Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner

Abstract 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 haloph...

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Main Authors: Ling Pan, Xu Hu, Li Liao, Tingchen Xu, Quanquan Sun, Minqiang Tang, Zhenbang Chen, Zhiyong Wang
Format: Article
Language:English
Published: BMC 2023-06-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04358-w
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author Ling Pan
Xu Hu
Li Liao
Tingchen Xu
Quanquan Sun
Minqiang Tang
Zhenbang Chen
Zhiyong Wang
author_facet Ling Pan
Xu Hu
Li Liao
Tingchen Xu
Quanquan Sun
Minqiang Tang
Zhenbang Chen
Zhiyong Wang
author_sort Ling Pan
collection DOAJ
description Abstract 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.
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spelling doaj.art-2ed908ca24064f73a99bec25f0ae15c92023-06-25T11:13:12ZengBMCBMC Plant Biology1471-22292023-06-0123111110.1186/s12870-023-04358-wLipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific mannerLing Pan0Xu Hu1Li Liao2Tingchen Xu3Quanquan Sun4Minqiang Tang5Zhenbang Chen6Zhiyong Wang7Key Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityDepartment of Crop and Soil Sciences, University of GeorgiaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan UniversityAbstract 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.https://doi.org/10.1186/s12870-023-04358-wSeashore PaspalumSalt ToleranceAntioxidant systemAmino acid metabolismLipid metabolism
spellingShingle Ling Pan
Xu Hu
Li Liao
Tingchen Xu
Quanquan Sun
Minqiang Tang
Zhenbang Chen
Zhiyong Wang
Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
BMC Plant Biology
Seashore Paspalum
Salt Tolerance
Antioxidant system
Amino acid metabolism
Lipid metabolism
title Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
title_full Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
title_fullStr Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
title_full_unstemmed Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
title_short Lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue-specific manner
title_sort lipid metabolism and antioxidant system contribute to salinity tolerance in halophytic grass seashore paspalum in a tissue specific manner
topic Seashore Paspalum
Salt Tolerance
Antioxidant system
Amino acid metabolism
Lipid metabolism
url https://doi.org/10.1186/s12870-023-04358-w
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