A Co-Expression Network in Hexaploid Wheat Reveals Mostly Balanced Expression and Lack of Significant Gene Loss of Homeologous Meiotic Genes Upon Polyploidization.
co-expression
hexaploid
meiosis
network
polyploidization
wheat
Journal
Frontiers in plant science
ISSN: 1664-462X
Titre abrégé: Front Plant Sci
Pays: Switzerland
ID NLM: 101568200
Informations de publication
Date de publication:
2019
2019
Historique:
received:
25
07
2019
accepted:
24
09
2019
entrez:
5
11
2019
pubmed:
5
11
2019
medline:
5
11
2019
Statut:
epublish
Résumé
Polyploidization has played an important role in plant evolution. However, upon polyploidization, the process of meiosis must adapt to ensure the proper segregation of increased numbers of chromosomes to produce balanced gametes. It has been suggested that meiotic gene (MG) duplicates return to a single copy following whole genome duplication to stabilize the polyploid genome. Therefore, upon the polyploidization of wheat, a hexaploid species with three related (homeologous) genomes, the stabilization process may have involved rapid changes in content and expression of MGs on homeologous chromosomes (homeologs). To examine this hypothesis, sets of candidate MGs were identified in wheat using co-expression network analysis and orthology informed approaches. In total, 130 RNA-Seq samples from a range of tissues including wheat meiotic anthers were used to define co-expressed modules of genes. Three modules were significantly correlated with meiotic tissue samples but not with other tissue types. These modules were enriched for GO terms related to cell cycle, DNA replication, and chromatin modification and contained orthologs of known MGs. Overall, 74.4% of genes within these meiosis-related modules had three homeologous copies which was similar to other tissue-related modules. Amongst wheat MGs identified by orthology, rather than co-expression, the majority (93.7%) were either retained in hexaploid wheat at the same number of copies (78.4%) or increased in copy number (15.3%) compared to ancestral wheat species. Furthermore, genes within meiosis-related modules showed more balanced expression levels between homeologs than genes in non-meiosis-related modules. Taken together, our results do not support extensive gene loss nor changes in homeolog expression of MGs upon wheat polyploidization. The construction of the MG co-expression network allowed identification of hub genes and provided key targets for future studies.
Identifiants
pubmed: 31681395
doi: 10.3389/fpls.2019.01325
pmc: PMC6813927
doi:
Types de publication
Journal Article
Langues
eng
Pagination
1325Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/J007188/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/J/00000128
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/J/000PR9788
Pays : United Kingdom
Informations de copyright
Copyright © 2019 Alabdullah, Borrill, Martin, Ramirez-Gonzalez, Hassani-Pak, Uauy, Shaw and Moore.
Références
Front Plant Sci. 2018 Dec 04;9:1791
pubmed: 30564262
Science. 1998 Jul 10;281(5374):272-4
pubmed: 9657725
Cell. 1994 Aug 12;78(3):487-98
pubmed: 7520368
Development. 2011 Aug;138(15):3319-30
pubmed: 21750041
Plant Cell. 2017 Aug;29(8):1806-1821
pubmed: 28808136
Ann Bot. 2017 Aug 1;120(2):183-194
pubmed: 28854567
Cytogenet Genome Res. 2016;150(1):1-16
pubmed: 27926907
Reproduction. 2016 Nov;152(5):431-7
pubmed: 27492080
Mol Cells. 2017 Nov 30;40(11):814-822
pubmed: 29179262
PLoS One. 2007 Apr 18;2(4):e383
pubmed: 17440619
Mol Cell Biol. 2017 Jan 19;37(3):
pubmed: 27821479
Epigenetics Chromatin. 2016 Jun 21;9:24
pubmed: 27330565
J Cell Sci. 2005 Jul 15;118(Pt 14):3037-48
pubmed: 15972315
J Biol Chem. 2002 Oct 11;277(41):38781-90
pubmed: 12149245
J Cell Sci. 2003 Jan 15;116(Pt 2):259-71
pubmed: 12482912
Curr Opin Plant Biol. 2016 Apr;30:82-7
pubmed: 26939088
Nat Cell Biol. 2004 Sep;6(9):906-8
pubmed: 15340450
Plant Cell. 2011 Feb;23(2):443-58
pubmed: 21325139
Plant J. 2009 Feb;57(3):487-97
pubmed: 18826431
Front Plant Sci. 2019 Oct 18;10:1325
pubmed: 31681395
Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):20121-6
pubmed: 19918061
Sci Rep. 2016 Dec 16;6:38956
pubmed: 27982071
Mol Reprod Dev. 2004 Oct;69(2):222-7
pubmed: 15293224
Cold Spring Harb Perspect Biol. 2015 May 18;7(6):
pubmed: 25986558
Reproduction. 2017 Sep;154(3):R65-R79
pubmed: 28696245
Annu Rev Plant Biol. 2015;66:297-327
pubmed: 25494464
Cytogenet Genome Res. 2008;120(3-4):281-90
pubmed: 18504357
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Mol Biol Evol. 2014 Jul;31(7):1724-7
pubmed: 24694832
Nature. 2001 May 10;411(6834):204-7
pubmed: 11346798
Science. 2014 Jul 18;345(6194):1249721
pubmed: 25035497
J Genet Genomics. 2014 Mar 20;41(3):125-37
pubmed: 24656233
Genome Res. 2009 Feb;19(2):327-35
pubmed: 19029536
Nucleic Acids Res. 2006;34(16):4438-48
pubmed: 16945961
Nature. 2000 Jul 6;406(6791):90-4
pubmed: 10894548
Mol Cell Biol. 1995 Dec;15(12):6572-81
pubmed: 8524222
Int J Biochem Cell Biol. 2016 Apr;73:99-110
pubmed: 26860958
Front Plant Sci. 2017 Sep 20;8:1640
pubmed: 28979289
BMC Genomics. 2012 Sep 19;13:492
pubmed: 22989011
Plant Cell. 2013 Oct;25(10):3885-99
pubmed: 24122830
Cell Rep. 2015 Dec 1;13(9):1772-80
pubmed: 26628362
Nature. 2013 Apr 4;496(7443):87-90
pubmed: 23535596
Cell Cycle. 2006 Apr;5(7):766-74
pubmed: 16582639
Chromosoma. 2000;109(1-2):62-71
pubmed: 10855496
Genome Biol. 2010;11(2):R14
pubmed: 20132535
Cytogenet Genome Res. 2013;140(2-4):185-203
pubmed: 23796636
DNA Res. 1994;1(1):15-26
pubmed: 7584025
PLoS One. 2018 Feb 9;13(2):e0192613
pubmed: 29425247
BMC Mol Biol. 2007 Aug 04;8:65
pubmed: 17683575
Genes Dev. 1999 Mar 15;13(6):666-74
pubmed: 10090723
Plant Cell Environ. 2009 Dec;32(12):1633-51
pubmed: 19712066
Nat Rev Genet. 2005 Nov;6(11):836-46
pubmed: 16304599
Mol Biol Cell. 2004 Mar;15(3):1224-32
pubmed: 14668482
PLoS Genet. 2007 May 25;3(5):e83
pubmed: 17530928
Cell Cycle. 2018;17(5):634-642
pubmed: 29417875
Science. 2014 Jul 18;345(6194):1250092
pubmed: 25035499
Mol Cell Biol. 2003 Dec;23(24):9104-16
pubmed: 14645522
Plant J. 1997 Jan;11(1):1-14
pubmed: 9025299
Planta. 2013 Jul;238(1):23-33
pubmed: 23624938
J Cell Sci. 2002 Sep 15;115(Pt 18):3645-55
pubmed: 12186950
Nature. 1997 Mar 13;386(6621):187-90
pubmed: 9062192
G3 (Bethesda). 2013 Nov 06;3(11):1927-43
pubmed: 24062528
Genome Biol. 2008;9(12):R181
pubmed: 19099579
Front Cell Dev Biol. 2016 Jun 21;4:58
pubmed: 27446912
Plant Cell Physiol. 2013 Feb;54(2):e6
pubmed: 23299411
Genome Biol. 2019 Apr 15;20(1):69
pubmed: 30982471
Plant Physiol. 2006 Apr;140(4):1355-66
pubmed: 16514015
New Phytol. 2011 Nov;192(3):577-89
pubmed: 21781122
PLoS One. 2011;6(10):e26162
pubmed: 22046259
J Genet Genomics. 2014 Mar 20;41(3):139-52
pubmed: 24656234
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6075-80
pubmed: 18417451
Mol Cell Biol. 1998 Apr;18(4):2118-29
pubmed: 9528784
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Plant Physiol. 2016 Apr;170(4):2172-86
pubmed: 26869702
Plant J. 2003 Oct;36(1):21-9
pubmed: 12974808
Theor Appl Genet. 2019 Mar;132(3):575-592
pubmed: 30483818
J Cell Sci. 2012 Jun 1;125(Pt 11):2581-91
pubmed: 22393242
Proc Natl Acad Sci U S A. 2017 Feb 7;114(6):E913-E921
pubmed: 28096351
Plant Signal Behav. 2010 Nov;5(11):1476-9
pubmed: 21057207
J Stat Softw. 2012 Mar;46(11):
pubmed: 23050260
Funct Plant Biol. 2008 Dec;35(12):1267-1277
pubmed: 32688873
Annu Rev Plant Biol. 2009;60:433-53
pubmed: 19575588
Cell. 2004 Aug 20;118(4):404-6
pubmed: 15315752
Rice (N Y). 2013 Feb 06;6(1):4
pubmed: 24280374
Genetics. 2000 Apr;154(4):1533-48
pubmed: 10747051
New Phytol. 2015 Dec;208(4):1067-77
pubmed: 26213803
Mol Biol Cell. 2006 Mar;17(3):1331-43
pubmed: 16394097
Chromosoma. 1997 Oct;106(5):327-33
pubmed: 9297511
Science. 2017 Jul 7;357(6346):93-97
pubmed: 28684525
Plant Cell. 2017 Sep;29(9):2150-2167
pubmed: 28814644
Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10836-41
pubmed: 12960374
Plant J. 2008 Apr;54(1):152-62
pubmed: 18182028
J Biol Chem. 2015 Apr 24;290(17):10751-63
pubmed: 25762720
Planta. 2019 May;249(5):1487-1501
pubmed: 30701323
BMC Plant Biol. 2007 Dec 20;7:67
pubmed: 18096080
Mol Cell Biol. 2003 Jul;23(14):4814-25
pubmed: 12832469
Science. 2018 Aug 17;361(6403):
pubmed: 30115783
Science. 1996 Mar 15;271(5255):1595-7
pubmed: 8599118
Planta. 2015 Aug;242(2):435-49
pubmed: 25809152
Trends Plant Sci. 2008 Dec;13(12):640-6
pubmed: 18948054
Front Genet. 2018 Nov 27;9:574
pubmed: 30542370
Nature. 2011 May 5;473(7345):97-100
pubmed: 21478875
BMC Res Notes. 2010 Sep 29;3:245
pubmed: 20920212
Plant Physiol. 2016 Apr;170(4):2218-31
pubmed: 26888061
Chromosoma. 2017 Dec;126(6):669-680
pubmed: 28365783
Stat Appl Genet Mol Biol. 2005;4:Article17
pubmed: 16646834
Mol Breed. 2017;37(8):95
pubmed: 28781573
Nature. 2017 Nov 23;551(7681):498-502
pubmed: 29143815
Nat Plants. 2018 Dec;4(12):1010-1016
pubmed: 30478361
Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167-74
pubmed: 8710842
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
Nat Commun. 2019 May 29;10(1):2354
pubmed: 31142748
Development. 2003 Dec;130(24):5975-87
pubmed: 14573517
Proc Natl Acad Sci U S A. 2018 Mar 6;115(10):2431-2436
pubmed: 29183972
BMC Evol Biol. 2011 Mar 24;11:78
pubmed: 21435253
Front Plant Sci. 2018 Apr 20;9:509
pubmed: 29731763
BMC Plant Biol. 2017 Nov 7;17(1):194
pubmed: 29115926
J Cell Sci. 2006 Jun 15;119(Pt 12):2486-96
pubmed: 16763194
Nucleic Acids Res. 2016 Nov 16;44(20):9681-9697
pubmed: 27431324
PLoS One. 2018 Aug 7;13(8):e0201861
pubmed: 30086160
DNA Repair (Amst). 2006 Apr 8;5(4):455-64
pubmed: 16442857
Genes Dev. 2018 Feb 1;32(3-4):283-296
pubmed: 29440262
Mol Cell Biol. 2003 Feb;23(4):1441-52
pubmed: 12556502
Genetics. 2008 Dec;180(4):1809-19
pubmed: 18832348
J Cell Biol. 2000 Jan 24;148(2):233-8
pubmed: 10648555
Mol Gen Genet. 1993 Feb;237(1-2):225-32
pubmed: 8455558
Int J Plant Genomics. 2012;2012:514398
pubmed: 22518114
Mol Gen Genet. 1994 Apr;243(1):17-23
pubmed: 8190067
Nature. 2006 Mar 16;440(7082):341-5
pubmed: 16541074
Appl Transl Genom. 2016 Nov 02;11:18-26
pubmed: 28018846
Chromosome Res. 2006;14(3):319-32
pubmed: 16628502
Front Plant Sci. 2011 Jun 20;2:19
pubmed: 22629260
Genetics. 2017 Feb;205(2):657-671
pubmed: 27913618
J Genet Genomics. 2014 Mar 20;41(3):165-75
pubmed: 24656236
Science. 2018 Aug 17;361(6403):
pubmed: 30115782
Science. 2004 Jan 2;303(5654):89-92
pubmed: 14704428