Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress
Abstract Ice plant (Mesembryanthemum crystallinum L.) is a halophyte and an inducible CAM plant. Ice plant seedlings display moderate salt tolerance, with root growth unaffected by 200 mM NaCl treatments, though hypocotyl elongation is hindered in salt-stressed etiolated seedlings. Superoxide anion...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
SpringerOpen
2025-01-01
|
| Series: | Botanical Studies |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40529-024-00450-y |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832585935164801024 |
|---|---|
| author | Li-Ching Hsieh Chia-Che Lee Kai-Fu Zhang Hui-Hsien Chang Cheng-Hsun Li Hsuan-Jung Huang Hungchen Emilie Yen |
| author_facet | Li-Ching Hsieh Chia-Che Lee Kai-Fu Zhang Hui-Hsien Chang Cheng-Hsun Li Hsuan-Jung Huang Hungchen Emilie Yen |
| author_sort | Li-Ching Hsieh |
| collection | DOAJ |
| description | Abstract Ice plant (Mesembryanthemum crystallinum L.) is a halophyte and an inducible CAM plant. Ice plant seedlings display moderate salt tolerance, with root growth unaffected by 200 mM NaCl treatments, though hypocotyl elongation is hindered in salt-stressed etiolated seedlings. Superoxide anion accumulation was prominent in cotyledons and primary leaves but decreased in root tissues over time, with no significant effect from salt treatment. Hydrogen peroxide levels initially surged in both control and salt-treated seedlings, with higher and more persistent accumulation in the salt-treated seedlings. The activities of H2O2-scavenging ascorbate-glutathione cycle enzymes ascorbate peroxidase (APX), monodehydroascorbate reductase, and dehydroascorbate reductase increased, while guaiacol-dependent peroxidase activity decreased and catalase activity showed no change, indicating APX activity as the primary response to salt stress. Salt-induced APX activities were detected mainly in the microsomal fraction for light-grown seedlings and the cytosolic fraction for etiolated seedlings, highlighting plastids as the primary site of ROS accumulation under salt stress. An RNA-seq analysis of etiolated seedlings revealed about 8% unigenes showing more than a four-fold change in expression after a 6-h 200 mM NaCl treatment. GO enrichment analysis indicated that differentially expressed genes (DEGs) with increased transcript abundance were associated with ion transport, antioxidant activity, and stress responses, while DEGs with decreased transcript abundance were linked to metabolic and biosynthesis processes such as ribosomal protein synthesis and cell wall formation. This indicates that salt stress hinders growth but enhances ion homeostasis and stress response mechanisms. The expression of all eight APX genes were induced by a 48-hour salt treatment, with varying expression patterns. For class III peroxidase family, 14 out of 53 identified unigenes qualified as DEGs. The time-course expression patterns revealed that the transcript levels of McPrx4.1, McPrx12.1, and McPrx12.3 increased, while McPrx60.3 decreased. These findings highlight the distinct roles of class III peroxidases in balancing plant growth and stress responses, advancing our understanding of the mechanisms behind salt tolerance in halophytes. This study comprehensively analyzed changes in gene expression, antioxidant enzyme activity, and ROS accumulation in ice plant seedlings. Unveiling these responses will advance our understanding of the growth–stress balance in the intrinsic salt tolerance in halophytes. |
| format | Article |
| id | doaj-art-a7688436783943f09c3b9a346700c8ef |
| institution | Kabale University |
| issn | 1999-3110 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | SpringerOpen |
| record_format | Article |
| series | Botanical Studies |
| spelling | doaj-art-a7688436783943f09c3b9a346700c8ef2025-01-26T12:21:35ZengSpringerOpenBotanical Studies1999-31102025-01-0166111710.1186/s40529-024-00450-yTranscriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stressLi-Ching Hsieh0Chia-Che Lee1Kai-Fu Zhang2Hui-Hsien Chang3Cheng-Hsun Li4Hsuan-Jung Huang5Hungchen Emilie Yen6Graduate Institute of Genomics and Bioinformatics, National Chung Hsing UniversityGraduate Institute of Genomics and Bioinformatics, National Chung Hsing UniversityDepartment of Life Sciences, National Chung Hsing UniversityDepartment of Life Sciences, National Chung Hsing UniversityDepartment of Life Sciences, National Chung Hsing UniversityDepartment of Life Sciences, National Chung Hsing UniversityDepartment of Life Sciences, National Chung Hsing UniversityAbstract Ice plant (Mesembryanthemum crystallinum L.) is a halophyte and an inducible CAM plant. Ice plant seedlings display moderate salt tolerance, with root growth unaffected by 200 mM NaCl treatments, though hypocotyl elongation is hindered in salt-stressed etiolated seedlings. Superoxide anion accumulation was prominent in cotyledons and primary leaves but decreased in root tissues over time, with no significant effect from salt treatment. Hydrogen peroxide levels initially surged in both control and salt-treated seedlings, with higher and more persistent accumulation in the salt-treated seedlings. The activities of H2O2-scavenging ascorbate-glutathione cycle enzymes ascorbate peroxidase (APX), monodehydroascorbate reductase, and dehydroascorbate reductase increased, while guaiacol-dependent peroxidase activity decreased and catalase activity showed no change, indicating APX activity as the primary response to salt stress. Salt-induced APX activities were detected mainly in the microsomal fraction for light-grown seedlings and the cytosolic fraction for etiolated seedlings, highlighting plastids as the primary site of ROS accumulation under salt stress. An RNA-seq analysis of etiolated seedlings revealed about 8% unigenes showing more than a four-fold change in expression after a 6-h 200 mM NaCl treatment. GO enrichment analysis indicated that differentially expressed genes (DEGs) with increased transcript abundance were associated with ion transport, antioxidant activity, and stress responses, while DEGs with decreased transcript abundance were linked to metabolic and biosynthesis processes such as ribosomal protein synthesis and cell wall formation. This indicates that salt stress hinders growth but enhances ion homeostasis and stress response mechanisms. The expression of all eight APX genes were induced by a 48-hour salt treatment, with varying expression patterns. For class III peroxidase family, 14 out of 53 identified unigenes qualified as DEGs. The time-course expression patterns revealed that the transcript levels of McPrx4.1, McPrx12.1, and McPrx12.3 increased, while McPrx60.3 decreased. These findings highlight the distinct roles of class III peroxidases in balancing plant growth and stress responses, advancing our understanding of the mechanisms behind salt tolerance in halophytes. This study comprehensively analyzed changes in gene expression, antioxidant enzyme activity, and ROS accumulation in ice plant seedlings. Unveiling these responses will advance our understanding of the growth–stress balance in the intrinsic salt tolerance in halophytes.https://doi.org/10.1186/s40529-024-00450-yIce plantHalophyteHydrogen peroxidePeroxidaseTranscriptome |
| spellingShingle | Li-Ching Hsieh Chia-Che Lee Kai-Fu Zhang Hui-Hsien Chang Cheng-Hsun Li Hsuan-Jung Huang Hungchen Emilie Yen Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress Botanical Studies Ice plant Halophyte Hydrogen peroxide Peroxidase Transcriptome |
| title | Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress |
| title_full | Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress |
| title_fullStr | Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress |
| title_full_unstemmed | Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress |
| title_short | Transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant (Mesembryanthemum crystallinum L.) under salt stress |
| title_sort | transcriptomic and enzymatic analysis of peroxidase families at the early growth stage of halophyte ice plant mesembryanthemum crystallinum l under salt stress |
| topic | Ice plant Halophyte Hydrogen peroxide Peroxidase Transcriptome |
| url | https://doi.org/10.1186/s40529-024-00450-y |
| work_keys_str_mv | AT lichinghsieh transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT chiachelee transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT kaifuzhang transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT huihsienchang transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT chenghsunli transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT hsuanjunghuang transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress AT hungchenemilieyen transcriptomicandenzymaticanalysisofperoxidasefamiliesattheearlygrowthstageofhalophyteiceplantmesembryanthemumcrystallinumlundersaltstress |