Insights into the Epigenetic Basis of Plant Salt Tolerance
Abstract
:1. Introduction
2. DNA Methylation
2.1. DNA Methylation in Plants
2.2. Global Alterations of DNA Methylation under Salt Stress
2.3. Regulation of Key Stress-Responsive Genes by DNA Methylation
2.4. Plant Stress Memory by DNA Methylation
3. Histone Methylation
3.1. Histone Methylation in Plants
3.2. Global Alterations of Histone Methylation under Salt Stress
3.3. Regulatory Mechanisms of Histone Methylation under Salt Stress
3.4. Memorized Stress by Histone Methylation
4. Histone Acetylation
4.1. Histone Acetylation in Plants
4.2. Global Alteration of Histone Acetylation under Salt Stress
4.3. Regulatory Roles and Mechanisms of Histone Acetylation under Salt Stress
5. Histone Variants
5.1. Histone Variants in Plants
5.2. Regulatory Roles and Mechanisms of Histone Variants under Salt Stress
6. Non-Coding RNAs
6.1. Non-Coding RNAs in Plants
6.2. Global Alterations of Non-Coding RNAs under Salt Stress
6.3. Regulation of Core Stress-Responsive Genes by Non-Coding RNAs
Non-Coding RNA | Species | Changes under Salt Stress | Target Genes and Biological Functions | References |
---|---|---|---|---|
MiR156 | Malus domestica (apple) | Downregulation of MIR156a | Upregulation of MdSPL13. OE of MIR156a reduces salt tolerance | [157] |
Zea mays | Downregulation of MIR156 | R2R3 Myb SBP-domain protein | [158] | |
MiR164 | Solanum lycopersicum (tomato) | N.A. | KO of Sly-miR164a leads to reduced ROS and enhanced salt tolerance | [142] |
Zea mays | Downregulation of MIR164 | NAC1, ARF8 | [158] | |
MiR165/166 | Arabidopsis thaliana | Downregulation of MIR165A, MIR166A and MIR166B | Salt stress induces PHB expression and production of cytokinin. | [143] |
MiR168 | Oryza sativa | N.A. | PINHEAD (OsAGO1). KD of miR168 leads to enhanced salt tolerance. | [159] |
Zea mays | Upregulation of MIR168 | AGO1 | [158] | |
MiR169 | Zea mays | Downregulation of zma-miR169 family members | ZmNF-YA1; ZmNF-YA4; ZmNF-YA6; ZmNF-YA7; ZmNF-YA11; ZmNF-YA13; ZmNF-YA14 | [160] |
MiR172 | Glycine max (soybean) | Upregulation of gma-miR172a | SSAC1. OE of gma-miR172a leads to downregulation of SSAC1 and enhanced salt tolerance. | [161] |
Glycine max (soybean) | Upregulation of miR172c | NNC1. OE of miR172c leads to enhanced salt tolerance. | [162] | |
Oryza sativa | Upregulation of miR172a/b | IDS1. OE of miR172 leads to downregulation of IDS1 and enhanced salt tolerance. | [163] | |
MiR319 | Arabidopsis thaliana | Upregulation of miR319 | [164] | |
Medicago truncatula (model legume) | Downregulation of miR319 | TCP4. OE of Mtr-miR319a leads to the downregulation of TCP4 and enhanced salt tolerance. | [151] | |
Solanum linnaeanum (eggplant) | Downregulation of miR319 | TCP family transcription factor | [165] | |
Triticum aestivum | Upregulation of miR319a | [166] | ||
Zea mays | Downregulation of miR319 | TCPs | [158] | |
MiR390 | Populus spp. (poplar) | Upregulation of miR390 | TAS3. OE of miR390 leads to downregulation of ARFs (ARF3.1, ARF3.2, and ARF4) and enhanced salt tolerance. | [139] |
MiR393 | Arabidopsis thaliana | Upregulation of MIR393A | TIR1, ABF2, ABF3. Loss of miR393ab leads to an increase of lateral root number under salt stress, whereas OE of miR393 leads to enhanced salt tolerance. | [140,167] |
Oryza sativa | Upregulation of OsmiR393 | OsTIR1 and OsAFB2. OE of OsmiR393 leads to less tolerance to salt stress. | [168,169] | |
MiR394 | Arabidopsis thaliana | Upregulation of miR394 | LCR. OE of miR394 leads to less tolerance to salt stress. | [141] |
MiR395 | Zea mays | Upregulation of MIR395 | NADP-dependent malic protein, ATP sulfurylase | [158] |
MiR396 | Chrysanthemum indicum | Upregulation of cin-miR396a | CiGRF1 and CiGRF5. OE of cin-miR396a leads to less tolerance to salt stress. | [170] |
Oryza sativa | Upregulation of miR396b and downregulation of miR396c | GRF6. Loss of miR396 leads to enhanced salt tolerance. | [171,172] | |
Zea mays | Upregulation of MIR396 | Cytochrome oxidase | [158] | |
MiR397 | Arabidopsis thaliana | Upregulation of miR397 | LAC2, LAC4, and LAC17. OE of AtmiR397 leads to less tolerance to salt stress. | [173] |
MiR399 | Arabidopsis thaliana | Upregulation of miR399f | CSP41b and ABF3. OE of miR399f leads to enhanced salt tolerance. | [174] |
MiR408 | Zea mays | Downregulation of miR408 | ZmLAC9. OE of miR408a/b leads to enhanced salt tolerance. | [147,175] |
Salvia miltiorrhiza | Upregulation of Sm-MIR408 | OE of Sm-miR408 leads to enhanced salt tolerance. | [144] | |
MiR414 | Gossypium hirsutum (cotton) | Downregulation of ghr-miR414c | GhFSD1. OE of ghr-miR414c leads to less tolerance to salt stress. | [145] |
MiR528 | Oryza sativa | Upregulation of miR528 | AO. OE of miR528 leads to enhanced salt tolerance. | [176] |
MiR1118 | Triticum aestivum | Downregulation of miR1118 | PIP1;5. | [177] |
MiR1848 | Oryza sativa | Upregulation of osa-miR1848 | OsCYP51G3. OE of osa-miR1848 leads to less tolerance to salt stress. | [178] |
Lnc_388, Lnc_883, Lnc_973, Lnc_253 | Gossypium hirsutum (cotton) | Upregulation of Lnc_388, Lnc_883, Lnc_973, and Lnc_253 | LRR8 (Lnc_388), msD3 (Lnc_883), miR399 (Lnc_973), and miR156 (Lnc_253). Loss of Lnc_973 leads to less tolerance to salt stress. | [179,180] |
LncRNA354 | Gossypium hirsutum (cotton) | Upregulation of LncRNA354 | CeRNA for miR160b. Loss of LncRNA354 leads to enhanced salt tolerance. | [181] |
Ptlinc-NAC72 | Populus trichocarpa | Upregulation of Ptlinc-NAC72 | PtNAC72.A/B. OE of Ptlinc-NAC72 leads to less tolerance to salt stress. | [182] |
PUPPIES | Arabidopsis thaliana | Upregulation of PUPPIES | DOG1. Loss of PUPPIES leads to reduced expression of DOG1. | [183] |
LncRNA77580 | Glycine max (soybean) | N.A. | OE of LncRNA77580 leads to less tolerance to salt stress. | [184] |
LncERF024 | Populus ssp. | Upregulation of LncERF024 | OE of LncERF024 leads to enhanced salt tolerance. | [154] |
DRIR | Arabidopsis thaliana | Upregulation of DRIR | OE of DRIR leads to enhanced salt tolerance. | [185] |
7. Conclusions and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Negacz, K.; Malek, Ž.; de Vos, A.; Vellinga, P. Saline soils worldwide: Identifying the most promising areas for saline agriculture. J. Arid Environ. 2022, 203, 104775. [Google Scholar] [CrossRef]
- da Costa, G.S.; Cerqueira, A.F.; de Brito, C.R.; Mielke, M.S.; Gaiotto, F.A. Epigenetics Regulation in Responses to Abiotic Factors in Plant Species: A Systematic Review. Plants 2024, 13, 2082. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Lang, Z.; Zhu, J.-K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 2018, 19, 489–506. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, G.; Kudapa, H.; Ramalingam, A.; Choudhary, D.; Sinha, P.; Garg, V.; Singh, V.K.; Patil, G.B.; Pandey, M.K.; Nguyen, H.T.; et al. Epigenetics and epigenomics: Underlying mechanisms, relevance, and implications in crop improvement. Funct. Integr. Genom. 2020, 20, 739–761. [Google Scholar] [CrossRef] [PubMed]
- Bender, J. DNA Methylation and Epigenetics. Annu. Rev. Plant Biol. 2004, 55, 41–68. [Google Scholar] [CrossRef]
- Matzke, M.A.; Kanno, T.; Matzke, A.J.M. RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annu. Rev. Plant Biol. 2015, 66, 243–267. [Google Scholar] [CrossRef]
- Li, Y.; Guo, D. Transcriptome and DNA Methylome Analysis of Two Contrasting Rice Genotypes under Salt Stress during Germination. Int. J. Mol. Sci. 2023, 24, 3978. [Google Scholar] [CrossRef]
- Singroha, G.; Kumar, S.; Gupta, O.P.; Singh, G.P.; Sharma, P. Uncovering the Epigenetic Marks Involved in Mediating Salt Stress Tolerance in Plants. Front. Genet. 2022, 13, 811732. [Google Scholar] [CrossRef]
- He, X.-J.; Chen, T.; Zhu, J.-K. Regulation and function of DNA methylation in plants and animals. Cell Res. 2011, 21, 442–465. [Google Scholar] [CrossRef]
- Kumar, S.; Chinnusamy, V.; Mohapatra, T. Epigenetics of Modified DNA Bases: 5-Methylcytosine and Beyond. Front. Genet. 2018, 9, 640. [Google Scholar] [CrossRef]
- Lin, W.; Sun, L.; Huang, R.Z.; Liang, W.; Liu, X.; He, H.; Fukuda, H.; He, X.; Qian, W. Active DNA demethylation regulates tracheary element differentiation in Arabidopsis. Sci. Adv. 2020, 6, eaaz2963. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Liang, W.; Liu, Y.; Ren, Z.; Ci, D.; Chang, J.; Qian, W. The Arabidopsis ATR-SOG1 signaling module regulates pleiotropic developmental adjustments in response to 3′-blocked DNA repair intermediates. Plant Cell 2022, 34, 852–866. [Google Scholar] [CrossRef]
- Li, Y.; Kumar, S.; Qian, W. Active DNA demethylation: Mechanism and role in plant development. Plant Cell Rep. 2017, 37, 77–85. [Google Scholar] [CrossRef] [PubMed]
- Lindermayr, C.; Rudolf, E.E.; Durner, J.; Groth, M. Interactions between metabolism and chromatin in plant models. Mol. Metab. 2020, 38, 100951. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Aguayo, I.; Rodríguez-Galán, J.M.; García, R.; Torreblanca, J.; Pardo, J.M. Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta 2004, 220, 278–285. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Chen, G.; Guo, S.; Wang, Y.; Sun, J. SlSAMS1 enhances salt tolerance through regulation DNA methylation of SlGI in tomato. Plant Sci. 2023, 335, 111808. [Google Scholar] [CrossRef]
- Zhang, X.; Bao, Z.; Gong, B.; Shi, Q. S-adenosylmethionine synthetase 1 confers drought and salt tolerance in transgenic tomato. Environ. Exp. Bot. 2020, 179, 104226. [Google Scholar] [CrossRef]
- Ahmed, I.M.; Nadira, U.A.; Qiu, C.W.; Cao, F.; Chen, Z.H.; Vincze, E.; Wu, F. The Barley S-Adenosylmethionine Synthetase 3 Gene HvSAMS3 Positively Regulates the Tolerance to Combined Drought and Salinity Stress in Tibetan Wild Barley. Cells 2020, 9, 1530. [Google Scholar] [CrossRef]
- Al-Bahry, S.; Victor, R.; Al-Lawati, A.; Yaish, M. Salt stress alters DNA methylation levels in alfalfa (Medicago spp.). Genet. Mol. Res. 2016, 15, 15018299. [Google Scholar]
- Yang, X.; Bai, Z.; He, Y.; Wang, N.; Sun, L.; Li, Y.; Yin, Z.; Wang, X.; Zhang, B.; Han, M.; et al. Genome-wide characterization of DNA methyltransferase family genes implies GhDMT6 improving tolerance of salt and drought on cotton. BMC Plant Biol. 2024, 24, 312. [Google Scholar] [CrossRef]
- Zhang, Y.; Liu, C.; Xu, X.; Kan, J.; Li, H.; Lin, J.; Cheng, Z.; Chang, Y. Comprehensive Analysis of the DNA Methyltransferase Genes and Their Association with Salt Response in Pyrus betulaefolia. Forests 2023, 14, 1751. [Google Scholar] [CrossRef]
- Ashapkin, V.V.; Kutueva, L.I.; Aleksandrushkina, N.I.; Vanyushin, B.F. Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses. Int. J. Mol. Sci. 2020, 21, 7457. [Google Scholar] [CrossRef] [PubMed]
- Gahlaut, V.; Skorupa, M.; Szczepanek, J.; Mazur, J.; Domagalski, K.; Tretyn, A.; Tyburski, J. Salt stress and salt shock differently affect DNA methylation in salt-responsive genes in sugar beet and its wild, halophytic ancestor. PLoS ONE 2021, 16, e0251675. [Google Scholar]
- Wang, B.; Fu, R.; Zhang, M.; Ding, Z.; Chang, L.; Zhu, X.; Wang, Y.; Fan, B.; Ye, W.; Yuan, Y. Analysis of methylation-sensitive amplified polymorphism in different cotton accessions under salt stress based on capillary electrophoresis. Genes Genom. 2015, 37, 713–724. [Google Scholar] [CrossRef]
- Wang, W.; Zhao, X.; Pan, Y.; Zhu, L.; Fu, B.; Li, Z. DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress. J. Genet. Genom. 2011, 38, 419–424. [Google Scholar] [CrossRef] [PubMed]
- Sun, M.; Yang, Z.; Liu, L.; Duan, L. DNA Methylation in Plant Responses and Adaption to Abiotic Stresses. Int. J. Mol. Sci. 2022, 23, 6910. [Google Scholar] [CrossRef]
- Konate, M.; Wilkinson, M.; Mayne, B.; Pederson, S.; Scott, E.; Berger, B.; Rodriguez Lopez, C. Salt Stress Induces Non-CG Methylation in Coding Regions of Barley Seedlings (Hordeum vulgare). Epigenomes 2018, 2, 12. [Google Scholar] [CrossRef]
- Chen, R.; Li, M.; Zhang, H.; Duan, L.; Sun, X.; Jiang, Q.; Zhang, H.; Hu, Z. Continuous salt stress-induced long non-coding RNAs and DNA methylation patterns in soybean roots. BMC Genom. 2019, 20, 730. [Google Scholar] [CrossRef]
- Lin, X.; Zhou, M.; Yao, J.; Li, Q.Q.; Zhang, Y.-Y. Phenotypic and Methylome Responses to Salt Stress in Arabidopsis thaliana Natural Accessions. Front. Plant Sci. 2022, 13, 841154. [Google Scholar] [CrossRef]
- Miryeganeh, M.; Marlétaz, F.; Gavriouchkina, D.; Saze, H. De novo genome assembly and in natura epigenomics reveal salinity-induced DNA methylation in the mangrove tree Bruguiera gymnorhiza. New Phytol. 2021, 233, 2094–2110. [Google Scholar] [CrossRef]
- Shahid, S. A DNA Methylation Reader with an Affinity for Salt Stress. Plant Cell 2020, 32, 3380–3381. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Nan, N.; Li, N.; Liu, Y.; Wang, T.-J.; Hwang, I.; Liu, B.; Xu, Z.-Y. A DNA Methylation Reader–Chaperone Regulator–Transcription Factor Complex Activates OsHKT1;5 Expression during Salinity Stress. Plant Cell 2020, 32, 3535–3558. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Beena, A.S.; Awana, M.; Singh, A. Salt-Induced Tissue-Specific Cytosine Methylation Downregulates Expression of HKT Genes in Contrasting Wheat (Triticum aestivum L.) Genotypes. DNA Cell Biol. 2017, 36, 283–294. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Qin, L.; Xie, C.; Li, W.; Yuan, J.; Kong, L.; Yu, W.; Xia, G.; Liu, S. Induced and Constitutive DNA Methylation in a Salinity-Tolerant Wheat Introgression Line. Plant Cell Physiol. 2014, 55, 1354–1365. [Google Scholar] [CrossRef] [PubMed]
- Kong, L.; Liu, Y.; Wang, X.; Chang, C. Insight into the Role of Epigenetic Processes in Abiotic and Biotic Stress Response in Wheat and Barley. Int. J. Mol. Sci. 2020, 21, 1480. [Google Scholar] [CrossRef]
- Siddique, A.B.; Parveen, S.; Rahman, M.Z.; Rahman, J. Revisiting plant stress memory: Mechanisms and contribution to stress adaptation. Physiol. Mol. Biol. Plants 2024, 30, 349–367. [Google Scholar] [CrossRef]
- Jiang, C.; Mithani, A.; Belfield, E.J.; Mott, R.; Hurst, L.D.; Harberd, N.P. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 2014, 24, 1821–1829. [Google Scholar] [CrossRef]
- Wu, K.; Ou, X.; Zhang, Y.; Xu, C.; Lin, X.; Zang, Q.; Zhuang, T.; Jiang, L.; von Wettstein, D.; Liu, B. Transgenerational Inheritance of Modified DNA Methylation Patterns and Enhanced Tolerance Induced by Heavy Metal Stress in Rice (Oryza sativa L.). PLoS ONE 2012, 7, e41143. [Google Scholar]
- Cong, W.; Miao, Y.; Xu, L.; Zhang, Y.; Yuan, C.; Wang, J.; Zhuang, T.; Lin, X.; Jiang, L.; Wang, N.; et al. Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol. 2019, 19, 282. [Google Scholar] [CrossRef]
- Herman, J.J.; Sultan, S.E. DNA methylation mediates genetic variation for adaptive transgenerational plasticity. Proc. R. Soc. B Biol. Sci. 2016, 283, 20160988. [Google Scholar] [CrossRef]
- Zheng, X.; Chen, L.; Xia, H.; Wei, H.; Lou, Q.; Li, M.; Li, T.; Luo, L. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci. Rep. 2017, 7, 39843. [Google Scholar] [CrossRef]
- Kambona, C.M.; Koua, P.A.; Léon, J.; Ballvora, A. Stress memory and its regulation in plants experiencing recurrent drought conditions. Theor. Appl. Genet. 2023, 136, 26. [Google Scholar] [CrossRef] [PubMed]
- Boyko, A.; Blevins, T.; Yao, Y.; Golubov, A.; Bilichak, A.; Ilnytskyy, Y.; Hollunder, J.; Meins, F., Jr.; Kovalchuk, I. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE 2010, 5, e9514. [Google Scholar] [CrossRef]
- Wibowo, A.; Becker, C.; Marconi, G.; Durr, J.; Price, J.; Hagmann, J.; Papareddy, R.; Putra, H.; Kageyama, J.; Becker, J.; et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 2016, 5, e13546. [Google Scholar] [CrossRef] [PubMed]
- Geng, Y.; Chang, N.; Zhao, Y.; Qin, X.; Lu, S.; Crabbe, M.J.C.; Guan, Y.; Zhang, T. Increased epigenetic diversity and transient epigenetic memory in response to salinity stress in Thlaspi arvense. Ecol. Evol. 2020, 10, 11622–11630. [Google Scholar] [CrossRef] [PubMed]
- Sani, E.; Herzyk, P.; Perrella, G.; Colot, V.; Amtmann, A. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 2013, 14, R59. [Google Scholar] [CrossRef]
- Feng, X.J.; Li, J.R.; Qi, S.L.; Lin, Q.F.; Jin, J.B.; Hua, X.J. Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 2016, 113, E8335–E8343. [Google Scholar] [CrossRef]
- Nunez-Vazquez, R.; Desvoyes, B.; Gutierrez, C. Histone variants and modifications during abiotic stress response. Front. Plant Sci. 2022, 13, 984702. [Google Scholar] [CrossRef]
- Xiao, J.; Lee, U.-S.; Wagner, D. Tug of war: Adding and removing histone lysine methylation in arabidopsis. Curr. Opin. Plant Biol. 2016, 34, 41–53. [Google Scholar] [CrossRef]
- Yung, W.S.; Li, M.W.; Sze, C.C.; Wang, Q.; Lam, H.M. Histone modifications and chromatin remodelling in plants in response to salt stress. Physiol. Plant 2021, 173, 1495–1513. [Google Scholar] [CrossRef]
- Chua, Y.; Gray, J.C. Histone Modifications and Transcription in Plants; Blackwell Publishing Ltd.: Oxford, UK, 2006; pp. 79–111. [Google Scholar]
- Liu, C.; Lu, F.; Cui, X.; Cao, X. Histone methylation in higher plants. Annu. Rev. Plant Biol. 2010, 61, 395–420. [Google Scholar] [CrossRef]
- Zhang, X.; Clarenz, O.; Cokus, S.; Bernatavichute, Y.V.; Pellegrini, M.; Goodrich, J.; Jacobsen, S.E. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007, 5, e129. [Google Scholar] [CrossRef]
- Roudier, F.; Ahmed, I.; Berard, C.; Sarazin, A.; Mary-Huard, T.; Cortijo, S.; Bouyer, D.; Caillieux, E.; Duvernois-Berthet, E.; Al-Shikhley, L.; et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011, 30, 1928–1938. [Google Scholar] [CrossRef]
- Han, B.; Xu, W.; Ahmed, N.; Yu, A.; Wang, Z.; Liu, A. Changes and Associations of Genomic Transcription and Histone Methylation with Salt Stress in Castor Bean. Plant Cell Physiol. 2020, 61, 1120–1133. [Google Scholar] [CrossRef]
- Asensi-Fabado, M.A.; Amtmann, A.; Perrella, G. Plant responses to abiotic stress: The chromatin context of transcriptional regulation. Biochim. Biophys. Acta Gene Regul. Mech. 2017, 1860, 106–122. [Google Scholar] [CrossRef]
- Jambhekar, A.; Dhall, A.; Shi, Y. Roles and regulation of histone methylation in animal development. Nat. Rev. Mol. Cell Biol. 2019, 20, 625–641. [Google Scholar] [CrossRef]
- Haider, S.; Farrona, S. Decoding histone 3 lysine methylation: Insights into seed germination and flowering. Curr. Opin. Plant Biol. 2024, 81, 102598. [Google Scholar] [CrossRef]
- Roudier, F.; Teixeira, F.K.; Colot, V. Chromatin indexing in Arabidopsis: An epigenomic tale of tails and more. Trends Genet. 2009, 25, 511–517. [Google Scholar] [CrossRef]
- Sequeira-Mendes, J.; Aragüez, I.; Peiró, R.; Mendez-Giraldez, R.; Zhang, X.; Jacobsen, S.E.; Bastolla, U.; Gutierrez, C. The Functional Topography of the Arabidopsis Genome Is Organized in a Reduced Number of Linear Motifs of Chromatin States. Plant Cell 2014, 26, 2351–2366. [Google Scholar] [CrossRef]
- Nützmann, H.-W.; Doerr, D.; Ramírez-Colmenero, A.; Sotelo-Fonseca, J.E.; Wegel, E.; Di Stefano, M.; Wingett, S.W.; Fraser, P.; Hurst, L.; Fernandez-Valverde, S.L.; et al. Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proc. Natl. Acad. Sci. USA 2020, 117, 13800–13809. [Google Scholar] [CrossRef]
- Berger, S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447, 407–412. [Google Scholar] [CrossRef] [PubMed]
- He, K.; Cao, X.; Deng, X. Histone methylation in epigenetic regulation and temperature responses. Curr. Opin. Plant Biol. 2021, 61, 102001. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.; Cui, X.; Shen, Y. The roles of histone methylation in the regulation of abiotic stress responses in plants. Plant Stress 2024, 11, 100303. [Google Scholar] [CrossRef]
- Liu, Y.; Wang, J.; Liu, B.; Xu, Z.Y. Dynamic regulation of DNA methylation and histone modifications in response to abiotic stresses in plants. J. Integr. Plant Biol. 2022, 64, 2252–2274. [Google Scholar] [CrossRef]
- Shen, Y.; Chi, Y.; Lu, S.; Lu, H.; Shi, L. Involvement of JMJ15 in the dynamic change of genome-wide H3K4me3 in response to salt stress. Front. Plant Sci. 2022, 13, 1009723. [Google Scholar] [CrossRef]
- Song, Y.; Ji, D.; Li, S.; Wang, P.; Li, Q.; Xiang, F. The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 2012, 7, e41274. [Google Scholar] [CrossRef]
- Bilichak, A.; Ilnystkyy, Y.; Hollunder, J.; Kovalchuk, I. The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 2012, 7, e30515. [Google Scholar] [CrossRef] [PubMed]
- Yung, W.S.; Wang, Q.; Huang, M.; Wong, F.L.; Liu, A.; Ng, M.S.; Li, K.P.; Sze, C.C.; Li, M.W.; Lam, H.M. Priming-induced alterations in histone modifications modulate transcriptional responses in soybean under salt stress. Plant J. 2022, 109, 1575–1590. [Google Scholar] [CrossRef]
- Paul, A.; Dasgupta, P.; Roy, D.; Chaudhuri, S. Comparative analysis of Histone modifications and DNA methylation at OsBZ8 locus under salinity stress in IR64 and Nonabokra rice varieties. Plant Mol. Biol. 2017, 95, 63–88. [Google Scholar] [CrossRef]
- Dong, W.; Gao, T.; Wang, Q.; Chen, J.; Lv, J.; Song, Y. Salinity stress induces epigenetic alterations to the promoter of MsMYB4 encoding a salt-induced MYB transcription factor. Plant Physiol. Biochem. 2020, 155, 709–715. [Google Scholar] [CrossRef]
- Yung, W.S.; Huang, C.; Li, M.W.; Lam, H.M. Changes in epigenetic features in legumes under abiotic stresses. Plant Genome 2023, 16, e20237. [Google Scholar] [CrossRef] [PubMed]
- Yin, W.; Xiao, Y.; Niu, M.; Meng, W.; Li, L.; Zhang, X.; Liu, D.; Zhang, G.; Qian, Y.; Sun, Z.; et al. ARGONAUTE2 Enhances Grain Length and Salt Tolerance by Activating BIG GRAIN3 to Modulate Cytokinin. Plant Cell 2020, 32, 2291–2306. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Conde, E.S.N.; Audonnet, L.; Servet, C.; Wei, W.; Zhou, D.X. Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis. Front. Plant Sci. 2014, 5, 290. [Google Scholar] [CrossRef]
- Mellor, J. It Takes a PHD to Read the Histone Code. Cell 2006, 126, 22–24. [Google Scholar] [CrossRef]
- Wei, W.; Tao, J.J.; Chen, H.W.; Li, Q.T.; Zhang, W.K.; Ma, B.; Lin, Q.; Zhang, J.S.; Chen, S.Y. A Histone Code Reader and a Transcriptional Activator Interact to Regulate Genes for Salt Tolerance. Plant Physiol. 2017, 175, 1304–1320. [Google Scholar] [CrossRef]
- Liu, Y.; Chen, X.; Xue, S.; Quan, T.; Cui, D.; Han, L.; Cong, W.; Li, M.; Yun, D.J.; Liu, B.; et al. SET DOMAIN GROUP 721 protein functions in saline–alkaline stress tolerance in the model rice variety Kitaake. Plant Biotechnol. J. 2021, 19, 2576–2588. [Google Scholar] [CrossRef]
- Fu, Z.W.; Li, J.H.; Feng, Y.R.; Yuan, X.; Lu, Y.T. The metabolite methylglyoxal-mediated gene expression is associated with histone methylglyoxalation. Nucleic Acids Res. 2021, 49, 1886–1899. [Google Scholar] [CrossRef]
- QiZhi, F.; ChunWu, Y.; XiuYun, L.; JinMing, W.; XiuFang, O.; ChunYu, Z.; Yu, C.; Bao, L. Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice (Oryza sativa). Aust. J. Crop Sci. 2012, 6, 877–883. [Google Scholar]
- Roychoudhury, A.; Banerjee, A.; Lahiri, V. Metabolic and molecular-genetic regulation of proline signaling and itscross-talk with major effectors mediates abiotic stress tolerance in plants. Turk. J. Bot. 2015, 39, 887–910. [Google Scholar] [CrossRef]
- Tian, Z.; Li, K.; Sun, Y.; Chen, B.; Pan, Z.; Wang, Z.; Pang, B.; He, S.; Miao, Y.; Du, X. Physiological and transcriptional analyses reveal formation of memory under recurring drought stresses in seedlings of cotton (Gossypium hirsutum). Plant Sci. 2024, 338, 111920. [Google Scholar] [CrossRef]
- Liu, H.c.; Lämke, J.; Lin, S.y.; Hung, M.J.; Liu, K.M.; Charng, Y.y.; Bäurle, I. Distinct heat shock factors and chromatin modifications mediate the organ-autonomous transcriptional memory of heat stress. Plant J. 2018, 95, 401–413. [Google Scholar] [CrossRef] [PubMed]
- Ding, Y.; Fromm, M.; Avramova, Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat. Commun. 2012, 3, 740. [Google Scholar] [CrossRef] [PubMed]
- Mozgova, I.; Hennig, L. The Polycomb Group Protein Regulatory Network. Annu. Rev. Plant Biol. 2015, 66, 269–296. [Google Scholar] [CrossRef] [PubMed]
- Onufriev, A.V.; Schiessel, H. The nucleosome: From structure to function through physics. Curr. Opin. Struct. Biol. 2019, 56, 119–130. [Google Scholar] [CrossRef]
- Earley, K.W.; Shook, M.S.; Brower-Toland, B.; Hicks, L.; Pikaard, C.S. In Vitro specificities of Arabidopsis co-activator histone acetyltransferases: Implications for histone hyperacetylation in gene activation. Plant J. 2007, 52, 615–626. [Google Scholar] [CrossRef]
- Ueda, M.; Matsui, A.; Tanaka, M.; Nakamura, T.; Abe, T.; Sako, K.; Sasaki, T.; Kim, J.M.; Ito, A.; Nishino, N.; et al. The Distinct Roles of Class I and II RPD3-Like Histone Deacetylases in Salinity Stress Response. Plant Physiol. 2017, 175, 1760–1773. [Google Scholar] [CrossRef]
- Zheng, Y.; Ding, Y.; Sun, X.; Xie, S.; Wang, D.; Liu, X.; Su, L.; Wei, W.; Pan, L.; Zhou, D.X. Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J. Exp. Bot. 2016, 67, 1703–1713. [Google Scholar] [CrossRef]
- Xing, G.; Jin, M.; Qu, R.; Zhang, J.; Han, Y.; Han, Y.; Wang, X.; Li, X.; Ma, F.; Zhao, X. Genome-wide investigation of histone acetyltransferase gene family and its responses to biotic and abiotic stress in foxtail millet (Setaria italica [L.] P. Beauv). BMC Plant Biol. 2022, 22, 292. [Google Scholar] [CrossRef]
- Wei, F.; Tang, D.; Li, Z.; Kashif, M.H.; Khan, A.; Lu, H.; Jia, R.; Chen, P. Molecular cloning and subcellular localization of six HDACs and their roles in response to salt and drought stress in kenaf (Hibiscus cannabinus L.). Biol. Res. 2019, 52, 20. [Google Scholar] [CrossRef]
- Liu, C.T.; Mao, B.G.; Yuan, D.Y.; Chu, C.C.; Duan, M.J. Salt tolerance in rice: Physiological responses and molecular mechanisms. Crop J. 2022, 10, 13–25. [Google Scholar] [CrossRef]
- Su, P.; Yan, J.; Li, W.; Wang, L.; Zhao, J.; Ma, X.; Li, A.; Wang, H.; Kong, L. A member of wheat class III peroxidase gene family, TaPRX-2A, enhanced the tolerance of salt stress. BMC Plant Biol. 2020, 20, 392. [Google Scholar] [CrossRef] [PubMed]
- Cheng, X.; Zhang, S.; Tao, W.; Zhang, X.; Liu, J.; Sun, J.; Zhang, H.; Pu, L.; Huang, R.; Chen, T. INDETERMINATE SPIKELET1 Recruits Histone Deacetylase and a Transcriptional Repression Complex to Regulate Rice Salt Tolerance. Plant Physiol. 2018, 178, 824–837. [Google Scholar] [CrossRef] [PubMed]
- Choudhary, C.; Weinert, B.T.; Nishida, Y.; Verdin, E.; Mann, M. The growing landscape of lysine acetylation links metabolism and cell signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 536–550. [Google Scholar] [CrossRef] [PubMed]
- Pietrocola, F.; Galluzzi, L.; Bravo-San Pedro, J.M.; Madeo, F.; Kroemer, G. Acetyl Coenzyme A: A Central Metabolite and Second Messenger. Cell Metab. 2015, 21, 805–821. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.; Lu, Y.; Zhao, Y.; Zhou, D.X. Histone Acetylation Dynamics Integrates Metabolic Activity to Regulate Plant Response to Stress. Front. Plant Sci. 2019, 10, 1236. [Google Scholar] [CrossRef]
- Chen, C.; Li, C.; Wang, Y.; Renaud, J.; Tian, G.; Kambhampati, S.; Saatian, B.; Nguyen, V.; Hannoufa, A.; Marsolais, F.; et al. Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis. Nat. Plants 2017, 3, 814–824. [Google Scholar] [CrossRef]
- Lorena, M.-P.; Vicent, P.; María, D.C.; Vicente, T. Dynamic remodeling of histone modifications in response to osmotic stress in Saccharomyces cerevisiae. BMC Genom. 2014, 15, 247. [Google Scholar]
- Truong, H.A.; Lee, S.; Trinh, C.S.; Lee, W.J.; Chung, E.H.; Hong, S.W.; Lee, H. Overexpression of the HDA15 Gene Confers Resistance to Salt Stress by the Induction of NCED3, an ABA Biosynthesis Enzyme. Front. Plant Sci. 2021, 12, 640443. [Google Scholar] [CrossRef]
- Ullah, F.; Xu, Q.; Zhao, Y.; Zhou, D.X. Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice. J. Integr. Plant Biol. 2020, 63, 451–467. [Google Scholar] [CrossRef]
- Zhao, X.; Wang, H.; Zhang, B.; Cheng, Y.; Ma, X. Overexpression of histone deacetylase gene 84KHDA909 from poplar confers enhanced tolerance to drought and salt stresses in Arabidopsis. Plant Sci. 2022, 324, 111434. [Google Scholar] [CrossRef]
- Sako, K.; Kim, J.M.; Matsui, A.; Nakamura, K.; Tanaka, M.; Kobayashi, M.; Saito, K.; Nishino, N.; Kusano, M.; Taji, T.; et al. Ky-2, a Histone Deacetylase Inhibitor, Enhances High-Salinity Stress Tolerance in Arabidopsis thaliana. Plant Cell Physiol. 2016, 57, 776–783. [Google Scholar] [CrossRef] [PubMed]
- Yolcu, S.; Ozdemir, F.; Guler, A.; Bor, M. Histone acetylation influences the transcriptional activation of POX in Beta vulgaris L. and Beta maritima L. under salt stress. Plant Physiol. Biochem. 2016, 100, 37–46. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.-T.; Luo, M.; Wang, Y.-Y.; Wu, K. Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J. Exp. Bot. 2010, 61, 3345–3353. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Yan, S.; Zhao, L.; Tan, J.; Zhang, Q.; Gao, F.; Wang, P.; Hou, H.; Li, L. Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol. 2014, 14, 105. [Google Scholar] [CrossRef]
- Zhu, N.; Cheng, S.; Liu, X.; Du, H.; Dai, M.; Zhou, D.-X.; Yang, W.; Zhao, Y. The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci. 2015, 236, 146–156. [Google Scholar] [CrossRef]
- Wei, H.; Wang, X.; He, Y.; Xu, H.; Wang, L. Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. EMBO J. 2021, 40, e105086. [Google Scholar] [CrossRef]
- Zheng, M.; Lin, J.; Liu, X.; Chu, W.; Li, J.; Gao, Y.; An, K.; Song, W.; Xin, M.; Yao, Y.; et al. Histone acetyltransferase TaHAG1 acts as a crucial regulator to strengthen salt tolerance of hexaploid wheat. Plant Physiol. 2021, 186, 1951–1969. [Google Scholar] [CrossRef]
- Sokol, A.; Kwiatkowska, A.; Jerzmanowski, A.; Prymakowska-Bosak, M. Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta 2007, 227, 245–254. [Google Scholar] [CrossRef]
- Zhao, J.; Zhang, W.; da Silva, J.A.T.; Liu, X.; Duan, J. Rice histone deacetylase HDA704 positively regulates drought and salt tolerance by controlling stomatal aperture and density. Planta 2021, 254, 79. [Google Scholar] [CrossRef]
- Wang, X.; Wang, Y.; Jiang, Y.; Wang, H.; Zhou, L.; Li, F.; Wang, L.; Jiang, J.; Chen, F.; Chen, S. Transcription factor CmHSFA4-CmMYBS3 complex enhances salt tolerance in chrysanthemum by repressing CmMYB121 expression. Plant Physiol. 2024, 195, 3119–3135. [Google Scholar] [CrossRef]
- Zheng, L.; Ma, S.; Shen, D.; Fu, H.; Wang, Y.; Liu, Y.; Shah, K.; Yue, C.; Huang, J. Genome-wide identification of Gramineae histone modification genes and their potential roles in regulating wheat and maize growth and stress responses. BMC Plant Biol. 2021, 21, 543. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.V.; Wigge, P.A. H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis. Cell 2010, 140, 136–147. [Google Scholar] [CrossRef] [PubMed]
- Osakabe, A.; Molaro, A. Histone renegades: Unusual H2A histone variants in plants and animals. Semin. Cell Dev. Biol. 2023, 135, 35–42. [Google Scholar] [CrossRef] [PubMed]
- Miao, R.; Zhang, Y.; Liu, X.; Yuan, Y.; Zang, W.; Li, Z.; Yan, X.; Pang, Q.; Zhang, A. Histone variant H2A.Z is required for plant salt response by regulating gene transcription. Plant Cell Environ. 2024, 47, 2691–2707. [Google Scholar] [CrossRef]
- Do, B.H.; Hiep, N.T.; Lao, T.D.; Nguyen, N.H. Loss-of-Function Mutation of ACTIN-RELATED PROTEIN 6 (ARP6) Impairs Root Growth in Response to Salinity Stress. Mol. Biotechnol. 2023, 65, 1414–1420. [Google Scholar] [CrossRef]
- Nguyen, N.H.; Cheong, J.-J. H2A.Z-containing nucleosomes are evicted to activate AtMYB44 transcription in response to salt stress. Biochem. Biophys. Res. Commun. 2018, 499, 1039–1043. [Google Scholar] [CrossRef]
- Jung, C.; Seo, J.S.; Han, S.W.; Koo, Y.J.; Kim, C.H.; Song, S.I.; Nahm, B.H.; Choi, Y.D.; Cheong, J.-J. Overexpression of AtMYB44 Enhances Stomatal Closure to Confer Abiotic Stress Tolerance in Transgenic Arabidopsis. Plant Physiol. 2008, 146, 323–324. [Google Scholar] [CrossRef]
- Qiu, S.-P.; Huang, J.; Pan, L.-J.; Wang, M.-M.; Zhang, H.-S. Salt Induces Expression of RH3.2A, Encoding an H3.2-type Histone H3 Protein in Rice (Oryza sativa L.). Acta Genet. Sin. 2006, 33, 833–840. [Google Scholar] [CrossRef]
- Probst, A.V.; Desvoyes, B.; Gutierrez, C.; Parry, G. Similar yet critically different: The distribution, dynamics and function of histone variants. J. Exp. Bot. 2020, 71, 5191–5204. [Google Scholar] [CrossRef]
- Hargreaves, D.C.; Crabtree, G.R. ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Res. 2011, 21, 396–420. [Google Scholar] [CrossRef]
- Xu, W.; Li, Y.; Cheng, Z.; Xia, G.; Wang, M. A wheat histone variant gene TaH2A.7 enhances drought tolerance and promotes stomatal closure in Arabidopsis. Plant Cell Rep. 2016, 35, 1853–1862. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Li, Y.; Zhou, F.; Zhang, L.; Gong, J.; Cheng, C.; Chen, J.; Lou, Q. Genome-wide characterization, phylogenetic and expression analysis of Histone gene family in cucumber (Cucumis sativus L.). Int. J. Biol. Macromol. 2023, 230, 123401. [Google Scholar] [CrossRef] [PubMed]
- Gao, Z.; Ma, C.; Zheng, C.; Yao, Y.; Du, Y. Advances in the regulation of plant salt-stress tolerance by miRNA. Mol. Biol. Rep. 2022, 49, 5041–5055. [Google Scholar] [CrossRef]
- Qiao, H.; Jiao, B.; Wang, J.; Yang, Y.; Yang, F.; Geng, Z.; Zhao, G.; Liu, Y.; Dong, F.; Wang, Y.; et al. Comparative Analysis of miRNA Expression Profiles under Salt Stress in Wheat. Genes 2023, 14, 1586. [Google Scholar] [CrossRef] [PubMed]
- Alzahrani, S.M.; Alaraidh, I.A.; Khan, M.A.; Migdadi, H.M.; Alghamdi, S.S.; Alsahli, A.A. Identification and Characterization of Salt-Responsive MicroRNAs in Vicia faba by High-Throughput Sequencing. Genes 2019, 10, 303. [Google Scholar] [CrossRef]
- Wei, L.; Du, Y.; Xiang, J.; Zheng, T.; Cheng, J.; Wu, J. Integrated mRNA and miRNA transcriptome analysis of grape in responses to salt stress. Front. Plant Sci. 2023, 14, 1173857. [Google Scholar] [CrossRef]
- Xie, R.; Zhang, J.; Ma, Y.; Pan, X.; Dong, C.; Pang, S.; He, S.; Deng, L.; Yi, S.; Zheng, Y.; et al. Combined analysis of mRNA and miRNA identifies dehydration and salinity responsive key molecular players in citrus roots. Sci. Rep. 2017, 7, 42094. [Google Scholar] [CrossRef]
- Nguyen, D.Q.; Nguyen, N.L.; Nguyen, V.T.; Tran, T.H.G.; Nguyen, T.H.; Nguyen, T.K.L.; Nguyen, H.H. Comparative analysis of microRNA expression profiles in shoot and root tissues of contrasting rice cultivars (Oryza sativa L.) with different salt stress tolerance. PLoS ONE 2023, 18, e0286140. [Google Scholar] [CrossRef]
- Liu, J.N.; Ma, X.; Yan, L.; Liang, Q.; Fang, H.; Wang, C.; Dong, Y.; Chai, Z.; Zhou, R.; Bao, Y.; et al. MicroRNA and Degradome Profiling Uncover Defense Response of Fraxinus velutina Torr. to Salt Stress. Front. Plant Sci. 2022, 13, 847853. [Google Scholar] [CrossRef]
- Yin, Z.; Han, X.; Li, Y.; Wang, J.; Wang, D.; Wang, S.; Fu, X.; Ye, W. Comparative Analysis of Cotton Small RNAs and Their Target Genes in Response to Salt Stress. Genes 2017, 8, 369. [Google Scholar] [CrossRef]
- Bravo-Vázquez, L.A.; García-Ortega, M.; Medina-Feria, S.; Srivastava, A.; Paul, S. Identification and expression profiling of microRNAs in leaf tissues of Foeniculum vulgare Mill. under salinity stress. Plant Signal Behav. 2024, 19, 2361174. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Ren, Y.; Sun, Y.; Yin, Y.; Han, B.; Zhang, L.; Song, Y.; Zhang, Z.; Xu, Y.; Fan, D.; et al. Identification and Analysis of the MIR399 Gene Family in Grapevine Reveal Their Potential Functions in Abiotic Stress. Int. J. Mol. Sci. 2024, 25, 2979. [Google Scholar] [CrossRef] [PubMed]
- Szymonik, K.; Klimek-Chodacka, M.; Lukasiewicz, A.; Macko-Podgórni, A.; Grzebelus, D.; Baranski, R. Comparative analysis of the carrot miRNAome in response to salt stress. Sci. Rep. 2023, 13, 21506. [Google Scholar] [CrossRef] [PubMed]
- Kumar, V.; Khare, T.; Shriram, V.; Wani, S.H. Plant small RNAs: The essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep. 2018, 37, 61–75. [Google Scholar] [CrossRef]
- Li, Z.; Zhou, H.; Xu, G.; Zhang, P.; Zhai, N.; Zheng, Q.; Liu, P.; Jin, L.; Bai, G.; Zhang, H. Genome-wide analysis of long noncoding RNAs in response to salt stress in Nicotiana tabacum. BMC Plant Biol. 2023, 23, 646. [Google Scholar] [CrossRef]
- Li, N.; Wang, Z.; Wang, B.; Wang, J.; Xu, R.; Yang, T.; Huang, S.; Wang, H.; Yu, Q. Identification and Characterization of Long Non-coding RNA in Tomato Roots Under Salt Stress. Front. Plant Sci. 2022, 13, 834027. [Google Scholar] [CrossRef]
- Gu, Y.; Li, G.; Wang, P.; Guo, Y.; Li, J. A simple and precise method (Y2H-in-frame-seq) improves yeast two-hybrid screening with cDNA libraries. J. Genet. Genom. 2022, 49, 595–598. [Google Scholar] [CrossRef]
- He, F.; Xu, C.; Fu, X.; Shen, Y.; Guo, L.; Leng, M.; Luo, K. The MicroRNA390/TRANS-ACTING SHORT INTERFERING RNA3 Module Mediates Lateral Root Growth under Salt Stress via the Auxin Pathway. Plant Physiol. 2018, 177, 775–791. [Google Scholar] [CrossRef]
- Iglesias, M.J.; Terrile, M.C.; Windels, D.; Lombardo, M.C.; Bartoli, C.G.; Vazquez, F.; Estelle, M.; Casalongué, C.A. MiR393 regulation of auxin signaling and redox-related components during acclimation to salinity in Arabidopsis. PLoS ONE 2014, 9, e107678. [Google Scholar] [CrossRef]
- Song, J.B.; Gao, S.; Sun, D.; Li, H.; Shu, X.X.; Yang, Z.M. miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biol. 2013, 13, 210. [Google Scholar] [CrossRef]
- Wan, X.; Wang, Z.; Duan, W.; Huang, T.; Song, H.; Xu, X. Knockdown of Sly-miR164a Enhanced Plant Salt Tolerance and Improved Preharvest and Postharvest Fruit Nutrition of Tomato. Int. J. Mol. Sci. 2023, 24, 4639. [Google Scholar] [CrossRef] [PubMed]
- Scintu, D.; Scacchi, E.; Cazzaniga, F.; Vinciarelli, F.; De Vivo, M.; Shtin, M.; Svolacchia, N.; Bertolotti, G.; Unterholzner, S.J.; Del Bianco, M.; et al. microRNA165 and 166 modulate response of the Arabidopsis root apical meristem to salt stress. Commun. Biol. 2023, 6, 834. [Google Scholar] [CrossRef] [PubMed]
- Guo, X.; Niu, J.; Cao, X. Heterologous Expression of Salvia miltiorrhiza MicroRNA408 Enhances Tolerance to Salt Stress in Nicotiana benthamiana. Int. J. Mol. Sci. 2018, 19, 3985. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Liu, D.; Chen, D.; Cheng, Y.; Zhang, X.; Song, L.; Hu, M.; Dong, J.; Shen, F. MicroRNA414c affects salt tolerance of cotton by regulating reactive oxygen species metabolism under salinity stress. RNA Biol. 2019, 16, 362–375. [Google Scholar] [CrossRef] [PubMed]
- Xing, L.; Zhu, M.; Luan, M.; Zhang, M.; Jin, L.; Liu, Y.; Zou, J.; Wang, L.; Xu, M. miR169q and NUCLEAR FACTOR YA8 enhance salt tolerance by activating PEROXIDASE1 expression in response to ROS. Plant Physiol. 2022, 188, 608–623. [Google Scholar] [CrossRef] [PubMed]
- Qin, R.; Hu, Y.; Chen, H.; Du, Q.; Yang, J.; Li, W.X. MicroRNA408 negatively regulates salt tolerance by affecting secondary cell wall development in maize. Plant Physiol. 2023, 192, 1569–1583. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Nahar, K.; Anee, T.I.; Fujita, M. Glutathione in plants: Biosynthesis and physiological role in environmental stress tolerance. Physiol. Mol. Biol. Plants 2017, 23, 249–268. [Google Scholar] [CrossRef]
- Lushchak, V.I. Glutathione Homeostasis and Functions: Potential Targets for Medical Interventions. J. Amino Acids 2012, 2012, 736837. [Google Scholar] [CrossRef]
- Mittova, V.; Theodoulou, F.L.; Kiddle, G.; Gómez, L.; Volokita, M.; Tal, M.; Foyer, C.H.; Guy, M. Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett. 2003, 554, 417–421. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Xu, L.; Zhang, L.; Li, X.; Cao, C.; Chen, L.; Kang, J.; Yang, Q.; Liu, Y.; Sod, B.; et al. Overexpression of Mtr-miR319a Contributes to Leaf Curl and Salt Stress Adaptation in Arabidopsis thaliana and Medicago truncatula. Int. J. Mol. Sci. 2022, 24, 429. [Google Scholar] [CrossRef]
- Rehman, O.U.; Uzair, M.; Farooq, M.S.; Saleem, B.; Attacha, S.; Attia, K.A.; Farooq, U.; Fiaz, S.; El-Kallawy, W.H.; Kimiko, I.; et al. Comprehensive insights into the regulatory mechanisms of lncRNA in alkaline-salt stress tolerance in rice. Mol. Biol. Rep. 2023, 50, 7381–7392. [Google Scholar] [CrossRef] [PubMed]
- Tian, R.; Sun, X.; Liu, C.; Chu, J.; Zhao, M.; Zhang, W.H. A Medicago truncatula lncRNA MtCIR1 negatively regulates response to salt stress. Planta 2023, 257, 32. [Google Scholar] [CrossRef] [PubMed]
- Li, G.; Chen, Q.; Bai, Q.; Feng, Y.; Mao, K.; Yang, M.; He, L.; Liu, M.; Liu, J.; Wan, D. LncRNA expression analysis by comparative transcriptomics among closely related poplars and their regulatory roles in response to salt stress. Tree Physiol. 2023, 43, 1233–1249. [Google Scholar] [CrossRef] [PubMed]
- Mirdar Mansuri, R.; Azizi, A.H.; Sadri, A.H.; Shobbar, Z.S. Long non-coding RNAs as the regulatory hubs in rice response to salt stress. Sci. Rep. 2022, 12, 21696. [Google Scholar] [CrossRef]
- Xu, W.B.; Cao, F.; Liu, P.; Yan, K.; Guo, Q.H. The multifaceted role of RNA-based regulation in plant stress memory. Front. Plant Sci. 2024, 15, 1387575. [Google Scholar] [CrossRef]
- Ma, Y.; Xue, H.; Zhang, F.; Jiang, Q.; Yang, S.; Yue, P.; Wang, F.; Zhang, Y.; Li, L.; He, P.; et al. The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol. J. 2021, 19, 311–323. [Google Scholar] [CrossRef]
- Ding, D.; Zhang, L.; Wang, H.; Liu, Z.; Zhang, Z.; Zheng, Y. Differential expression of miRNAs in response to salt stress in maize roots. Ann. Bot. 2009, 103, 29–38. [Google Scholar] [CrossRef]
- Wan, J.; Meng, S.; Wang, Q.; Zhao, J.; Qiu, X.; Wang, L.; Li, J.; Lin, Y.; Mu, L.; Dang, K.; et al. Suppression of microRNA168 enhances salt tolerance in rice (Oryza sativa L.). BMC Plant Biol. 2022, 22, 563. [Google Scholar] [CrossRef]
- Luan, M.; Xu, M.; Lu, Y.; Zhang, Q.; Zhang, L.; Zhang, C.; Fan, Y.; Lang, Z.; Wang, L. Family-wide survey of miR169s and NF-YAs and their expression profiles response to abiotic stress in maize roots. PLoS ONE 2014, 9, e91369. [Google Scholar] [CrossRef]
- Pan, W.J.; Tao, J.J.; Cheng, T.; Bian, X.H.; Wei, W.; Zhang, W.K.; Ma, B.; Chen, S.Y.; Zhang, J.S. Soybean miR172a Improves Salt Tolerance and Can Function as a Long-Distance Signal. Mol. Plant 2016, 9, 1337–1340. [Google Scholar] [CrossRef]
- Sahito, Z.A.; Wang, L.; Sun, Z.; Yan, Q.; Zhang, X.; Jiang, Q.; Ullah, I.; Tong, Y.; Li, X. The miR172c-NNC1 module modulates root plastic development in response to salt in soybean. BMC Plant Biol. 2017, 17, 229. [Google Scholar] [CrossRef] [PubMed]
- Cheng, X.; He, Q.; Tang, S.; Wang, H.; Zhang, X.; Lv, M.; Liu, H.; Gao, Q.; Zhou, Y.; Wang, Q.; et al. The miR172/IDS1 signaling module confers salt tolerance through maintaining ROS homeostasis in cereal crops. New Phytol. 2021, 230, 1017–1033. [Google Scholar] [CrossRef]
- Sunkar, R.; Zhu, J.K. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 2004, 16, 2001–2019. [Google Scholar] [CrossRef] [PubMed]
- Zhuang, Y.; Zhou, X.H.; Liu, J. Conserved miRNAs and their response to salt stress in wild eggplant Solanum linnaeanum roots. Int. J. Mol. Sci. 2014, 15, 839–849. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Sun, Y.F.; Song, N.; Wei, J.P.; Wang, X.J.; Feng, H.; Yin, Z.Y.; Kang, Z.S. MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol. Biochem. 2014, 80, 90–96. [Google Scholar] [CrossRef]
- Chen, Z.; Hu, L.; Han, N.; Hu, J.; Yang, Y.; Xiang, T.; Zhang, X.; Wang, L. Overexpression of a miR393-resistant form of transport inhibitor response protein 1 (mTIR1) enhances salt tolerance by increased osmoregulation and Na+ exclusion in Arabidopsis thaliana. Plant Cell Physiol. 2015, 56, 73–83. [Google Scholar] [CrossRef]
- Xia, K.; Wang, R.; Ou, X.; Fang, Z.; Tian, C.; Duan, J.; Wang, Y.; Zhang, M. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 2012, 7, e30039. [Google Scholar] [CrossRef]
- Gao, P.; Bai, X.; Yang, L.; Lv, D.; Pan, X.; Li, Y.; Cai, H.; Ji, W.; Chen, Q.; Zhu, Y. osa-MIR393: A salinity- and alkaline stress-related microRNA gene. Mol. Biol. Rep. 2011, 38, 237–242. [Google Scholar] [CrossRef]
- Liu, X.; Xia, B.; Purente, N.; Chen, B.; Zhou, Y.; He, M. Transgenic Chrysanthemum indicum overexpressing cin-miR396a exhibits altered plant development and reduced salt and drought tolerance. Plant Physiol. Biochem. 2021, 168, 17–26. [Google Scholar] [CrossRef]
- Yuan, H.; Cheng, M.; Wang, R.; Wang, Z.; Fan, F.; Wang, W.; Si, F.; Gao, F.; Li, S. miR396b/GRF6 module contributes to salt tolerance in rice. Plant Biotechnol. J. 2024, 22, 2079–2092. [Google Scholar] [CrossRef]
- Gao, P.; Bai, X.; Yang, L.; Lv, D.; Li, Y.; Cai, H.; Ji, W.; Guo, D.; Zhu, Y. Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 2010, 231, 991–1001. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, D.Q.; Brown, C.W.; Pegler, J.L.; Eamens, A.L.; Grof, C.P.L. Molecular Manipulation of MicroRNA397 Abundance Influences the Development and Salt Stress Response of Arabidopsis thaliana. Int. J. Mol. Sci. 2020, 21, 7879. [Google Scholar] [CrossRef] [PubMed]
- Baek, D.; Chun, H.J.; Kang, S.; Shin, G.; Park, S.J.; Hong, H.; Kim, C.; Kim, D.H.; Lee, S.Y.; Kim, M.C.; et al. A Role for Arabidopsis miR399f in Salt, Drought, and ABA Signaling. Mol. Cells 2016, 39, 111–118. [Google Scholar] [CrossRef] [PubMed]
- Macovei, A.; Tuteja, N. microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol. 2012, 12, 183. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Guo, W.; Li, J.; Pan, X.; Pan, L.; Zhao, J.; Zhang, Y.; Cai, S.; Huang, X.; Wang, A.; et al. The miR528-AO Module Confers Enhanced Salt Tolerance in Rice by Modulating the Ascorbic Acid and Abscisic Acid Metabolism and ROS Scavenging. J. Agric. Food Chem. 2021, 69, 8634–8648. [Google Scholar] [CrossRef] [PubMed]
- Shamloo-Dashtpagerdi, R.; Sisakht, J.N.; Tahmasebi, A. MicroRNA miR1118 contributes to wheat (Triticum aestivum L.) salinity tolerance by regulating the Plasma Membrane Intrinsic Proteins1;5 (PIP1;5) gene. J. Plant Physiol. 2022, 278, 153827. [Google Scholar] [CrossRef] [PubMed]
- Xia, K.; Ou, X.; Tang, H.; Wang, R.; Wu, P.; Jia, Y.; Wei, X.; Xu, X.; Kang, S.H.; Kim, S.K.; et al. Rice microRNA osa-miR1848 targets the obtusifoliol 14α-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress. New Phytol. 2015, 208, 790–802. [Google Scholar] [CrossRef] [PubMed]
- Deng, F.; Zhang, X.; Wang, W.; Yuan, R.; Shen, F. Identification of Gossypium hirsutum long non-coding RNAs (lncRNAs) under salt stress. BMC Plant Biol. 2018, 18, 23. [Google Scholar] [CrossRef]
- Zhang, X.; Dong, J.; Deng, F.; Wang, W.; Cheng, Y.; Song, L.; Hu, M.; Shen, J.; Xu, Q.; Shen, F. The long non-coding RNA lncRNA973 is involved in cotton response to salt stress. BMC Plant Biol. 2019, 19, 459. [Google Scholar] [CrossRef]
- Zhang, X.; Shen, J.; Xu, Q.; Dong, J.; Song, L.; Wang, W.; Shen, F. Long noncoding RNA lncRNA354 functions as a competing endogenous RNA of miR160b to regulate ARF genes in response to salt stress in upland cotton. Plant Cell Environ. 2021, 44, 3302–3321. [Google Scholar] [CrossRef]
- Ye, X.; Wang, S.; Zhao, X.; Gao, N.; Wang, Y.; Yang, Y.; Wu, E.; Jiang, C.; Cheng, Y.; Wu, W.; et al. Role of lncRNAs in cis- and trans-regulatory responses to salt in Populus trichocarpa. Plant J. 2022, 110, 978–993. [Google Scholar] [CrossRef]
- Montez, M.; Majchrowska, M.; Krzyszton, M.; Bokota, G.; Sacharowski, S.; Wrona, M.; Yatusevich, R.; Massana, F.; Plewczynski, D.; Swiezewski, S. Promoter-pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt. EMBO J. 2023, 42, e112443. [Google Scholar] [CrossRef]
- Chen, X.; Jiang, X.; Niu, F.; Sun, X.; Hu, Z.; Gao, F.; Zhang, H.; Jiang, Q. Overexpression of lncRNA77580 Regulates Drought and Salinity Stress Responses in Soybean. Plants 2023, 12, 181. [Google Scholar] [CrossRef] [PubMed]
- Qin, T.; Zhao, H.; Cui, P.; Albesher, N.; Xiong, L. A Nucleus-Localized Long Non-Coding RNA Enhances Drought and Salt Stress Tolerance. Plant Physiol. 2017, 175, 1321–1336. [Google Scholar] [CrossRef] [PubMed]
- Miller, J.C.; Patil, D.P.; Xia, D.F.; Paine, C.B.; Fauser, F.; Richards, H.W.; Shivak, D.A.; Bendaña, Y.R.; Hinkley, S.J.; Scarlott, N.A.; et al. Enhancing gene editing specificity by attenuating DNA cleavage kinetics. Nat. Biotechnol. 2019, 37, 945–952. [Google Scholar] [CrossRef] [PubMed]
- Nakamura, S.; Watanabe, S.; Ando, N.; Ishihara, M.; Sato, M. Transplacental Gene Delivery (TPGD) as a Noninvasive Tool for Fetal Gene Manipulation in Mice. Int. J. Mol. Sci. 2019, 20, 5926. [Google Scholar] [CrossRef] [PubMed]
- Paschon, D.E.; Lussier, S.; Wangzor, T.; Xia, D.F.; Li, P.W.; Hinkley, S.J.; Scarlott, N.A.; Lam, S.C.; Waite, A.J.; Truong, L.N.; et al. Diversifying the structure of zinc finger nucleases for high-precision genome editing. Nat. Commun. 2019, 10, 1133. [Google Scholar] [CrossRef]
- Kim, E.Y.; Kim, K.D.; Cho, J. Harnessing epigenetic variability for crop improvement: Current status and future prospects. Genes Genom. 2021, 44, 259–266. [Google Scholar] [CrossRef]
Epigenetic Modification | Species | Types | Description | References |
---|---|---|---|---|
DNA methylation | Arabidopsis thaliana | Long-term, transgenerational inheritance | Newly acquired stress tolerance and associated de novo DNA methylation are transmitted to the offspring. Progeny exposed to salt exhibited higher tolerance to stress. The PSM depends on altered DNA methylation and small RNA silencing pathways. | [43,44] |
Long-term, transgenerational inheritance | Salt-stress-altered DNA methylation was stably passed on to the next generation. | [37] | ||
Thlaspi arvense | Long-term, transgenerational inheritance | Salinity stress results in higher levels of epigenetic diversities, which are maintained in offspring, affecting the magnitude of phenotypic variation. | [45] | |
Histone methylation | Arabidopsis thaliana | Long-term, somatic memory | Salt treatment-induced shortening and fractionation of H3K27me3 islands affect somatic memory. For example, in primed plants, HKT1 responded more effectively and rapidly to the second salt-stress event. | [46] |
Arabidopsis thaliana | Long-term, somatic memory | Light exposure is essential for salt-induced transcriptional memory to maintain H3K4me3 levels on the P5CS1 gene. | [47] |
Histone Acetylation Sites | Species | Target Genes | Changes under Salt Stress | References |
---|---|---|---|---|
H3K9 | Beta vulgaris | POX | Acetylation | [103] |
Glycine max | Glyma11g02400, Glyma08g41450, Glyma16g27950, Glyma20g30840 | Acetylation | [67] | |
Arabidopsis thaliana | DREB2A, RD29A, RD29B | Acetylation | [104] | |
AtLIP4, AtLTP6, AtLIP3, AtPAD3, AtGST1, AtRAP2.6, AtMYB29, AtCYP79B2, AtGOLS2, AtPLC1, AtIMS3, AtANN1, AtAAP6, AtGSTF10 | Acetylation | [88] | ||
AtANN4 | Deacetylation | |||
Zea mays | ZmEXPB2, ZmXET1, ZmHATB, ZmGCN | Acetylation | [105] | |
Oryza sativa | OsBZ8 | Acetylation | [70] | |
OsMYB91 | Acetylation | [106] | ||
OsHKT2;1 | Deacetylation | [107] | ||
Triticum aestivum | TraesCS4D02G324800, TraesCS1D02G284900, TraesCS3D02G347900 | Acetylation | [108] | |
H3K14 | Arabidopsis thaliana | DREB2A, RD29A, RD29B | Deacetylation | [104] |
NCED3 | Deacetylation | [99] | ||
Nicotiana tabacum | Tsi1, NtC7 | Acetylation | [109] | |
Triticum aestivum | TraesCS4D02G324800, TraesCS1D02G284900, TraesCS3D02G347900 | Acetylation | [108] | |
H3K27 | Beta vulgaris | POX | Acetylation | [103] |
Oryza sativa | OsBZ8 | Acetylation | [70] | |
H4K5 | Zea mays | ZmHATB, ZmGCN5 | Acetylation | [105] |
H4K16 | Arabidopsis thaliana | NCED3 | Deacetylation | [99] |
H3 | Oryza sativa | OsLEA3, OsABI5, OsbZIP72, OsNHX1 | Acetylation | [100] |
LEA1, SOS1 | Acetylation | [93] | ||
DST, ABIL2 | Deacetylation | [110] | ||
Chrysanthemum morifolium | CmMYB121 | Acetylation | [111] | |
H4 | Arabidopsis thaliana | AtSOS1 | Acetylation | [102] |
Oryza sativa | OsLEA3, OsABI5, OsbZIP72, OsNHX1 | Acetylation | [100] | |
DST, ABIL2 | Deacetylation | [110] | ||
Chrysanthemum morifolium | CmMYB121 | Acetylation | [111] |
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Zhang, D.; Zhang, D.; Zhang, Y.; Li, G.; Sun, D.; Zhou, B.; Li, J. Insights into the Epigenetic Basis of Plant Salt Tolerance. Int. J. Mol. Sci. 2024, 25, 11698. https://doi.org/10.3390/ijms252111698
Zhang D, Zhang D, Zhang Y, Li G, Sun D, Zhou B, Li J. Insights into the Epigenetic Basis of Plant Salt Tolerance. International Journal of Molecular Sciences. 2024; 25(21):11698. https://doi.org/10.3390/ijms252111698
Chicago/Turabian StyleZhang, Dongyu, Duoqian Zhang, Yaobin Zhang, Guanlin Li, Dehao Sun, Bo Zhou, and Jingrui Li. 2024. "Insights into the Epigenetic Basis of Plant Salt Tolerance" International Journal of Molecular Sciences 25, no. 21: 11698. https://doi.org/10.3390/ijms252111698