Rethinking asexuality: the enigmatic case of functional sexual genes in Lepraria (Stereocaulaceae).
Asexual
Comparative genomics
Lichenized fungi
Mating
Meiosis
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
26 Oct 2024
26 Oct 2024
Historique:
received:
10
06
2024
accepted:
14
10
2024
medline:
26
10
2024
pubmed:
26
10
2024
entrez:
25
10
2024
Statut:
epublish
Résumé
The ubiquity of sex across eukaryotes, given its high costs, strongly suggests it is evolutionarily advantageous. Asexual lineages can avoid, for example, the risks and energetic costs of recombination, but suffer short-term reductions in adaptive potential and long-term damage to genome integrity. Despite these costs, lichenized fungi have frequently evolved asexual reproduction, likely because it allows the retention of symbiotic algae across generations. The lichenized fungal genus Lepraria is thought to be exclusively asexual, while its sister genus Stereocaulon completes a sexual reproductive cycle. A comparison of sister sexual and asexual clades should shed light on the evolution of asexuality in lichens in general, as well as the apparent long-term maintenance of asexuality in Lepraria, specifically. In this study, we assembled and annotated representative long-read genomes from the putatively asexual Lepraria genus and its sexual sister genus Stereocaulon, and added short-read assemblies from an additional 22 individuals across both genera. Comparative genomic analyses revealed that both genera were heterothallic, with intact mating-type loci of both idiomorphs present across each genus. Additionally, we identified and assessed 29 genes involved in meiosis and mitosis and 45 genes that contribute to formation of fungal sexual reproductive structures (ascomata). All genes were present and appeared functional in nearly all Lepraria, and we failed to identify a general pattern of relaxation of selection on these genes across the Lepraria lineage. Together, these results suggest that Lepraria may be capable of sexual reproduction, including mate recognition, meiosis, and production of ascomata. Despite apparent maintenance of machinery essential for fungal sex, over 200 years of careful observations by lichenologists have produced no evidence of canonical sexual reproduction in Lepraria. We suggest that Lepraria may have instead evolved a form of parasexual reproduction, perhaps by repurposing MAT and meiosis-specific genes. This may, in turn, allow these lichenized fungi to avoid long-term consequences of asexuality, while maintaining the benefit of an unbroken bond with their algal symbionts.
Sections du résumé
BACKGROUND
BACKGROUND
The ubiquity of sex across eukaryotes, given its high costs, strongly suggests it is evolutionarily advantageous. Asexual lineages can avoid, for example, the risks and energetic costs of recombination, but suffer short-term reductions in adaptive potential and long-term damage to genome integrity. Despite these costs, lichenized fungi have frequently evolved asexual reproduction, likely because it allows the retention of symbiotic algae across generations. The lichenized fungal genus Lepraria is thought to be exclusively asexual, while its sister genus Stereocaulon completes a sexual reproductive cycle. A comparison of sister sexual and asexual clades should shed light on the evolution of asexuality in lichens in general, as well as the apparent long-term maintenance of asexuality in Lepraria, specifically.
RESULTS
RESULTS
In this study, we assembled and annotated representative long-read genomes from the putatively asexual Lepraria genus and its sexual sister genus Stereocaulon, and added short-read assemblies from an additional 22 individuals across both genera. Comparative genomic analyses revealed that both genera were heterothallic, with intact mating-type loci of both idiomorphs present across each genus. Additionally, we identified and assessed 29 genes involved in meiosis and mitosis and 45 genes that contribute to formation of fungal sexual reproductive structures (ascomata). All genes were present and appeared functional in nearly all Lepraria, and we failed to identify a general pattern of relaxation of selection on these genes across the Lepraria lineage. Together, these results suggest that Lepraria may be capable of sexual reproduction, including mate recognition, meiosis, and production of ascomata.
CONCLUSIONS
CONCLUSIONS
Despite apparent maintenance of machinery essential for fungal sex, over 200 years of careful observations by lichenologists have produced no evidence of canonical sexual reproduction in Lepraria. We suggest that Lepraria may have instead evolved a form of parasexual reproduction, perhaps by repurposing MAT and meiosis-specific genes. This may, in turn, allow these lichenized fungi to avoid long-term consequences of asexuality, while maintaining the benefit of an unbroken bond with their algal symbionts.
Identifiants
pubmed: 39455957
doi: 10.1186/s12864-024-10898-8
pii: 10.1186/s12864-024-10898-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1003Subventions
Organisme : Spanish Ministry of Science
ID : CTM2015-64728-C2-1-R
Informations de copyright
© 2024. The Author(s).
Références
Weismann A. Essays upon Heredity and Kindred Biological problems. Clarendon; 1891.
Muller HJ. Some genetic aspects of sex. Am Nat. 1932;66:118–38.
doi: 10.1086/280418
Maynard Smith J. What use is sex? J Theor Biol. 1971;30:319–35.
doi: 10.1016/0022-5193(71)90058-0
Birky CW, Walsh JB. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci. 1988;85:6414–8.
pubmed: 3413105
pmcid: 281982
doi: 10.1073/pnas.85.17.6414
Hörandl E, Bast J, Brandt A, Scheu S, Bleidorn C, Cordellier M, et al. Genome evolution of Asexual organisms and the Paradox of sex in eukaryotes. In: Pontarotti P, editor. Evolutionary Biology—A Transdisciplinary Approach. Cham: Springer International Publishing; 2020. pp. 133–67.
doi: 10.1007/978-3-030-57246-4_7
Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974;78:737–56.
pubmed: 4448362
pmcid: 1213231
doi: 10.1093/genetics/78.2.737
Siderakis M, Tarsounas M. Telomere regulation and function during meiosis. Chromosome Res. 2007;15:667–79.
pubmed: 17674153
pmcid: 2459255
doi: 10.1007/s10577-007-1149-7
Speijer D. What can we infer about the origin of sex in early eukaryotes? Philosophical Trans Royal Soc B: Biol Sci. 2016;371:20150530.
doi: 10.1098/rstb.2015.0530
Hörandl E, Speijer D. How oxygen gave rise to eukaryotic sex. Proc Royal Soc B: Biol Sci. 2018;285:20172706.
doi: 10.1098/rspb.2017.2706
Shiu PKT, Raju NB, Zickler D, Metzenberg RL. Meiotic silencing by unpaired DNA. Cell. 2001;107:905–16.
pubmed: 11779466
doi: 10.1016/S0092-8674(01)00609-2
Halary S, Malik S-B, Lildhar L, Slamovits CH, Hijri M, Corradi N. Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biol Evol. 2011;3:950–8.
pubmed: 21876220
pmcid: 3184777
doi: 10.1093/gbe/evr089
Brandt A, Schaefer I, Glanz J, Schwander T, Maraun M, Scheu S, et al. Effective purifying selection in ancient asexual oribatid mites. Nat Commun. 2017;8:873.
pubmed: 29026136
pmcid: 5638860
doi: 10.1038/s41467-017-01002-8
Hofstatter PG, Lahr DJG. All eukaryotes are sexual, unless proven otherwise. BioEssays. 2019;41:1800246.
doi: 10.1002/bies.201800246
Vakhrusheva OA, Mnatsakanova EA, Galimov YR, Neretina TV, Gerasimov ES, Naumenko SA, et al. Genomic signatures of recombination in a natural population of the bdelloid rotifer Adineta vaga. Nat Commun. 2020;11:6421.
pubmed: 33339818
pmcid: 7749112
doi: 10.1038/s41467-020-19614-y
Schurko AM, Logsdon JM Jr. Using a meiosis detection toolkit to investigate ancient asexual scandals and the evolution of sex. BioEssays. 2008;30:579–89.
pubmed: 18478537
doi: 10.1002/bies.20764
Steins L, Guerreiro MA, Duhamel M, Liu F, Wang Q-M, Boekhout T, et al. Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales). BMC Genomics. 2023;24:321.
pubmed: 37312063
pmcid: 10262431
doi: 10.1186/s12864-023-09387-1
Milgroom MG, Jiménez-Gasco M, del García M, Drott CO, Jiménez-Díaz MT. Recombination between clonal lineages of the asexual fungus verticillium dahliae detected by genotyping by sequencing. PLoS ONE. 2014;9:e106740.
pubmed: 25181515
pmcid: 4152335
doi: 10.1371/journal.pone.0106740
Tripp EA, Lendemer JC. Twenty-seven modes of reproduction in the obligate lichen symbiosis. Brittonia. 2018;70:1–14.
doi: 10.1007/s12228-017-9500-6
Metzenberg RL, Glass NL. Mating type and mating strategies in Neurospora. BioEssays. 1990;12:53–9.
pubmed: 2140508
doi: 10.1002/bies.950120202
Coppin E, Debuchy R, Arnaise S, Picard M. Mating types and sexual development in filamentous ascomycetes. Microbiol Mol Biol Rev. 1997;61:411–28.
pubmed: 9409146
pmcid: 232618
Murtagh GJ, Dyer PS, Crittenden PD. Sex and the single lichen. Nature. 2000;404:564–564.
pubmed: 10766229
doi: 10.1038/35007142
Pizarro D, Dal Grande F, Leavitt SD, Dyer PS, Schmitt I, Crespo A, et al. Whole-genome sequence data uncover widespread heterothallism in the largest group of lichen-forming fungi. Genome Biol Evol. 2019;11:721–30.
pubmed: 30715356
pmcid: 6414310
doi: 10.1093/gbe/evz027
White KH, Keepers K, Kane N, Lendemer JC. Discovery of new genomic configuration of mating-type loci in the largest lineage of lichen-forming fungi. Genome Biol Evol. 2024;16:evae094.
pubmed: 38686438
pmcid: 11126327
doi: 10.1093/gbe/evae094
Büdel B, Scheidegger C. Thallus morphology and anatomy. In: Lichen Biology. 3rd edition. Cambridge University Press; 2008. pp. 40–68.
Ekman S, Tønsberg T. Most species of Lepraria and Leproloma form a monophyletic group closely related to Stereocaulon. Mycol Res. 2002;106:1262–76.
doi: 10.1017/S0953756202006718
Büdel B, Friedl T, Beyschlag W, editors. Biology of Algae, Lichens and Bryophytes. Berlin, Heidelberg: Springer Berlin Heidelberg; 2024.
Lendemer JC, Hodkinson BP. A radical shift in the taxonomy of Lepraria s.l.: molecular and morphological studies shed new light on the evolution of asexuality and lichen growth form diversification. Mycologia. 2013;105:994–1018.
pubmed: 23709574
doi: 10.3852/12-338
Fehrer J, Slavíková-Bayerová Š, Orange A. Large genetic divergence of new, morphologically similar species of sterile lichens from Europe (Lepraria, Stereocaulaceae, Ascomycota): concordance of DNA sequence data with secondary metabolites. Cladistics. 2008;24:443–58.
pubmed: 34879629
doi: 10.1111/j.1096-0031.2008.00216.x
Barcenas-Peña A, Diaz R, Grewe F, Widhelm T, Lumbsch HT. Contributions to the phylogeny of Lepraria (Stereocaulaceae) species from the Southern Hemisphere, including three new species. Bryologist. 2021;124:494–505.
doi: 10.1639/0007-2745-124.4.494
Kraichak E, Huang J-P, Nelsen M, Leavitt SD, Lumbsch HT. A revised classification of orders and families in the two major subclasses of Lecanoromycetes (Ascomycota) based on a temporal approach. Bot J Linn Soc. 2018;188:233–49.
Högnabba F. Molecular phylogeny of the genus Stereocaulon. Mycol Res. 2006;110:1080–92. Stereocaulaceae, lichenized ascomycetes.
pubmed: 16934965
doi: 10.1016/j.mycres.2006.04.013
Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290:1151–5.
pubmed: 11073452
doi: 10.1126/science.290.5494.1151
Normark BB, Judson OP, Moran NA. Genomic signatures of ancient asexual lineages. Biol J Linn Soc. 2003;79:69–84.
doi: 10.1046/j.1095-8312.2003.00182.x
Pfeffer B, Lymbery C, Booth B, Allen JL. Chromosomal genome sequence assembly and mating-type (MAT) locus characterization of the leprose asexual lichenized fungus Lepraria neglecta. (Nyl) Erichsen Lichenologist. 2023;55:41–50.
doi: 10.1017/S002428292200041X
Arup U, Ekman S, Lindblom L, Mattsson J-E. High performance thin layer chromatography (HPTLC), an improved technique for screening lichen substances. Lichenologist. 1993;25:61–71.
doi: 10.1006/lich.1993.1018
Culberson CF, Johnson A. Substitution of methyl tert.-butyl ether for diethyl ether in the standardized thin-layer chromatographic method for lichen products. J Chromatogr A. 1982;238:483–7.
doi: 10.1016/S0021-9673(00)81336-9
Lumbsch HT. Analysis of phenolic products in lichens for identification and taxonomy. In: Kranner IC, Beckett RP, Varma AK, editors. Protocols in Lichenology: culturing, Biochemistry, Ecophysiology and Use in Biomonitoring. Berlin, Heidelberg: Springer; 2002. pp. 281–95.
doi: 10.1007/978-3-642-56359-1_17
Orange A, James PW, White FJ. Microchemical methods for the identification of lichens. Second edition with additions and corrections. London: British Lichen Society; 2010.
Wilken PM, Aylward J, Chand R, Grewe F, Lane FA, Sinha S, et al. IMA Genome - F13. IMA Fungus. 2020;11:19.
pubmed: 33014691
pmcid: 7513301
doi: 10.1186/s43008-020-00039-7
Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genomics. 2017;3:e000132.
doi: 10.1099/mgen.0.000132
Andrews S. FastQC: A quality control tool for high throughput sequence data. 2010. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ . Accessed 18 Jan 2023.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37:540–6.
pubmed: 30936562
doi: 10.1038/s41587-019-0072-8
Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017;27:737–46.
pubmed: 28100585
pmcid: 5411768
doi: 10.1101/gr.214270.116
medaka. Sequence correction provided by ONT Research. https://github.com/nanoporetech/medaka . Accessed 12 Mar 2022.
Hu J, Fan J, Sun Z, Liu S. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics. 2020;36:2253–5.
pubmed: 31778144
doi: 10.1093/bioinformatics/btz891
Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257.
pubmed: 31779668
pmcid: 6883579
doi: 10.1186/s13059-019-1891-0
Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics. 2018;34:i142–50.
pubmed: 29949969
pmcid: 6022658
doi: 10.1093/bioinformatics/bty266
Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021;38:4647–54.
pubmed: 34320186
pmcid: 8476166
doi: 10.1093/molbev/msab199
Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci. 2020;117:9451–7.
pubmed: 32300014
pmcid: 7196820
doi: 10.1073/pnas.1921046117
Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2013. http://www.repeatmasker.org . Accessed 27 Oct 2023.
Koochekian N, Ascanio A, Farleigh K, Card DC, Schield DR, Castoe TA, et al. A chromosome-level genome assembly and annotation of the desert horned lizard, Phrynosoma platyrhinos, provides insight into chromosomal rearrangements among reptiles. GigaScience. 2022;11:giab098.
pubmed: 35134927
pmcid: 8848323
doi: 10.1093/gigascience/giab098
Palmer JM, Stajich JE. Funannotate v1.8.1: Eukaryotic genome annotation. Zenodo; 2020.
Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes De Novo Assembler. Curr Protocols Bioinf. 2020;70:e102.
doi: 10.1002/cpbi.102
Shen W, Le S, Li Y, Hu F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE. 2016;11:e0163962.
pubmed: 27706213
doi: 10.1371/journal.pone.0163962
Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238.
pubmed: 31727128
pmcid: 6857279
doi: 10.1186/s13059-019-1832-y
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Rambaut A, FigTree. 2023. http://tree.bio.ed.ac.uk/software/figtree/ . Accessed 5 Sep 2023.
Buchfink B, Reuter K, Drost H-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18:366–8.
pubmed: 33828273
pmcid: 8026399
doi: 10.1038/s41592-021-01101-x
Ament-Velásquez SL, Tuovinen V, Bergström L, Spribille T, Vanderpool D, Nascimbene J et al. The plot thickens: haploid and triploid-like thalli, hybridization, and biased mating type ratios in Letharia. Front Fungal Biology. 2021;2.
Wang J, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu S, et al. The conserved domain database in 2023. Nucleic Acids Res. 2023;51:D384–8.
pubmed: 36477806
doi: 10.1093/nar/gkac1096
Gioti A, Nystedt B, Li W, Xu J, Andersson A, Averette AF, et al. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia Sympodialis. mBio. 2013;4. https://doi.org/10.1128/mbio.00572-12 .
Maciver SK, de Koutsogiannis Z. Obeso Fernández Del Valle A. ‘Meiotic genes’ are constitutively expressed in an asexual amoeba and are not necessarily involved in sexual reproduction. Biol Lett. 2019;15:20180871.
pubmed: 30836881
pmcid: 6451372
doi: 10.1098/rsbl.2018.0871
Wilson AM, Wilken PM, van der Nest MA, Wingfield MJ, Wingfield BD. It’s all in the genes: the regulatory pathways of sexual reproduction in filamentous ascomycetes. Genes. 2019;10:330.
pubmed: 31052334
pmcid: 6562746
doi: 10.3390/genes10050330
Teichert I, Pöggeler S, Nowrousian M. Sordaria macrospora: 25 years as a model organism for studying the molecular mechanisms of fruiting body development. Appl Microbiol Biotechnol. 2020;104:3691–704.
pubmed: 32162092
pmcid: 7162830
doi: 10.1007/s00253-020-10504-3
Ranwez V, Douzery EJP, Cambon C, Chantret N, Delsuc F. MACSE v2: toolkit for the alignment of coding sequences accounting for frameshifts and stop codons. Mol Biol Evol. 2018;35:2582–4.
pubmed: 30165589
pmcid: 6188553
doi: 10.1093/molbev/msy159
Paradis E, Schliep K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–8.
pubmed: 30016406
doi: 10.1093/bioinformatics/bty633
Wertheim JO, Murrell B, Smith MD, Kosakovsky Pond SL, Scheffler K. RELAX: detecting relaxed selection in a phylogenetic framework. Mol Biol Evol. 2015;32:820–32.
pubmed: 25540451
doi: 10.1093/molbev/msu400
Kosakovsky Pond SL, Poon AFY, Velazquez R, Weaver S, Hepler NL, Murrell B, et al. HyPhy 2.5—a customizable platform for evolutionary hypothesis testing using phylogenies. Mol Biol Evol. 2020;37:295–9.
pubmed: 31504749
doi: 10.1093/molbev/msz197
Armaleo D, Müller O, Lutzoni F, Andrésson ÓS, Blanc G, Bode HB, et al. The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris Glomerata. BMC Genomics. 2019;20:605.
pubmed: 31337355
pmcid: 6652019
doi: 10.1186/s12864-019-5629-x
Rydholm C, Dyer PS, Lutzoni F. DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell. 2007;6:868–74.
pubmed: 17384199
pmcid: 1899244
doi: 10.1128/EC.00319-06
Dyer PS, Inderbitzin P, Debuchy R. 14 mating-type structure, function, regulation and evolution in the Pezizomycotina. In: Wendland J, editor. Growth, differentiation and sexuality. Cham: Springer International Publishing; 2016. pp. 351–85.
doi: 10.1007/978-3-319-25844-7_14
Wilson AM, Wilken PM, Wingfield MJ, Wingfield BD. Genetic networks that govern sexual Reproduction in the Pezizomycotina. Microbiol Mol Biol Rev. 2021;85:e00020–21.
pubmed: 34585983
pmcid: 8485983
doi: 10.1128/MMBR.00020-21
Coelho MA, Ianiri G, David-Palma M, Theelen B, Goyal R, Narayanan A et al. Frequent transitions in mating-type locus chromosomal organization in Malassezia and early steps in sexual reproduction. Proceedings of the National Academy of Sciences. 2023;120:e2305094120.
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci. 2013;110:20117–22.
pubmed: 24277808
pmcid: 3864322
doi: 10.1073/pnas.1313452110
Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L, et al. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol. 2016;1:1–9.
doi: 10.1038/nmicrobiol.2016.33
Mateus ID, Rojas EC, Savary R, Dupuis C, Masclaux FG, Aletti C, et al. Coexistence of genetically different Rhizophagus Irregularis isolates induces genes involved in a putative fungal mating response. ISME J. 2020;14:2381–94.
pubmed: 32514118
pmcid: 7490403
doi: 10.1038/s41396-020-0694-3
Mateus ID, Lee S-J, Sanders IR. Co-existence of AMF with different putative MAT-alleles induces genes homologous to those involved in mating in other fungi: a reply to Malar et al. ISME J. 2021;15:2180–2.
pubmed: 33941891
pmcid: 8319373
doi: 10.1038/s41396-021-00979-x
Short DPG, Gurung S, Hu X, Inderbitzin P, Subbarao KV. Maintenance of sex-related genes and the co-occurrence of both mating types in Verticillium Dahliae. PLoS ONE. 2014;9:e112145.
pubmed: 25383550
pmcid: 4226480
doi: 10.1371/journal.pone.0112145
Li W-H, Gojobori T, Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981;292:237–9.
pubmed: 7254315
doi: 10.1038/292237a0
Croll D, Sanders IR. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evol Biol. 2009;9:13.
pubmed: 19146661
pmcid: 2630297
doi: 10.1186/1471-2148-9-13
Mateus ID, Auxier B, Ndiaye MMS, Cruz J, Lee S-J, Sanders IR. Reciprocal recombination genomic signatures in the symbiotic arbuscular mycorrhizal fungi Rhizophagus Irregularis. PLoS ONE. 2022;17:e0270481.
pubmed: 35776745
pmcid: 9249182
doi: 10.1371/journal.pone.0270481
Braus GH, Irniger S, Bayram Ö. Fungal development and the COP9 signalosome. Curr Opin Microbiol. 2010;13:672–6.
pubmed: 20934903
doi: 10.1016/j.mib.2010.09.011
Busch S, Eckert SE, Krappmann S, Braus GH. The COP9 signalosome is an essential regulator of development in the filamentous fungus aspergillus nidulans. Mol Microbiol. 2003;49:717–30.
pubmed: 12864854
doi: 10.1046/j.1365-2958.2003.03612.x
Busch S, Schwier EU, Nahlik K, Bayram Ö, Helmstaedt K, Draht OW, et al. An eight-subunit COP9 signalosome with an intact JAMM motif is required for fungal fruit body formation. Proc Natl Acad Sci. 2007;104:8089–94.
pubmed: 17470786
pmcid: 1876576
doi: 10.1073/pnas.0702108104
Lendemer J. A monograph of the crustose members of the genus Lepraria Ach. s. str. (Stereoculaceae, Lichenized Ascomycetes) in North America north of Mexico. Opuscula Philolichenum. 2013;13:36–141.
Tønsberg T, Jørgensen PM. On the alleged apothecia of Leproloma membranaceum (DICKS.) Vain. Lichenologist. 1997;29:597–9.
doi: 10.1006/lich.1997.0110
Dyer PS, Kück U. Sex and the imperfect fungi. Microbiol Spectr. 2017;5:5310.
doi: 10.1128/microbiolspec.FUNK-0043-2017
Hull CM, Johnson AD. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science. 1999;285:1271–5.
pubmed: 10455055
doi: 10.1126/science.285.5431.1271
Forche A, Alby K, Schaefer D, Johnson AD, Berman J, Bennett RJ. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 2008;6:e110.
pubmed: 18462019
pmcid: 2365976
doi: 10.1371/journal.pbio.0060110
Schoustra SE, Debets AJM, Slakhorst M, Hoekstra RF. Mitotic recombination accelerates adaptation in the fungus aspergillus nidulans. PLoS Genet. 2007;3:e68.
pubmed: 17465683
pmcid: 1857732
doi: 10.1371/journal.pgen.0030068
Doellman MM, Sun Y, Barcenas-Peña A, Lumbsch HT, Grewe F. Rethinking asexuality: the enigmatic case of functional sexual genes in Lepraria (Stereocaulaceae). 2024. https://www.ncbi.nlm.nih.gov/bioproject/1119491 .
Doellman MM, Sun Y, Barcenas-Peña A, Lumbsch HT, Grewe F. Data from: rethinking asexuality: the enigmatic case of functional sexual genes in Lepraria (Stereocaulaceae). 2024. https://datadryad.org/stash/dataset/doi:10.5061/dryad.pzgmsbcwz .