Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.).
Cotton
Methylome
Small RNA
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
13 Oct 2023
13 Oct 2023
Historique:
received:
17
05
2023
accepted:
28
09
2023
medline:
23
10
2023
pubmed:
13
10
2023
entrez:
12
10
2023
Statut:
epublish
Résumé
Heterosis is a complex phenomenon wherein the hybrids outperform their parents. Understanding the underlying molecular mechanism by which hybridization leads to higher yields in allopolyploid cotton is critical for effective breeding programs. Here, we integrated DNA methylation, transcriptomes, and small RNA profiles to comprehend the genetic and molecular basis of heterosis in allopolyploid cotton at three developmental stages. Transcriptome analysis revealed that numerous DEGs responsive to phytohormones (auxin and salicylic acid) were drastically altered in F1 hybrid compared to the parental lines. DEGs involved in energy metabolism and plant growth were upregulated, whereas DEGs related to basal defense were downregulated. Differences in homoeologous gene expression in F1 hybrid were greatly reduced after hybridization, suggesting that higher levels of parental expression have a vital role in heterosis. Small RNAome and methylome studies showed that the degree of DNA methylation in hybrid is higher when compared to the parents. A substantial number of allele-specific expression genes were found to be strongly regulated by CG allele-specific methylation levels. The hybrid exhibited higher 24-nt-small RNA (siRNA) expression levels than the parents. The regions in the genome with increased levels of 24-nt-siRNA were chiefly related to genes and their flanking regulatory regions, demonstrating a possible effect of these molecules on gene expression. The transposable elements correlated with siRNA clusters in the F1 hybrid had higher methylation levels but lower expression levels, which suggest that these non-additively expressed siRNA clusters, reduced the activity of transposable elements through DNA methylation in the hybrid. These multi-omics data provide insights into how changes in epigenetic mechanisms and gene expression patterns can lead to heterosis in allopolyploid cotton. This makes heterosis a viable tool in cotton breeding.
Sections du résumé
BACKGROUND
BACKGROUND
Heterosis is a complex phenomenon wherein the hybrids outperform their parents. Understanding the underlying molecular mechanism by which hybridization leads to higher yields in allopolyploid cotton is critical for effective breeding programs. Here, we integrated DNA methylation, transcriptomes, and small RNA profiles to comprehend the genetic and molecular basis of heterosis in allopolyploid cotton at three developmental stages.
RESULTS
RESULTS
Transcriptome analysis revealed that numerous DEGs responsive to phytohormones (auxin and salicylic acid) were drastically altered in F1 hybrid compared to the parental lines. DEGs involved in energy metabolism and plant growth were upregulated, whereas DEGs related to basal defense were downregulated. Differences in homoeologous gene expression in F1 hybrid were greatly reduced after hybridization, suggesting that higher levels of parental expression have a vital role in heterosis. Small RNAome and methylome studies showed that the degree of DNA methylation in hybrid is higher when compared to the parents. A substantial number of allele-specific expression genes were found to be strongly regulated by CG allele-specific methylation levels. The hybrid exhibited higher 24-nt-small RNA (siRNA) expression levels than the parents. The regions in the genome with increased levels of 24-nt-siRNA were chiefly related to genes and their flanking regulatory regions, demonstrating a possible effect of these molecules on gene expression. The transposable elements correlated with siRNA clusters in the F1 hybrid had higher methylation levels but lower expression levels, which suggest that these non-additively expressed siRNA clusters, reduced the activity of transposable elements through DNA methylation in the hybrid.
CONCLUSIONS
CONCLUSIONS
These multi-omics data provide insights into how changes in epigenetic mechanisms and gene expression patterns can lead to heterosis in allopolyploid cotton. This makes heterosis a viable tool in cotton breeding.
Identifiants
pubmed: 37828433
doi: 10.1186/s12870-023-04495-2
pii: 10.1186/s12870-023-04495-2
pmc: PMC10571366
doi:
Substances chimiques
DNA Transposable Elements
0
RNA, Small Interfering
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
488Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Plants (Basel). 2015 Feb 16;4(1):112-66
pubmed: 27135320
Front Plant Sci. 2019 Mar 01;10:246
pubmed: 30881369
Nat Rev Mol Cell Biol. 2018 Aug;19(8):489-506
pubmed: 29784956
BMC Plant Biol. 2020 Jul 3;20(1):311
pubmed: 32620077
PLoS One. 2012;7(10):e47043
pubmed: 23118865
Plant Cell Rep. 2018 Mar;37(3):515-528
pubmed: 29318384
Trends Plant Sci. 2007 Dec;12(12):556-63
pubmed: 18198522
Plants (Basel). 2021 May 30;10(6):
pubmed: 34070712
Plant Biotechnol J. 2020 Aug;18(8):1697-1710
pubmed: 31925873
BMC Plant Biol. 2021 Jan 6;21(1):19
pubmed: 33407144
Genomics. 2020 Sep;112(5):3354-3364
pubmed: 32574832
GM Crops Food. 2021 Jan 2;12(1):224-241
pubmed: 33410724
Curr Opin Chem Biol. 2019 Aug;51:11-17
pubmed: 30825741
Plant Physiol Biochem. 2021 Nov;168:381-397
pubmed: 34715564
Proc Natl Acad Sci U S A. 2015 Nov 17;112(46):E6397-406
pubmed: 26527659
Front Plant Sci. 2022 Apr 27;13:770098
pubmed: 35574131
Planta. 2021 Aug 30;254(3):62
pubmed: 34459999
Nucleic Acids Res. 2023 Jan 6;51(D1):D587-D592
pubmed: 36300620
Plant Cell Rep. 2022 Mar;41(3):765-773
pubmed: 34228188
Mol Plant. 2015 Jul;8(7):998-1010
pubmed: 25620770
Gene. 2020 Aug 5;750:144725
pubmed: 32360839
Planta. 2016 Feb;243(2):429-40
pubmed: 26445769
Proc Natl Acad Sci U S A. 2012 Jul 24;109(30):12040-5
pubmed: 22778444
Nat Commun. 2012 Jul 17;3:950
pubmed: 22805557
Proc Natl Acad Sci U S A. 2022 Nov;119(44):e2209743119
pubmed: 36279429
BMC Genomics. 2018 Aug 6;19(1):586
pubmed: 30081834
BMC Plant Biol. 2022 Jul 18;22(1):348
pubmed: 35843937
BMC Genomics. 2021 Apr 17;22(1):277
pubmed: 33865322
Front Genet. 2021 Feb 24;12:643761
pubmed: 33719351
PLoS One. 2019 Jun 24;14(6):e0218381
pubmed: 31233531
Plant Cell. 2012 Mar;24(3):875-92
pubmed: 22438023
Nat Commun. 2019 Jul 5;10(1):2982
pubmed: 31278256
Plant Physiol Biochem. 2015 Sep;94:153-64
pubmed: 26093308
Annu Rev Plant Biol. 2013;64:71-88
pubmed: 23394499
Chembiochem. 2015 Jan 19;16(2):195-203
pubmed: 25469751
BMC Plant Biol. 2020 May 27;20(1):239
pubmed: 32460693
Natl Sci Rev. 2017 Jan;4(1):10-15
pubmed: 30034910
Nat Rev Genet. 2022 Jan;23(1):55-68
pubmed: 34526697
Nat Plants. 2015 Jul 06;1:15092
pubmed: 27250257
Plant J. 2021 Oct;108(2):347-357
pubmed: 34314526
Breed Sci. 2018 Mar;68(2):145-158
pubmed: 29875598
BMC Plant Biol. 2008 Nov 11;8:114
pubmed: 19000321
Mol Plant. 2010 Sep;3(5):794-806
pubmed: 20720155
BMC Genomics. 2020 Feb 10;21(1):140
pubmed: 32041531
Genes (Basel). 2021 Oct 24;12(11):
pubmed: 34828294
Front Genet. 2021 Aug 20;12:685788
pubmed: 34490032
Proc Natl Acad Sci U S A. 2021 Apr 20;118(16):
pubmed: 33846256
PLoS Genet. 2016 Aug 19;12(8):e1006263
pubmed: 27541584
Theor Appl Genet. 2006 Sep;113(5):831-45
pubmed: 16868764
Trends Plant Sci. 2013 Mar;18(3):157-66
pubmed: 22939172
Plant Cell. 2007 Jan;19(1):148-62
pubmed: 17237352
Genomics. 2021 May;113(3):1146-1156
pubmed: 33667647
Plants (Basel). 2022 Apr 22;11(9):
pubmed: 35567137
Plant J. 2017 Sep;91(5):874-893
pubmed: 28544196
Proc Natl Acad Sci U S A. 2012 May 1;109(18):7109-14
pubmed: 22493265
J Exp Bot. 2014 Nov;65(20):5989-6002
pubmed: 25129133
Hortic Res. 2021 Mar 1;8(1):39
pubmed: 33642594
Biochim Biophys Acta Gene Regul Mech. 2017 May;1860(5):636-644
pubmed: 27989935
Proc Natl Acad Sci U S A. 2011 Feb 8;108(6):2617-22
pubmed: 21266545
Gene. 2018 Jun 20;660:80-91
pubmed: 29577977
Protein Sci. 2019 Nov;28(11):1947-1951
pubmed: 31441146
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
PeerJ. 2019 Sep 13;7:e7621
pubmed: 31565564
Front Plant Sci. 2022 Mar 31;13:761244
pubmed: 35432420
Genes (Basel). 2021 Jan 11;12(1):
pubmed: 33440604
J Integr Plant Biol. 2022 Mar;64(3):671-687
pubmed: 34963038
Front Plant Sci. 2022 Feb 18;13:824240
pubmed: 35251094
Biology (Basel). 2021 Aug 11;10(8):
pubmed: 34439998
J Exp Bot. 2019 Mar 27;70(6):1859-1873
pubmed: 30759246
Molecules. 2019 Sep 17;24(18):
pubmed: 31533323
Proc Natl Acad Sci U S A. 2017 Apr 25;114(17):E3555-E3562
pubmed: 28396418
Genes Dev. 2017 Jan 1;31(1):72-83
pubmed: 28115468