Genomic determination of breeding systems and trans-specific evolution of HD MAT genes in suilloid fungi.

Rhizopogon Suillus balancing selection breeding system evolution fungi homeodomain protein mating self-incompatibility

Journal

Genetics
ISSN: 1943-2631
Titre abrégé: Genetics
Pays: United States
ID NLM: 0374636

Informations de publication

Date de publication:
26 05 2023
Historique:
received: 24 02 2023
accepted: 23 03 2023
pmc-release: 18 04 2024
medline: 29 5 2023
pubmed: 19 4 2023
entrez: 18 4 2023
Statut: ppublish

Résumé

Studying the signatures of evolution can help to understand genetic processes. Here, we demonstrate how the existence of balancing selection can be used to identify the breeding systems of fungi from genomic data. The breeding systems of fungi are controlled by self-incompatibility loci that determine mating types between potential mating partners, resulting in strong balancing selection at the loci. Within the fungal phylum Basidiomycota, two such self-incompatibility loci, namely HD MAT locus and P/R MAT locus, control mating types of gametes. Loss of function at one or both MAT loci results in different breeding systems and relaxes the MAT locus from balancing selection. By investigating the signatures of balancing selection at MAT loci, one can infer a species' breeding system without culture-based studies. Nevertheless, the extreme sequence divergence among MAT alleles imposes challenges for retrieving full variants from both alleles when using the conventional read-mapping method. Therefore, we employed a combination of read-mapping and local de novo assembly to construct haplotypes of HD MAT alleles from genomes in suilloid fungi (genera Suillus and Rhizopogon). Genealogy and pairwise divergence of HD MAT alleles showed that the origins of mating types predate the split between these two closely related genera. High sequence divergence, trans-specific polymorphism, and the deeply diverging genealogy confirm the long-term functionality and multiallelic status of HD MAT locus in suilloid fungi. This work highlights a genomics approach to studying breeding systems regardless of the culturability of organisms based on the interplay between evolution and genetics.

Identifiants

pubmed: 37070772
pii: 7127679
doi: 10.1093/genetics/iyad069
pmc: PMC10213496
pii:
doi:

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Déclaration de conflit d'intérêts

Conflicts of interest The author(s) declare no conflict of interest.

Références

BMC Bioinformatics. 2015 Mar 25;16:98
pubmed: 25887972
Genome Res. 2017 May;27(5):801-812
pubmed: 27940952
Mol Ecol. 2015 Jun;24(11):2747-58
pubmed: 25728665
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Bioinformatics. 2010 Mar 1;26(5):589-95
pubmed: 20080505
New Phytol. 2009 Jan;181(2):245-248
pubmed: 19121026
Cell. 1996 Apr 19;85(2):145-8
pubmed: 8612267
Plant Cell. 1995 Jun;7(6):773-83
pubmed: 12242384
Mycologia. 2013 Nov-Dec;105(6):1374-90
pubmed: 23928418
Heredity (Edinb). 2013 Dec;111(6):445-55
pubmed: 23838688
Genome Res. 2008 May;18(5):821-9
pubmed: 18349386
Bioinformatics. 2011 Nov 1;27(21):2987-93
pubmed: 21903627
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9172-7
pubmed: 10430915
Mycorrhiza. 2008 Apr;18(4):205-210
pubmed: 18320240
Theor Appl Genet. 1982 Mar;61(1):65-8
pubmed: 24271376
Mycologia. 2006 Mar-Apr;98(2):233-8
pubmed: 16894968
Methods Mol Biol. 2014;1079:155-70
pubmed: 24170401
Biol Rev Camb Philos Soc. 1949 Oct;24(4):411-47
pubmed: 24536314
Genome Biol. 2017 Dec 12;18(1):231
pubmed: 29233166
Bacteriol Rev. 1972 Jun;36(2):156-71
pubmed: 4557167
New Phytol. 2021 Apr;230(2):774-792
pubmed: 33355923
Microbiol Spectr. 2017 Jun;5(3):
pubmed: 28597825
Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1513-8
pubmed: 21187386
Nat Biotechnol. 2010 Sep;28(9):957-63
pubmed: 20622885
Genome Res. 2004 Jul;14(7):1394-403
pubmed: 15231754
Mol Biol Evol. 1999 Jul;16(7):975-86
pubmed: 10406114
Nat Genet. 2015 Apr;47(4):410-5
pubmed: 25706625
G3 (Bethesda). 2017 Jun 7;7(6):1775-1789
pubmed: 28450370
R Soc Open Sci. 2020 Feb 26;7(2):192126
pubmed: 32257356
Mol Biol Evol. 2013 Oct;30(10):2286-301
pubmed: 23864721
PLoS Genet. 2010 Aug 05;6(8):
pubmed: 20700437
Q Rev Biol. 1953 Sep;28(3):233-59
pubmed: 13100618
PLoS Genet. 2022 Mar 31;18(3):e1010097
pubmed: 35358178
Syst Biol. 2010 May;59(3):307-21
pubmed: 20525638

Auteurs

Yi-Hong Ke (YH)

Biology Department, Duke University, 130 Science Dr, Durham, NC 27708, USA.

Sara Branco (S)

Integrative Biology, University of Colorado, 1151 Arapahoe St, SI 2071, Denver, CO 80204, USA.

Anna L Bazzicalupo (AL)

Department of Zoology, University of British Columbia, 4200-6270 University Blvd, Vancouver, British Columbia, Canada, V6T 1Z4.

Nhu H Nguyen (NH)

Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, 3190 Maile Way, Honolulu, HI 96822, USA.

Hui-Ling Liao (HL)

North Florida Research and Education Center, University of Florida, 155 Research Rd, Quincy, FL 32351, USA.
Soil and Water Sciences Department, University of Florida, 1692 McCarty Dr, Room 2181, Building A, Gainesville, FL 32611, USA.

Peter Kennedy (P)

Department of Plant and Microbial Biology, University of Minnesota, 1475 Gortner Ave, Saint Paul, MN 55108, USA.

Thomas D Bruns (TD)

Department of Plant and Microbial Biology, University of California at Berkeley, 111 Koshland Hall, Berkeley, CA 94720, USA.

Alan Kuo (A)

Lawrence Berkeley National Laboratory, US Department of Energy Joint Genome Institute, 1 Cyclotron Road, Berkeley, CA 94720, USA.

Kurt LaButti (K)

Lawrence Berkeley National Laboratory, US Department of Energy Joint Genome Institute, 1 Cyclotron Road, Berkeley, CA 94720, USA.

Kerrie Barry (K)

Lawrence Berkeley National Laboratory, US Department of Energy Joint Genome Institute, 1 Cyclotron Road, Berkeley, CA 94720, USA.

Igor Grigoriev (I)

Department of Plant and Microbial Biology, University of California at Berkeley, 111 Koshland Hall, Berkeley, CA 94720, USA.
Lawrence Berkeley National Laboratory, US Department of Energy Joint Genome Institute, 1 Cyclotron Road, Berkeley, CA 94720, USA.

Rytas Vilgalys (R)

Biology Department, Duke University, 130 Science Dr, Durham, NC 27708, USA.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Populus Soil Microbiology Soil Microbiota Fungi
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins

Classifications MeSH