Evolutionary Plasticity of Mating-Type Determination Mechanisms in Paramecium aurelia Sibling Species.
ciliates
evolutionary genomics
programmed genome rearrangements
self-incompatibility systems
Journal
Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707
Informations de publication
Date de publication:
03 02 2021
03 02 2021
Historique:
accepted:
09
12
2020
pubmed:
15
12
2020
medline:
24
12
2021
entrez:
14
12
2020
Statut:
ppublish
Résumé
The Paramecium aurelia complex, a group of morphologically similar but sexually incompatible sibling species, is a unique example of the evolutionary plasticity of mating-type systems. Each species has two mating types, O (Odd) and E (Even). Although O and E types are homologous in all species, three different modes of determination and inheritance have been described: genetic determination by Mendelian alleles, stochastic developmental determination, and maternally inherited developmental determination. Previous work in three species of the latter kind has revealed the key roles of the E-specific transmembrane protein mtA and its highly specific transcription factor mtB: type O clones are produced by maternally inherited genome rearrangements that inactivate either mtA or mtB during development. Here we show, through transcriptome analyses in five additional species representing the three determination systems, that mtA expression specifies type E in all cases. We further show that the Mendelian system depends on functional and nonfunctional mtA alleles, and identify novel developmental rearrangements in mtA and mtB which now explain all cases of maternally inherited mating-type determination. Epistasis between these genes likely evolved from less specific interactions between paralogs in the P. aurelia common ancestor, after a whole-genome duplication, but the mtB gene was subsequently lost in three P. aurelia species which appear to have returned to an ancestral regulation mechanism. These results suggest a model accounting for evolutionary transitions between determination systems, and highlight the diversity of molecular solutions explored among sibling species to maintain an essential mating-type polymorphism in cell populations.
Identifiants
pubmed: 33313646
pii: 6031912
doi: 10.1093/gbe/evaa258
pmc: PMC7900874
pii:
doi:
Substances chimiques
Membrane Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
PLoS Genet. 2014 Sep 25;10(9):e1004665
pubmed: 25254958
Genetics. 1963 Jun;48(6):815-34
pubmed: 17248172
Nat Biotechnol. 2010 May;28(5):511-5
pubmed: 20436464
PLoS Biol. 2013;11(3):e1001518
pubmed: 23555191
Genetics. 1977 Dec;87(4):633-53
pubmed: 17248783
Nucleic Acids Res. 2014 Aug;42(14):8970-83
pubmed: 25016527
Philos Trans R Soc Lond B Biol Sci. 2016 Oct 19;371(1706):
pubmed: 27619695
Evolution. 2012 Apr;66(4):947-56
pubmed: 22486681
Genetics. 2014 Aug;197(4):1417-28
pubmed: 24840360
Nat Commun. 2019 Jun 20;10(1):2710
pubmed: 31221974
Annu Rev Genet. 1977;11:349-67
pubmed: 413472
PLoS Genet. 2014 Aug 28;10(8):e1004552
pubmed: 25166013
PLoS Genet. 2020 Apr 16;16(4):e1008723
pubmed: 32298257
Bioinformatics. 2018 Nov 15;34(22):3929-3930
pubmed: 29868763
Cold Spring Harb Perspect Biol. 2013 Dec 01;5(12):a017764
pubmed: 24296171
Fungal Biol Rev. 2015 Dec 1;29(3-4):108-117
pubmed: 26834823
Curr Biol. 2020 May 18;30(10):R502-R510
pubmed: 32428490
Annu Rev Microbiol. 2017 Sep 8;71:133-156
pubmed: 28715961
Trends Genet. 2009 Aug;25(8):344-50
pubmed: 19596481
Nature. 2006 Nov 9;444(7116):171-8
pubmed: 17086204
Biol Cell. 2012 Jun;104(6):309-25
pubmed: 22352444
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W465-9
pubmed: 18424797
Cold Spring Harb Protoc. 2010 Jan;2010(1):pdb.prot5361
pubmed: 20150120
Mol Phylogenet Evol. 2014 Feb;71:142-8
pubmed: 24315865
Nature. 2014 May 22;509(7501):447-52
pubmed: 24805235
Mol Biol Evol. 2017 May 1;34(5):1194-1216
pubmed: 28204679
BMC Genomics. 2017 Jun 26;18(1):483
pubmed: 28651633
Protist. 2015 Sep;166(4):438-56
pubmed: 26277215
Genetics. 1973 May;74(1):63-80
pubmed: 17248611
Cold Spring Harb Protoc. 2010 Jan;2010(1):pdb.prot5364
pubmed: 20150123
Adv Genet. 1947;1:263-358
pubmed: 20259287
Annu Rev Microbiol. 2019 Sep 8;73:267-291
pubmed: 31150584
Cold Spring Harb Protoc. 2010 Jan;2010(1):pdb.prot5362
pubmed: 20150121
Biol Rev Camb Philos Soc. 2011 May;86(2):421-42
pubmed: 21489122
Protein Sci. 2018 Jan;27(1):135-145
pubmed: 28884485
BMC Bioinformatics. 2011 Apr 22;12:116
pubmed: 21513511
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Int J Evol Biol. 2012;2012:436196
pubmed: 22888464
Cell Mol Life Sci. 2020 Nov;77(22):4615-4629
pubmed: 32462406
Genetics. 1955 May;40(3):321-30
pubmed: 17247555
Nat Methods. 2015 Jan;12(1):59-60
pubmed: 25402007
Mol Cell Biol. 2004 Sep;24(17):7370-9
pubmed: 15314149
Genes Dev. 2009 Nov 1;23(21):2478-83
pubmed: 19884254
Brief Bioinform. 2019 Jul 19;20(4):1160-1166
pubmed: 28968734
Genome Biol. 2013 Apr 25;14(4):R36
pubmed: 23618408
J Cell Sci. 1978 Aug;32:55-66
pubmed: 701405
PLoS Genet. 2012;8(10):e1002984
pubmed: 23071448
Microbiol Spectr. 2014 Dec;2(6):
pubmed: 26104450
Genome Res. 2014 Oct;24(10):1665-75
pubmed: 25085612
Genetics. 1980 Apr;94(4):951-9
pubmed: 17249026
Adv Genet. 2002;46:305-37
pubmed: 11931229