Genome-wide mapping of main histone modifications and coordination regulation of metabolic genes under salt stress in pea (Pisum sativum L)

Heping Wan , Lan Cao , Ping Wang , Hanbing Hu , Rui Guo , Jingdong Chen , Huixia Zhao , Changli Zeng , Xiaoyun Liu

Horticulture Research ›› 2024, Vol. 11 ›› Issue (12) : 259

PDF (212KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (12) :259 DOI: 10.1093/hr/uhae259
Articles
research-article
Genome-wide mapping of main histone modifications and coordination regulation of metabolic genes under salt stress in pea (Pisum sativum L)
Author information +
History +
PDF (212KB)

Abstract

Pea occupy a key position in modern biogenetics, playing multifaceted roles as food, vegetable, fodder, and green manure. However, due to the complex nature of its genome and the prolonged unveiling of high-quality genetic maps, research into the molecular mechanisms underlying pea development and stress responses has been significantly delayed. Furthermore, the exploration of its epigenetic modification profiles and associated regulatory mechanisms remains uncharted. This research conducted a comprehensive investigation of four specific histone marks, namely H3K4me3, H3K27me3, H3K9ac, and H3K9me2, and the transcriptome in pea under normal conditions, and established a global map of genome-wide regulatory elements, chromatin states, and dynamics based on these major modifications. Our analysis identified epigenomic signals across ∼82.6% of the genome. Each modification exhibits distinct enrichment patterns: H3K4me3 is predominantly associated with the gibberellin response pathway, H3K27me3 is primarily associated with auxin and ethylene responses, and H3K9ac is primarily associated with negative regulatory stimulus responses. We also identified a novel bivalent chromatin state (H3K9ac-H3K27me3) in pea, which is related to their development and stress response. Additionally, we unveil that these histone modifications synergistically regulate metabolic-related genes, influencing metabolite production under salt stress conditions. Our findings offer a panoramic view of the major histone modifications in pea, elucidate their interplay, and highlight their transcriptional regulatory roles during salt stress.

Cite this article

Download citation ▾
Heping Wan, Lan Cao, Ping Wang, Hanbing Hu, Rui Guo, Jingdong Chen, Huixia Zhao, Changli Zeng, Xiaoyun Liu. Genome-wide mapping of main histone modifications and coordination regulation of metabolic genes under salt stress in pea (Pisum sativum L). Horticulture Research, 2024, 11 (12) : 259 DOI:10.1093/hr/uhae259

登录浏览全文

4963

注册一个新账户 忘记密码

Author contributions

W.H.P, C.L., W.P., H.H.B., and G.R. performed the experiments. L.X.Y., W.H.P., W.P., C.J.D., and Z.H.X. analyzed the data. L.X.Y., W.H.P., and W.P. wrote the manuscript. L.X.Y. and Z.C.L. designed the experiment and supervised the research. All authors contributed to the article and approved the submitted version.

Data availability

All raw sequencing data generated in this project, including RNA-seq and Chip-seq, were deposited at GSA (https://www.ngdc.cncb.ac.cn/) under BioProject accession number PRJCA020204.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008; 59:651-81

[2]

Shrivastava P, Kumar R. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci. 2015; 22:123-31

[3]

Datir S, Singh N, Joshi I. Effect of NaCl-induced salinity stress on growth, osmolytes and enzyme activities in wheat genotypes. Bull Environ Contam Toxicol. 2020; 104:351-7

[4]

Parida AK, Das AB. Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf. 2005; 60:324-49

[5]

Agarwal PK, Shukla PS, Gupta K. et al. Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol. 2013; 54:102-23

[6]

Zhang M, Smith JA, Harberd NP. et al. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol. 2016; 91:651-9

[7]

Zhu JK. Abiotic stress signaling and responses in plants. Cell. 2016; 167:313-24

[8]

Steffen PA, Ringrose L. What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat Rev Mol Cell Biol. 2014; 15:340-56

[9]

Zhang X, Bernatavichute YV, Cokus S. et al. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 2009; 10:R62

[10]

Makarevitch I, Eichten SR, Briskine R. et al. Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell. 2013; 25:780-93

[11]

Liu Y, Wang J, Liu B. et al. Dynamic regulation of DNA methylation and histone modifications in response to abiotic stresses in plants. J Integr Plant Biol. 2022; 64:2252-74

[12]

Shen Y, Chi Y, Lu S. et al. Involvement of JMJ 15 in the dynamic change of genome-wide H3K4me3 in response to salt stress. Front Plant Sci. 2022; 13:1009723

[13]

Liu Y, Chen X, Xue S. et al. SET DOMAIN GROUP 721 protein functions in saline-alkaline stress tolerance in the model rice variety Kitaake. Plant Biotechnol J. 2021; 19:2576-88

[14]

Sani E, Herzyk P, Perrella G. et al. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 2013; 14:R59

[15]

Sun L, Song G, Guo W. et al. Dynamic changes in genome-wide Histone3 Lysine27 Trimethylation and gene expression of soybean roots in response to salt stress. Front Plant Sci. 2019; 10:1031

[16]

Paul A, Dasgupta P, Roy D. et al. Comparative analysis of histone modifications and DNA methylation at OsBZ 8 locus under salinity stress in IR64 and Nonabokra rice varieties. Plant Mol Biol. 2017; 95:63-88

[17]

Li H, Yan S, Zhao L. et al. 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

[18]

Liu K, Chen J, Sun S. et al. Histone deacetylase OsHDA706 increases salt tolerance via H4K5/K8 deacetylation of OsPP2C49 in rice. J Integr Plant Biol. 2023; 65:1394-407

[19]

Magraner-Pardo L, Pelechano V, Coloma MD. et al. Dynamic remodeling of histone modifications in response to osmotic stress in Saccharomyces cerevisiae. BMC Genomics. 2014; 15:247

[20]

Sokol A, Kwiatkowska A, Jerzmanowski A. et al. 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 H 4 modifications. Planta. 2007; 227:245-54

[21]

Tilak P, Kotnik F, Née G. et al. Proteome-wide lysine acetylation profiling to investigate the involvement of histone deacetylase HDA 5 in the salt stress response of Arabidopsis leaves. Plant J. 2023; 115:275-92

[22]

Zheng Y, Ding Y, Sun X. et al. Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot. 2016; 67:1703-13

[23]

Yolcu S, Ozdemir F, Guler A. et al. 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

[24]

Ueda M, Matsui A, Tanaka M. et al. The distinct roles of Class I and II RPD3-like histone deacetylases in salinity stress response. Plant Physiol. 2017; 175:1760-73

[25]

Ueda M, Matsui A, Watanabe S. et al. Transcriptome analysis of the hierarchical response of histone deacetylase proteins that respond in an antagonistic manner to salinity stress. Front Plant Sci. 2019; 10:1323

[26]

Wei F, Tang D, Li Z. et al. 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

[27]

Zheng M, Liu X, Lin J. et al. Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. Plant J. 2019; 97:587-602

[28]

Kaldis A, Tsementzi D, Tanriverdi O. et al. Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses. Planta. 2011; 233:749-62

[29]

Yung W, Wang Q, Huang M. et al. Priming-induced alterations in histone modifications modulate transcriptional responses in soybean under salt stress. Plant J. 2022; 109:1575-90

[30]

Yang T, Liu R, Luo Y. et al. Improved pea reference genome and pan-genome highlight genomic features and evolutionary characteristics. Nat Genet. 2022; 54:1553-+

[31]

Tayeh N, Aubert G, Pilet-Nayel ML. et al. Genomic tools in pea breeding programs: status and perspectives. Front Plant Sci. 2015; 6:1037

[32]

Subbarao GV, Nam NH, Chauhan YS. et al. Osmotic adjustment, water relations and carbohydrate remobilization in pigeonpea under water deficits. J Plant Physiol. 2000; 157:651-9

[33]

Hossain Khan MA, Baset Mia MA, Quddus MA. et al. Salinity-induced physiological changes in pea (Pisum sativum L.): germination rate, biomass accumulation, relative water content, seedling vigor and salt tolerance index. Plants (Basel). 2022; 11:3493

[34]

Najafi F, Khavari-Nejad RA, Rastgar-Jazii F. et al. Growth and some physiological attributes of pea (Pisum sativum L.) as affected by salinity. Pak J Biol Sci. 2007; 10:2752-5

[35]

Ellis THN, Hofer JMI, Timmerman-Vaughan GM. et al. Mendel, 150 years on. Trends Plant Sci. 2011; 16:590-6

[36]

Reid JB, Ross JJ. Mendel’s genes: toward a full molecular characterization. Genetics. 2011; 189:3-10

[37]

Chandrasekaran S. Tying metabolic branches with histone tails using systems biology. Epigenet Insights. 2019; 12:251686571986968

[38]

Chen X, Zhou DX. Rice epigenomics and epigenetics: challenges and opportunities. Curr Opin Plant Biol. 2013; 16:164-9

[39]

Roudier F, Ahmed I, Bérard C. et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011; 30:1928-38

[40]

Sequeira-Mendes J, Aragüez I, Peiró R. et al. The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell. 2014; 26:2351-66

[41]

Afonin AM, Gribchenko ES, Zorin EA. et al. DNA methylation patterns differ between free-living rhizobium leguminosarum RCAM1026 and bacteroids formed in symbiosis with pea (Pisum sativum L.). MICROORGANISMS. 2021; 9:2458

[42]

Macas J, Ávila Robledillo L, Kreplak J. et al. Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes. PLoS Genet. 2023; 19:e1010633

[43]

Alhosin M. Epigenetics mechanisms of honeybees: secrets of Royal Jelly. Epigenet Insights. 2023; 16:25168657231213717

[44]

He G, Zhu X, Elling AA. et al. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell. 2010; 22:17-33

[45]

Du Z, Li H, Wei Q. et al. Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Japonica. Mol Plant. 2013; 6:1463-72

[46]

Zhang Q, Guan P, Zhao L. et al. Asymmetric epigenome maps of subgenomes reveal imbalanced transcription and distinct evolutionary trends in Brassica napus. Mol Plant. 2021; 14:604-19

[47]

Zhou C, Zhou H, Ma X. et al. Genome-wide identification and characterization of main histone modifications in sorghum decipher regulatory mechanisms involved by mRNA and long noncoding RNA genes. J Agric Food Chem. 2021; 69:2337-47

[48]

Li Z, Wang M, Lin K. et al. The bread wheat epigenomic map reveals distinct chromatin architectural and evolutionary features of functional genetic elements. Genome Biol. 2019; 20:139

[49]

Ernst J, Kellis M. Chromatin-state discovery and genome annotation with ChromHMM. Nat Protoc. 2017; 12:2478-92

[50]

Han B, Xu W, Ahmed N. et al. Changes and associations of genomic transcription and histone methylation with salt stress in Castor bean. Plant Cell Physiol. 2020; 61:1120-33

[51]

Hu Y, Liu D, Zhong X. et al. CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci USA. 2012; 109:5773-8

[52]

Charron JB, He H, Elling AA. et al. Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell. 2009; 21:3732-48

[53]

Bernstein BE, Mikkelsen TS, Xie X. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006; 125:315-26

[54]

Zhao XD, Han X, Chew JL. et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell. 2007; 1:286-98

[55]

Xiang Y, Zhang Y, Xu Q. et al. Epigenomic analysis of gastrulation identifies a unique chromatin state for primed pluripotency. Nat Genet. 2020; 52:95-105

[56]

Kim S, Lee J, Yang J. et al. Arabidopsis histone methyltransferase SET DOMAIN GROUP2 is required for regulation of various hormone responsive genes. JOURNAL OF PLANT BIOLOGY. 2013; 56:39-48

[57]

Liu N, Fromm M, Avramova Z. H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of Arabidopsis thaliana. Mol Plant. 2014; 7:502-13

[58]

Zeng Z, Zhang W, Marand AP. et al. Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato. Genome Biol. 2019; 20:123

[59]

Blanco E, Gonzalez-Ramirez M, Alcaine-Colet A. et al. The bivalent genome: characterization, structure, and regulation. Trends Genet. 2020; 36:118-31

[60]

Zhao L, Xie L, Zhang Q. et al. Integrative analysis of reference epigenomes in 20 rice varieties. Nat Commun. 2020; 11:2658

[61]

Chen S, Zhou Y, Chen Y. et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34:i884-90

[62]

Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37:907-15

[63]

Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15:550

[64]

Saleh A, Alvarez-Venegas R, Avramova Z. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc. 2008; 3:1018-25

[65]

Desvoyes B, Sequeira-Mendes J, Vergara Z. et al. Sequential ChIP protocol for profiling bivalent epigenetic modifications (ReChIP). Methods Mol Biol. 2018; 1675:83-97

[66]

Zhang Y, Liu T, Meyer CA. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008; 9:R137

[67]

Robinson JT, Thorvaldsdóttir H, Winckler W. et al. Integrative genomics viewer. Nat Biotechnol. 2011; 29:24-6

[68]

Ramirez F, Ryan DP, Grüning B. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016; 44:W160-5

[69]

Du Z, Zhou X, Ling Y. et al. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010; 38:W64-70

[70]

Mao XZ, Cai T, Olyarchuk JG. et al. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005; 21:3787-93

[71]

Wu LY, Shang GD, Wang FX. et al. Dynamic chromatin state profiling reveals regulatory roles of auxin and cytokinin in shoot regeneration. Dev Cell. 2022; 57:526-542.e7

[72]

Zhang H, Jin Z, Cui F. et al. Epigenetic modifications regulate cultivar-specific root development and metabolic adaptation to nitrogen availability in wheat. Nat Commun. 2023; 14:8238

[73]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25:402-8

[74]

Die JV, Roman B, Nadal S. et al. Evaluation of candidate reference genes for expression studies in Pisum sativum under different experimental conditions. Planta. 2010; 232:145-53

PDF (212KB)

81

Accesses

0

Citation

Detail

Sections
Recommended

/