Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold.


Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
17 Feb 2022
Historique:
received: 29 09 2021
accepted: 13 01 2022
entrez: 18 2 2022
pubmed: 19 2 2022
medline: 22 2 2022
Statut: epublish

Résumé

DNA methylation is thought to influence the expression of genes, especially in response to changing environmental conditions and developmental changes. Sugar beet (Beta vulgaris ssp. vulgaris), and other biennial or perennial plants are inevitably exposed to fluctuating temperatures throughout their lifecycle and might even require such stimulus to acquire floral competence. Therefore, plants such as beets, need to fine-tune their epigenetic makeup to ensure phenotypic plasticity towards changing environmental conditions while at the same time steering essential developmental processes. Different crop species may show opposing reactions towards the same abiotic stress, or, vice versa, identical species may respond differently depending on the specific kind of stress. In this study, we investigated common effects of cold treatment on genome-wide DNA methylation and gene expression of two Beta vulgaris accessions via multi-omics data analysis. Cold exposure resulted in a pronounced reduction of DNA methylation levels, which particularly affected methylation in CHH context (and to a lesser extent CHG) and was accompanied by transcriptional downregulation of the chromomethyltransferase CMT2 and strong upregulation of several genes mediating active DNA demethylation. Integration of methylomic and transcriptomic data revealed that, rather than methylation having directly influenced expression, epigenetic modifications correlated with changes in expression of known players involved in DNA (de)methylation. In particular, cold triggered upregulation of genes putatively contributing to DNA demethylation via the ROS1 pathway. Our observations suggest that these transcriptional responses precede the cold-induced global DNA-hypomethylation in non-CpG, preparing beets for additional transcriptional alterations necessary for adapting to upcoming environmental changes.

Sections du résumé

BACKGROUND BACKGROUND
DNA methylation is thought to influence the expression of genes, especially in response to changing environmental conditions and developmental changes. Sugar beet (Beta vulgaris ssp. vulgaris), and other biennial or perennial plants are inevitably exposed to fluctuating temperatures throughout their lifecycle and might even require such stimulus to acquire floral competence. Therefore, plants such as beets, need to fine-tune their epigenetic makeup to ensure phenotypic plasticity towards changing environmental conditions while at the same time steering essential developmental processes. Different crop species may show opposing reactions towards the same abiotic stress, or, vice versa, identical species may respond differently depending on the specific kind of stress.
RESULTS RESULTS
In this study, we investigated common effects of cold treatment on genome-wide DNA methylation and gene expression of two Beta vulgaris accessions via multi-omics data analysis. Cold exposure resulted in a pronounced reduction of DNA methylation levels, which particularly affected methylation in CHH context (and to a lesser extent CHG) and was accompanied by transcriptional downregulation of the chromomethyltransferase CMT2 and strong upregulation of several genes mediating active DNA demethylation.
CONCLUSION CONCLUSIONS
Integration of methylomic and transcriptomic data revealed that, rather than methylation having directly influenced expression, epigenetic modifications correlated with changes in expression of known players involved in DNA (de)methylation. In particular, cold triggered upregulation of genes putatively contributing to DNA demethylation via the ROS1 pathway. Our observations suggest that these transcriptional responses precede the cold-induced global DNA-hypomethylation in non-CpG, preparing beets for additional transcriptional alterations necessary for adapting to upcoming environmental changes.

Identifiants

pubmed: 35176993
doi: 10.1186/s12864-022-08312-2
pii: 10.1186/s12864-022-08312-2
pmc: PMC8855596
doi:

Substances chimiques

Proto-Oncogene Proteins 0
Sugars 0
Protein-Tyrosine Kinases EC 2.7.10.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

144

Informations de copyright

© 2022. The Author(s).

Références

Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Mol Plant. 2014 Sep;7(9):1470-1485
pubmed: 25009302
Plant Cell. 2010 Feb;22(2):321-34
pubmed: 20173091
Nucleic Acids Res. 2019 Jul 2;47(W1):W260-W265
pubmed: 31028399
Plant Mol Biol. 2015 Jul;88(4-5):387-400
pubmed: 25944663
Nat Struct Mol Biol. 2009 Dec;16(12):1325-7
pubmed: 19915591
Nature. 2013 Jun 20;498(7454):385-9
pubmed: 23636332
Plants (Basel). 2020 May 04;9(5):
pubmed: 32375329
Mol Plant. 2018 Mar 5;11(3):381-387
pubmed: 29032247
Funct Integr Genomics. 2009 Aug;9(3):277-86
pubmed: 19221817
Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32
pubmed: 26296162
Mol Plant. 2019 Jun 3;12(6):879-892
pubmed: 30639314
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Front Plant Sci. 2019 Mar 01;10:246
pubmed: 30881369
Epigenetics. 2012 Aug;7(8):950-60
pubmed: 22810086
Plant J. 2021 Jun;106(5):1312-1327
pubmed: 33730390
Nat Rev Genet. 2010 Mar;11(3):204-20
pubmed: 20142834
PLoS Genet. 2011 Jul;7(7):e1002195
pubmed: 21811420
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6752-7
pubmed: 17409185
Nat Rev Mol Cell Biol. 2018 Aug;19(8):489-506
pubmed: 29784956
J Exp Bot. 2016 Jan;67(1):207-25
pubmed: 26463996
PLoS Genet. 2010 Oct 28;6(10):e1001182
pubmed: 21060858
Nat Rev Mol Cell Biol. 2011 Jul 22;12(8):483-92
pubmed: 21779025
Proc Natl Acad Sci U S A. 2018 May 15;115(20):E4720-E4729
pubmed: 29712855
3 Biotech. 2018 Mar;8(3):172
pubmed: 29556426
Nat Rev Genet. 2014 Jun;15(6):394-408
pubmed: 24805120
Mol Cell. 2009 Jan 30;33(2):192-203
pubmed: 19110459
Front Plant Sci. 2016 Nov 08;7:1627
pubmed: 27877178
Plant Physiol. 2018 Jun;177(2):652-670
pubmed: 29572390
Genome Biol. 2015 Sep 02;16:184
pubmed: 26328666
Mol Plant. 2013 Nov;6(6):1961-74
pubmed: 23966636
Genome Biol. 2014;15(12):550
pubmed: 25516281
PLoS Genet. 2015 Mar 31;11(3):e1005142
pubmed: 25826366
Curr Biol. 2007 Feb 20;17(4):379-84
pubmed: 17239600
Methods Mol Biol. 2017;1640:1-21
pubmed: 28608331
Nat Plants. 2016 Nov 03;2(11):16163
pubmed: 27808230
PLoS Genet. 2014 Dec 11;10(12):e1004842
pubmed: 25503602
J Integr Plant Biol. 2020 Jan;62(1):148-159
pubmed: 31628716
Plant J. 2014 Jun;78(6):937-50
pubmed: 24661787
Cell. 2008 May 2;133(3):523-36
pubmed: 18423832
Plant Cell Rep. 2018 Jan;37(1):77-85
pubmed: 29026973
Curr Opin Plant Biol. 2009 Apr;12(2):133-9
pubmed: 19179104
Biochim Biophys Acta. 2011 Aug;1809(8):360-8
pubmed: 21549230
BMC Bioinformatics. 2019 May 16;20(1):253
pubmed: 31096906
BMC Res Notes. 2014 Oct 14;7:721
pubmed: 25316414
Cell. 2013 Mar 28;153(1):193-205
pubmed: 23540698
BMC Genomics. 2020 May 29;21(1):375
pubmed: 32471342
Proc Natl Acad Sci U S A. 2013 May 14;110(20):8290-5
pubmed: 23637343
Nucleic Acids Res. 2012 Sep 1;40(17):e136
pubmed: 22649061
Int J Mol Sci. 2017 Apr 18;18(4):
pubmed: 28420190
Plant J. 2017 Jun;90(6):1156-1175
pubmed: 28257158
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W465-9
pubmed: 18424797
Nat Struct Mol Biol. 2014 Jan;21(1):64-72
pubmed: 24336224
BMC Genomics. 2020 Mar 2;21(1):189
pubmed: 32122300
Science. 2003 Jan 31;299(5607):716-9
pubmed: 12522258
Genome Biol. 2018 Dec 4;19(1):212
pubmed: 30514401
Cell. 2002 Dec 13;111(6):803-14
pubmed: 12526807
Nature. 2014 Jan 23;505(7484):546-9
pubmed: 24352233
Proc Natl Acad Sci U S A. 2015 Jan 20;112(3):911-6
pubmed: 25561521
Mol Cell. 2019 Aug 8;75(3):576-589.e5
pubmed: 31398324
PLoS Genet. 2014 Jan 30;10(1):e1004115
pubmed: 24497839
Genetics. 2003 Mar;163(3):1109-22
pubmed: 12663548
Plant J. 2021 Aug;107(3):727-739
pubmed: 33977637
BMC Genomics. 2012 Jul 02;13:300
pubmed: 22747568
Front Plant Sci. 2013 Apr 01;4:66
pubmed: 23554602
Curr Opin Plant Biol. 2015 Oct;27:154-64
pubmed: 26344361
Cell. 2013 Jan 17;152(1-2):352-64
pubmed: 23313553
Physiol Mol Biol Plants. 2013 Jul;19(3):379-87
pubmed: 24431506
Bioinformatics. 2016 Oct 1;32(19):3047-8
pubmed: 27312411
Physiol Plant. 2018 Feb;162(2):239-250
pubmed: 29080251
Nature. 2008 Mar 13;452(7184):215-9
pubmed: 18278030
PLoS Genet. 2013 Nov;9(11):e1003946
pubmed: 24244201
J Exp Bot. 2017 Feb 1;68(5):1213-1224
pubmed: 28158841
Proc Natl Acad Sci U S A. 2006 May 2;103(18):6853-8
pubmed: 16624880
Mol Cell. 2015 Mar 19;57(6):971-983
pubmed: 25684209
Genome Biol. 2012 Oct 03;13(10):R87
pubmed: 23034086
Plant Cell. 2020 Oct;32(10):3206-3223
pubmed: 32769131
Elife. 2021 Jan 20;10:
pubmed: 33470193
Elife. 2021 Dec 01;10:
pubmed: 34850679
Science. 2010 May 14;328(5980):916-9
pubmed: 20395474
Plant Mol Biol. 2005 Jan;57(2):173-88
pubmed: 15821876
PLoS Biol. 2004 May;2(5):E104
pubmed: 15024409
Cell. 2006 Sep 22;126(6):1189-201
pubmed: 16949657
Front Plant Sci. 2020 Dec 07;11:608540
pubmed: 33365044
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Proc Natl Acad Sci U S A. 2018 Sep 11;115(37):E8793-E8802
pubmed: 30150382
Mol Cell. 2012 Dec 14;48(5):811-8
pubmed: 23142082
Plant Mol Biol. 2007 Apr;63(6):777-85
pubmed: 17221360
Cell Discov. 2018 Oct 16;4:55
pubmed: 30345072
Sci Rep. 2020 May 15;10(1):8013
pubmed: 32415195
Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11796-801
pubmed: 16864782
Plant J. 2012 Sep;71(5):776-86
pubmed: 22519754
Genome Biol. 2016 Sep 27;17(1):194
pubmed: 27671052
PLoS One. 2018 Jan 19;13(1):e0191492
pubmed: 29352281
PLoS Genet. 2016 Dec 20;12(12):e1006526
pubmed: 27997534
Front Plant Sci. 2015 May 06;6:308
pubmed: 25999972
Cell Res. 2015 Jun;25(6):757-60
pubmed: 25906993
J Agric Food Chem. 2020 Jul 1;68(26):7024-7031
pubmed: 32520546
Annu Rev Genet. 2009;43:143-66
pubmed: 19659441
Genes Dev. 2009 Feb 1;23(3):318-30
pubmed: 19204117
Plant Physiol. 2021 May 27;186(1):420-433
pubmed: 33591319
BMC Plant Biol. 2018 Apr 23;18(1):70
pubmed: 29685105
Curr Biol. 2002 Jul 9;12(13):1138-44
pubmed: 12121623
Mol Cell Biol. 2005 Dec;25(23):10507-15
pubmed: 16287862
Bioinformatics. 2011 Jun 1;27(11):1571-2
pubmed: 21493656
Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13729-34
pubmed: 26483493
Nat Methods. 2015 Feb;12(2):115-21
pubmed: 25633503
Plant Cell Environ. 2017 Oct;40(10):2236-2249
pubmed: 28707409
Plant Cell Rep. 2017 May;36(5):759-772
pubmed: 27999979
Nucleic Acids Res. 2018 Jan 4;46(D1):D1190-D1196
pubmed: 29069403
Proc Natl Acad Sci U S A. 2016 Nov 1;113(44):12580-12585
pubmed: 27791156
Cell. 2014 May 22;157(5):1050-60
pubmed: 24855943
Science. 2005 Apr 1;308(5718):118-20
pubmed: 15692015
Environ Mol Mutagen. 2008 Jan;49(1):61-72
pubmed: 17948278
Plant J. 2008 Aug;55(4):596-606
pubmed: 18433438
BMC Genomics. 2018 Jan 24;19(1):78
pubmed: 29361906
Nat Plants. 2016 Oct 31;2(11):16169
pubmed: 27797352
Plant Cell. 2007 Oct;19(10):2975-87
pubmed: 17921315
Proc Natl Acad Sci U S A. 2017 Jan 3;114(1):172-177
pubmed: 27999181
J Biol Chem. 2002 Oct 4;277(40):37741-6
pubmed: 12124387
Elife. 2019 May 28;8:
pubmed: 31135340
Chromosoma. 2004 Mar;112(6):308-15
pubmed: 15014946
BMC Genomics. 2017 Apr 13;18(1):297
pubmed: 28407801
Nat Genet. 2018 Jun;50(6):865-873
pubmed: 29736015
Proc Natl Acad Sci U S A. 2018 Jan 30;115(5):E1069-E1074
pubmed: 29339507
Plant Mol Biol. 2008 Aug;67(6):671-81
pubmed: 18493721
Cell. 2005 Mar 11;120(5):613-22
pubmed: 15766525
Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3553-7
pubmed: 25733903
Epigenetics. 2011 Mar;6(3):344-54
pubmed: 21150311
Plant Cell Environ. 2020 Jan;43(1):275-291
pubmed: 31703150
Proc Natl Acad Sci U S A. 2019 Aug 13;116(33):16641-16650
pubmed: 31363048

Auteurs

Sindy Gutschker (S)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany.

José María Corral (JM)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany.

Alfred Schmiedl (A)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany.

Frank Ludewig (F)

KWS SAAT SE & Co. KGaA, Grimsehlstraße 31, 37574, Einbeck, Germany.

Wolfgang Koch (W)

KWS SAAT SE & Co. KGaA, Grimsehlstraße 31, 37574, Einbeck, Germany.

Karin Fiedler-Wiechers (K)

KWS SAAT SE & Co. KGaA, Grimsehlstraße 31, 37574, Einbeck, Germany.

Olaf Czarnecki (O)

KWS SAAT SE & Co. KGaA, Grimsehlstraße 31, 37574, Einbeck, Germany.

Karsten Harms (K)

Südzucker AG, Central Department for Research, Development, and Service, Wormser Straße 11, 67283, Obrigheim/Pfalz, Germany.

Isabel Keller (I)

Plant Physiology, TU Kaiserslautern, Building 22, Erwin-Schrödinger-Straße, 67663, Kaiserslautern, Germany.

Cristina Martins Rodrigues (C)

Plant Physiology, TU Kaiserslautern, Building 22, Erwin-Schrödinger-Straße, 67663, Kaiserslautern, Germany.

Benjamin Pommerrenig (B)

Plant Physiology, TU Kaiserslautern, Building 22, Erwin-Schrödinger-Straße, 67663, Kaiserslautern, Germany.

H Ekkehard Neuhaus (HE)

Plant Physiology, TU Kaiserslautern, Building 22, Erwin-Schrödinger-Straße, 67663, Kaiserslautern, Germany.

Wolfgang Zierer (W)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany.

Uwe Sonnewald (U)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany.

Christina Müdsam (C)

Biochemistry, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Staudtstraße 5, 91058, Erlangen, Germany. christina.muedsam@fau.de.

Articles similaires

Endometriosis Female Humans Animals Mice
Humans DNA Methylation Female Male Alcohol Oxidoreductases
Animals Epigenesis, Genetic DNA Methylation Skates, Fish CpG Islands

Classifications MeSH