The hard clam genome reveals massive expansion and diversification of inhibitors of apoptosis in Bivalvia.
Divergence
Gene duplication
IAP gene family
Molecular evolution
Mollusca
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
25 01 2021
25 01 2021
Historique:
received:
14
07
2020
accepted:
17
12
2020
entrez:
25
1
2021
pubmed:
26
1
2021
medline:
1
10
2021
Statut:
epublish
Résumé
Inhibitors of apoptosis (IAPs) are critical regulators of programmed cell death that are essential for development, oncogenesis, and immune and stress responses. However, available knowledge regarding IAP is largely biased toward humans and model species, while the distribution, function, and evolutionary novelties of this gene family remain poorly understood in many taxa, including Mollusca, the second most speciose phylum of Metazoa. Here, we present a chromosome-level genome assembly of an economically significant bivalve, the hard clam Mercenaria mercenaria, which reveals an unexpected and dramatic expansion of the IAP gene family to 159 members, the largest IAP gene repertoire observed in any metazoan. Comparative genome analysis reveals that this massive expansion is characteristic of bivalves more generally. Reconstruction of the evolutionary history of molluscan IAP genes indicates that most originated in early metazoans and greatly expanded in Bivalvia through both lineage-specific tandem duplication and retroposition, with 37.1% of hard clam IAPs located on a single chromosome. The expanded IAPs have been subjected to frequent domain shuffling, which has in turn shaped their architectural diversity. Further, we observed that extant IAPs exhibit dynamic and orchestrated expression patterns among tissues and in response to different environmental stressors. Our results suggest that sophisticated regulation of apoptosis enabled by the massive expansion and diversification of IAPs has been crucial for the evolutionary success of hard clam and other molluscan lineages, allowing them to cope with local environmental stresses. This study broadens our understanding of IAP proteins and expression diversity and provides novel resources for studying molluscan biology and IAP function and evolution.
Sections du résumé
BACKGROUND
Inhibitors of apoptosis (IAPs) are critical regulators of programmed cell death that are essential for development, oncogenesis, and immune and stress responses. However, available knowledge regarding IAP is largely biased toward humans and model species, while the distribution, function, and evolutionary novelties of this gene family remain poorly understood in many taxa, including Mollusca, the second most speciose phylum of Metazoa.
RESULTS
Here, we present a chromosome-level genome assembly of an economically significant bivalve, the hard clam Mercenaria mercenaria, which reveals an unexpected and dramatic expansion of the IAP gene family to 159 members, the largest IAP gene repertoire observed in any metazoan. Comparative genome analysis reveals that this massive expansion is characteristic of bivalves more generally. Reconstruction of the evolutionary history of molluscan IAP genes indicates that most originated in early metazoans and greatly expanded in Bivalvia through both lineage-specific tandem duplication and retroposition, with 37.1% of hard clam IAPs located on a single chromosome. The expanded IAPs have been subjected to frequent domain shuffling, which has in turn shaped their architectural diversity. Further, we observed that extant IAPs exhibit dynamic and orchestrated expression patterns among tissues and in response to different environmental stressors.
CONCLUSIONS
Our results suggest that sophisticated regulation of apoptosis enabled by the massive expansion and diversification of IAPs has been crucial for the evolutionary success of hard clam and other molluscan lineages, allowing them to cope with local environmental stresses. This study broadens our understanding of IAP proteins and expression diversity and provides novel resources for studying molluscan biology and IAP function and evolution.
Identifiants
pubmed: 33487168
doi: 10.1186/s12915-020-00943-9
pii: 10.1186/s12915-020-00943-9
pmc: PMC7831173
doi:
Substances chimiques
Inhibitor of Apoptosis Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15Subventions
Organisme : National Key R&D Program of China
ID : 2019YFD0900800
Organisme : Modern Agro-industry Technology Research System
ID : CARS-49
Organisme : Major Applied Technology Innovation Project in Agriculture of Shandong Province
ID : SF1405303301
Références
Oncogene. 2014 Feb 6;33(6):671-6
pubmed: 23474760
BMC Plant Biol. 2014 Apr 11;14:93
pubmed: 24720629
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Plant J. 2007 Jun;50(5):873-85
pubmed: 17470057
J Mol Biol. 1992 Jul 5;226(1):141-57
pubmed: 1619647
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Cell. 1997 Feb 7;88(3):347-54
pubmed: 9039261
Bioconjug Chem. 2019 May 15;30(5):1395-1404
pubmed: 30888797
Nat Rev Cancer. 2010 Aug;10(8):561-74
pubmed: 20651737
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Mob DNA. 2015 Jun 02;6:11
pubmed: 26045719
Mol Biol Evol. 2017 May 1;34(5):1083-1099
pubmed: 28104746
Cell. 1994 Mar 11;76(5):777-9
pubmed: 8124715
Brief Bioinform. 2007 Nov;8(6):382-92
pubmed: 17932080
Genomics Proteomics Bioinformatics. 2010 Mar;8(1):77-80
pubmed: 20451164
Fish Shellfish Immunol. 2015 Sep;46(1):131-44
pubmed: 26004318
Dev Comp Immunol. 2015 Jul;51(1):74-8
pubmed: 25720977
Nucleic Acids Res. 2017 Jan 4;45(D1):D190-D199
pubmed: 27899635
Apoptosis. 2017 Jul;22(7):898-919
pubmed: 28424988
Fish Shellfish Immunol. 2012 Jan;32(1):69-78
pubmed: 22051180
Nature. 2012 Oct 4;490(7418):49-54
pubmed: 22992520
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Genomics. 2006 Dec;88(6):745-751
pubmed: 16857340
Genomics. 1997 Jun 15;42(3):514-8
pubmed: 9205126
Bioinformatics. 2014 May 1;30(9):1236-40
pubmed: 24451626
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Protoc. 2012 Mar 01;7(3):562-78
pubmed: 22383036
Bioinformatics. 2005 Jun;21 Suppl 1:i351-8
pubmed: 15961478
Genome Res. 2004 May;14(5):988-95
pubmed: 15123596
Apoptosis. 2007 Sep;12(9):1543-68
pubmed: 17573556
Genome Res. 2009 Feb;19(2):327-35
pubmed: 19029536
Nature. 1992 Apr 2;356(6368):397-400
pubmed: 1557121
PLoS One. 2010 Dec 30;5(12):e15633
pubmed: 21209894
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21087-92
pubmed: 21084634
Nucleic Acids Res. 1999 Jan 15;27(2):573-80
pubmed: 9862982
Curr Genomics. 2009 Aug;10(5):306-17
pubmed: 20119528
BMC Bioinformatics. 2018 Nov 29;19(1):460
pubmed: 30497373
Genome Biol. 2002;3(2):RESEARCH0008
pubmed: 11864370
Bioinformatics. 2007 May 1;23(9):1061-7
pubmed: 17332020
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Fish Shellfish Immunol. 2015 Sep;46(1):107-19
pubmed: 25989624
Nucleic Acids Res. 2004 Jan 1;32(Database issue):D115-9
pubmed: 14681372
Nucleic Acids Res. 2016 Jan 4;44(D1):D457-62
pubmed: 26476454
Genome Res. 2003 Sep;13(9):2178-89
pubmed: 12952885
Nat Commun. 2017 Nov 23;8(1):1721
pubmed: 29167427
Mol Ecol Resour. 2019 Nov;19(6):1647-1658
pubmed: 31483923
Biochim Biophys Acta. 2011 Jan;1813(1):238-59
pubmed: 20969895
Methods Mol Biol. 2014;1079:131-46
pubmed: 24170399
Trends Cell Biol. 1999 Aug;9(8):323-8
pubmed: 10407412
Med Hypotheses. 1985 Dec;18(4):399-404
pubmed: 3854167
Cell Death Differ. 2002 Apr;9(4):367-93
pubmed: 11965491
Comput Appl Biosci. 1997 Oct;13(5):555-6
pubmed: 9367129
EMBO J. 2005 Feb 9;24(3):645-55
pubmed: 15650747
Oncogene. 1998 Dec 24;17(25):3247-59
pubmed: 9916987
Cell. 1995 Dec 29;83(7):1243-52
pubmed: 8548810
Mol Cell. 2003 Feb;11(2):519-27
pubmed: 12620238
J Exp Zool B Mol Dev Evol. 2007 Jan 15;308(1):58-73
pubmed: 16838295
Nature. 2000 Oct 12;407(6805):796-801
pubmed: 11048731
Genome Res. 2014 Dec;24(12):2041-9
pubmed: 25327137
Gigascience. 2017 Aug 1;6(8):1-12
pubmed: 28873964
Cell. 2001 Mar 9;104(5):791-800
pubmed: 11257232
Stat Appl Genet Mol Biol. 2005;4:Article17
pubmed: 16646834
Science. 1966 Nov 4;154(3749):604-12
pubmed: 5332319
J Mol Biol. 1997 Apr 25;268(1):78-94
pubmed: 9149143
Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15682-7
pubmed: 14671323
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W465-7
pubmed: 15980513
Comp Biochem Physiol A Comp Physiol. 1974 Feb 1;47(2):447-60
pubmed: 4156206
Arch Environ Contam Toxicol. 2014 Apr;66(3):450-62
pubmed: 24531857
Bioinformatics. 2006 Nov 1;22(21):2688-90
pubmed: 16928733
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Genome Biol. 2013 Apr 25;14(4):R36
pubmed: 23618408
Nat Ecol Evol. 2017 Apr 03;1(5):121
pubmed: 28812709
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
Bioinformatics. 2006 May 15;22(10):1269-71
pubmed: 16543274
iScience. 2019 Sep 27;19:1225-1237
pubmed: 31574780
Bioinformatics. 2011 Mar 15;27(6):764-70
pubmed: 21217122
Curr Biol. 2016 Jul 11;26(13):R620-R627
pubmed: 27404257
J Clin Oncol. 2008 Jan 20;26(3):493-500
pubmed: 18202424
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8
pubmed: 17485477
Genome Biol. 2008 Jan 11;9(1):R7
pubmed: 18190707
Comp Biochem Physiol Part D Genomics Proteomics. 2016 Mar;17:48-57
pubmed: 26845471
J Biol Chem. 2006 Feb 10;281(6):3254-60
pubmed: 16339151
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Nat Methods. 2013 Jun;10(6):563-9
pubmed: 23644548
Discov Med. 2011 Mar;11(58):221-31
pubmed: 21447281
BMC Genomics. 2019 Dec 5;20(1):937
pubmed: 31805848
EMBO Rep. 2006 Oct;7(10):988-94
pubmed: 17016456
Sci Rep. 2015 Mar 03;5:8693
pubmed: 25732911
Mol Biol Evol. 2018 Jul 1;35(7):1638-1652
pubmed: 29672732
Genome Biol. 2001;2(7):REVIEWS3009
pubmed: 11516343
Bioinformatics. 2004 Nov 1;20(16):2878-9
pubmed: 15145805
Biol Rev Camb Philos Soc. 1951 Feb;26(1):59-86
pubmed: 24540363
Gigascience. 2020 Jan 1;9(1):
pubmed: 31942620
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
DNA Res. 2018 Dec 1;25(6):655-665
pubmed: 30295708
BMC Bioinformatics. 2004 May 14;5:59
pubmed: 15144565