DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica
Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica , but the mechanisms underlying the priming and memory processes remain unclea...
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| Published in | PLoS genetics Vol. 17; no. 4; p. e1009549 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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United States
Public Library of Science
30.04.2021
Public Library of Science (PLoS) |
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| Abstract | Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant
Boea hygrometrica
, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the
B
.
hygrometrica
genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including
pre-mRNA-splicing factor 38A
,
vacuolar amino acid transporter 1-like
, and
UDP-sugar pyrophosphorylase
, which may contribute directly or indirectly to the improvement of dehydration tolerance in
B
.
hygrometrica
plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation. |
|---|---|
| AbstractList | Specific drought- and desiccation-induced proteins, such as late embryogenesis abundant (LEA) proteins, early light-inducible proteins (ELIPs), small heat shock proteins (sHSPs), and antioxidative enzymes, may act directly as protectants during desiccation and rehydration or as enzymes that catalyze the synthesis of antioxidants protect against intracellular oxidative damage [9,10]. [...]genes that provide altered responses (changes in the transcription rate or transcript abundance) in subsequent stress episodes were referred to as ‘memory genes’, whereas those genes responding similarly to each stress episode form the ‘non-memory’ category [12,19,21]. Previous global transcriptome and gas chromatography–mass spectrometry (GC–MS)-based metabolomics analyses have revealed the putative involvement of genes related to autophagy, ubiquitination, and ABA signal transduction, as well as metabolites such as maltose, glutaric acid, L-tryptophan, and α-tocopherol in the process of drought acclimation-induced RDT acquisition [28,29]. [...]the photosynthetic efficiency of dehydrated leaves from neither non-acclimated control groups (FD, F4D, and F18D) nor RDT-erased acclimated plants (A18D) restored to normal levels after rehydration (FDR, F4DR, F18DR, and A18DR), although their leaf RWC was rapidly recovered to approximately 80%. [...]a significant increase (p < 0.01) in leaf relative electrical conductivity (REC) was observed in all fresh plants subjected to dehydration stress (SD/F, FD/F, AD/A, A4D/A4, F4D/F4, A18D/A18, and F18D/F18), but it could be restored only in the plants that acquired or maintained RDT (A/SD, ADR/AD, and A4DR/A4D) (Fig 1D). Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation.Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation. Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation. Specific drought- and desiccation-induced proteins, such as late embryogenesis abundant (LEA) proteins, early light-inducible proteins (ELIPs), small heat shock proteins (sHSPs), and antioxidative enzymes, may act directly as protectants during desiccation and rehydration or as enzymes that catalyze the synthesis of antioxidants protect against intracellular oxidative damage [9,10]. [...]genes that provide altered responses (changes in the transcription rate or transcript abundance) in subsequent stress episodes were referred to as ‘memory genes’, whereas those genes responding similarly to each stress episode form the ‘non-memory’ category [12,19,21]. Previous global transcriptome and gas chromatography–mass spectrometry (GC–MS)-based metabolomics analyses have revealed the putative involvement of genes related to autophagy, ubiquitination, and ABA signal transduction, as well as metabolites such as maltose, glutaric acid, L-tryptophan, and α-tocopherol in the process of drought acclimation-induced RDT acquisition [28,29]. [...]the photosynthetic efficiency of dehydrated leaves from neither non-acclimated control groups (FD, F4D, and F18D) nor RDT-erased acclimated plants (A18D) restored to normal levels after rehydration (FDR, F4DR, F18DR, and A18DR), although their leaf RWC was rapidly recovered to approximately 80%. [...]a significant increase (p < 0.01) in leaf relative electrical conductivity (REC) was observed in all fresh plants subjected to dehydration stress (SD/F, FD/F, AD/A, A4D/A4, F4D/F4, A18D/A18, and F18D/F18), but it could be restored only in the plants that acquired or maintained RDT (A/SD, ADR/AD, and A4DR/A4D) (Fig 1D). Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica , but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B . hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A , vacuolar amino acid transporter 1-like , and UDP-sugar pyrophosphorylase , which may contribute directly or indirectly to the improvement of dehydration tolerance in B . hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation. Drought is a major adverse environmental condition affecting plant growth and productivity. Although plants can be trained to improved tolerance to the subsequent drought stress, most land plants are unable to recover from severe dehydration when the relative water content in their vegetative tissues drops below 20–30%. However, a small group of angiosperms, termed resurrection plants, can survive extreme water deficiency of their vegetative tissues to an air-dried state and recovered upon rehydration. Understanding the biochemical and molecular basis of desiccation tolerance is valuable for extending our knowledge of the maximum ability of plants to deal with extreme water loss. Boea hygrometrica is a well-characterized resurrection plant that can not only tolerate slow dehydration but also extend its ability to survive rapid dehydration after a priming process of slow dehydration and rehydration. The rapid desiccation tolerance in primed plants can be maintained for at least four weeks. Here, we utilized this system of drought acclimation-induced RDT acquisition, maintenance, and erasing to explore plant phenotypic, physiological, and transcriptional changes, as well as DNA methylation dynamics. The analyses of the effect of DNA methylation on gene expression and promoter methylation changes with differential gene expression revealed the putative epigenetic control of dehydration stress memory in plants. Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica , but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B . hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A , vacuolar amino acid transporter 1-like , and UDP-sugar pyrophosphorylase , which may contribute directly or indirectly to the improvement of dehydration tolerance in B . hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation. |
| Audience | Academic |
| Author | Liu, Jie Wang, Yuan-Yuan Sun, Run-Ze Deng, Xin |
| AuthorAffiliation | 2 Facility Horticulture Laboratory of Universities in Shandong, Weifang University of Science and Technology, Shouguang, China 1 Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, China University of Cambridge, UNITED KINGDOM 3 College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China |
| AuthorAffiliation_xml | – name: University of Cambridge, UNITED KINGDOM – name: 3 College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China – name: 2 Facility Horticulture Laboratory of Universities in Shandong, Weifang University of Science and Technology, Shouguang, China – name: 1 Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, China |
| Author_xml | – sequence: 1 givenname: Run-Ze orcidid: 0000-0003-2654-3954 surname: Sun fullname: Sun, Run-Ze – sequence: 2 givenname: Jie orcidid: 0000-0002-2103-2816 surname: Liu fullname: Liu, Jie – sequence: 3 givenname: Yuan-Yuan orcidid: 0000-0002-3216-0477 surname: Wang fullname: Wang, Yuan-Yuan – sequence: 4 givenname: Xin orcidid: 0000-0002-6075-2429 surname: Deng fullname: Deng, Xin |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33930012$$D View this record in MEDLINE/PubMed |
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| Issue | 4 |
| Language | English |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The authors have declared that no competing interests exist. |
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| SubjectTerms | Abscisic acid Acclimation Antioxidants Autophagy Biology and life sciences Dehydration Desiccation DNA DNA methylation Drought Drying Electrical conductivity Embryogenesis Enzymes Epigenetics Gas chromatography Gene expression Genetic aspects Genomes Genomics Hardiness LEA protein Leaves Maltose Mass spectroscopy Medicine and Health Sciences Metabolites Metabolomics Methylation Phagocytosis Physiological aspects Physiology Plants Proteins Rehydration Signal transduction Small heat shock proteins Transcription Transcriptomes Tryptophan Ubiquitination Vitamin E |
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| Title | DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica |
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