i>P. tenuiflora</i>, 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 <i>P. tenuiflora</i> 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 <i>P. tenuiflora</i> 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 <i>P. tenuiflora</i> 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.
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spelling doaj-art-6500836ec21a4a2c8dbf6aa42f28e8672025-08-20T01:55:37ZengMDPI AGPlants2223-77472024-12-011323344510.3390/plants13233445Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity StressLei Han0Zhanwu Gao1Luhao Li2Changyou Li3Houxing Yan4Binbin Xiao5Yimeng Ma6Huan Wang7Chunwu Yang8Hongwei Xun9Key Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaTourism and Geographical Science Institute, Baicheng Normal University, Baicheng 137000, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaSchool of Life Science, Jilin Normal University, Siping 136000, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaDepartment of Agronomy, Jilin Agricultural University, Changchun 130018, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaKey Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun 130024, ChinaSalinity 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, <i>Puccinellia tenuiflora</i>, 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 <i>P. tenuiflora</i>, 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 <i>P. tenuiflora</i> 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 <i>P. tenuiflora</i> 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 <i>P. tenuiflora</i> 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.https://www.mdpi.com/2223-7747/13/23/3445<i>Puccinellia tenuiflora</i>salinity stressmetabolitesplant hormones
spellingShingle Lei Han
Zhanwu Gao
Luhao Li
Changyou Li
Houxing Yan
Binbin Xiao
Yimeng Ma
Huan Wang
Chunwu Yang
Hongwei Xun
Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
Plants
<i>Puccinellia tenuiflora</i>
salinity stress
metabolites
plant hormones
title Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
title_full Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
title_fullStr Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
title_full_unstemmed Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
title_short Adaptive Strategy of the Perennial Halophyte Grass <i>Puccinellia tenuiflora</i> to Long-Term Salinity Stress
title_sort adaptive strategy of the perennial halophyte grass i puccinellia tenuiflora i to long term salinity stress
topic <i>Puccinellia tenuiflora</i>
salinity stress
metabolites
plant hormones
url https://www.mdpi.com/2223-7747/13/23/3445
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