Cross-species gene transfer is often associated with bacteria, which have evolved several mechanisms that facilitate horizontal DNA exchange. However, the increased availability of whole-genome sequences has revealed that fungal species also exchange DNA, leading to intertwined lineages, blurred species boundaries or even novel species. In contrast to prokaryotes, fungal DNA exchange originates from interspecific hybridization, where two genomes are merged into a single, often highly unstable, polyploid genome that evolves rapidly into stabler derivatives. The resulting hybrids can display novel combinations of genetic and phenotypic variation that enhance fitness and allow colonization of new niches. Interspecific hybridization led to the emergence of important pathogens of humans and plants (for example, various Candida and ‘powdery mildew’ species, respectively) and industrially important yeasts, such as Saccharomyces hybrids that are important in the production of cold-fermented lagers or cold-cellared Belgian ales. In this Review, we discuss the genetic processes and evolutionary implications of fungal interspecific hybridization and highlight some of the best-studied examples. In addition, we explain how hybrids can be used to study molecular mechanisms underlying evolution, adaptation and speciation, and serve as a route towards development of new variants for industrial applications.
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Griffith, F. The significance of pneumococcal types. J. Hyg. 27, 113–159 (1928).
Sun, D. Pull in and push out: mechanisms of horizontal gene transfer in bacteria. Front. Microbiol. 9, 2154 (2018).
Riley, M. A. & Lizotte-Waniewski, M. Population genomics and the bacterial species concept. Methods Mol. Biol. 532, 367–377 (2009).
Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then…and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).
Stebbins, G. The role of hybridization in evolution. Proc. Am. Philos. Soc. 103, 231–251 (1959).
Hübner, S. et al. Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nat. Plants 5, 54–62 (2019).
Lamichhaney, S. et al. Rapid hybrid speciation in Darwin’s finches. Science 359, 224–228 (2018).
Edelman, N. B. et al. Genomic architecture and introgression shape a butterfly radiation. Science 366, 594–599 (2019).
Mixão, V. & Gabaldón, T. Hybridization and emergence of virulence in opportunistic human yeast pathogens. Yeast 35, 5–20 (2018). In this review, the authors comprehensively discuss how hybridization can influence the origin and evolution of pathogenic fungal lineages.
Gallone, B. et al. Interspecific hybridization facilitates niche adaptation in beer yeast. Nat. Ecol. Evol. 3, 1562–1575 (2019).
Möller, M. & Stukenbrock, E. H. Evolution and genome architecture in fungal plant pathogens. Nat. Rev. Microbiol. 15, 756–771 (2017).
Kominek, J. et al. Eukaryotic acquisition of a bacterial operon. Cell 176, 1356–1366.e10 (2019). In this article, the authors identify a case of adaptive ‘horizontal operon transfer’ from bacteria to fungi, which (after selection to facilitate gene expression) led to efficient iron scavenging.
Routh, A., Domitrovic, T. & Johnson, J. E. Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus. Proc. Natl Acad. Sci. USA 109, 1907–1912 (2012).
Lee, S. C., Ni, M., Li, W., Shertz, C. & Heitman, J. The evolution of sex: a perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 72, 298–340 (2010).
Idnurm, A., James, T. Y. & Vilgalys, R. Sex in the rest: mysterious mating in the Chytridiomycota and Zygomycota. in Sex in Fungi 405–418 (ASM Press, 2007).
Coelho, M. A., Bakkeren, G., Sun, S., Hood, M. E. & Giraud, T. Fungal sex: basidiomycota. Fungal Kingd. 5, 147–175 (2017).
Clutterbuck, A. J. Parasexual recombination in fungi. J. Genet. 75, 281–286 (1996).
Bennett, R. J. The parasexual lifestyle of Candida albicans. Curr. Opin. Microbiol. 28, 10–17 (2015).
Anderson, J. B. et al. Determinants of divergent adaptation and Dobzhansky-Muller interaction in experimental yeast populations. Curr. Biol. 20, 1383–1388 (2010).
Mallet, J. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos. Trans. R. Soc. B Biol. Sci. 363, 2971–2986 (2008).
D’Angiolo, M. et al. A yeast living ancestor reveals the origin of genomic introgressions. Nature 587, 420–425 (2020). This article shows how genome instability during mitotic growth of hybrid populations can lead to introgresssions and how this process over time can restore fertility.
Kiss, L. et al. Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Mol. Ecol. 20, 1492–1507 (2011).
Greig, D. & Leu, J. Y. Natural history of budding yeast. Curr. Biol. 19, R886–R890 (2009).
Giraud, T., Yockteng, R., López-Villavicencio, M., Refrégier, G. & Hood, M. E. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot. Cell 7, 765–775 (2008).
Karlsson, M., Nygren, K. & Johannesson, H. The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic. Neurospora. Mol. Biol. Evol. 25, 168–178 (2007).
Grabenstein, K. C. & Taylor, S. A. Breaking barriers: causes, consequences, and experimental utility of human-mediated hybridization. Trends Ecol. Evol. 33, 198–212 (2018).
Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463 (2019).
Fisher, M. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).
O’Hanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018).
Greenspan, S. E. et al. Hybrids of amphibian chytrid show high virulence in native hosts. Sci. Rep. 8, 9600 (2018).
Wallace, A. R. Darwinism: An Exposition of the Theory of Natural Selection, with Some of Its Applications (Cosimo Inc., 2007).
Kuehne, H. A., Murphy, H. A., Francis, C. A. & Sniegowski, P. D. Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Curr. Biol. 17, 407–411 (2007).
Giraud, T. & Gourbière, S. The tempo and modes of evolution of reproductive isolation in fungi. Heredity 109, 204–214 (2012).
Turner, E., Jacobson, D. J. & Taylor, J. W. Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus. J. Evol. Biol. 23, 1642–1656 (2010).
Gac, M. L. E. & Giraud, T. Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota. J. Evol. Biol. 21, 761–772 (2008).
Brasier, C. The rise of the hybrid fungi. Nature 405, 134–135 (2000).
Dujon, B. A. & Louis, E. J. Genome diversity and evolution in the budding yeasts (Saccharomycotina). Genetics 206, 717–750 (2017).
Dettman, J. R., Sirjusingh, C., Kohn, L. M. & Anderson, J. B. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447, 585–588 (2007).
Paoletti, M. Vegetative incompatibility in fungi: From recognition to cell death, whatever does the trick. Fungal Biol. Rev. 30, 152–162 (2016).
Rogers, D. W., McConnell, E., Ono, J. & Greig, D. Spore-autonomous fluorescent protein expression identifies meiotic chromosome mis-segregation as the principal cause of hybrid sterility in yeast. PLoS Biol. 16, e2005066 (2018).
Bozdag, G. O. et al. Engineering recombination between diverged yeast species reveals genetic incompatibilities. bioRxiv https://doi.org/10.1101/755165 (2019).
Charron, G., Marsit, S., Hénault, M., Martin, H. & Landry, C. R. Spontaneous whole-genome duplication restores fertility in interspecific hybrids. Nat. Commun. 10, 4126 (2019).
Ortiz-Merino, R. A. et al. Evolutionary restoration of fertility in an interspecies hybrid yeast, by whole-genome duplication after a failed mating-type switch. PLoS Biol. 15, e2002128 (2017).
Wolfe, K. H. Origin of the yeast whole-genome duplication. PLoS Biol. 13, e1002221 (2015).
Marcet-Houben, M. & Gabaldón, T. Beyond the whole-genome duplication: Phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol. 13, e1002220 (2015).
Mozzachiodi, S. et al. Aborting meiosis overcomes hybrid sterility. bioRxiv https://doi.org/10.1101/2020.12.04.411579 (2020).
Leducq, J. B. et al. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat. Microbiol. 1, 1–10 (2016).
Stukenbrock, E. H., Christiansen, F. B., Hansen, T. T., Dutheil, J. Y. & Schierup, M. H. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc. Natl Acad. Sci. USA 109, 10954–10959 (2012). This article describes one of the few cases of homoploid speciation discovered in fungi to date.
Bar-Zvi, D., Lupo, O., Levy, A. A. & Barkai, N. Hybrid vigor: the best of both parents, or a genomic clash? Curr. Opin. Syst. Biol. 6, 22–27 (2017).
Birchler, J. A., Yao, H., Chudalayandi, S., Vaiman, D. & Veitia, R. A. Heterosis. Plant Cell 22, 2105–2112 (2010).
Carlborg, Ö. & Haley, C. S. Epistasis: too often neglected in complex trait studies? Nat. Rev. Genet. 5, 618–625 (2004).
Krogerus, K. et al. Ploidy influences the functional attributes of de novo lager yeast hybrids. Appl. Microbiol. Biotechnol. 100, 7203–7222 (2016).
Herbst, R. H. et al. Heterosis as a consequence of regulatory incompatibility. BMC Biol. 15, 38 (2017).
Tirosh, I., Reikhav, S., Levy, A. A. & Barkai, N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324, 659–662 (2009). In this article, the authors map the contribution of cis and trans polymorphisms to expression variation in an interspecific yeast hybrid.
Feurtey, A., Stevens, D. M., Stephan, W. & Stukenbrock, E. H. Interspecific gene exchange introduces high genetic variability in crop pathogen. Genome Biol. Evol. 11, 3095–9105 (2019).
Corcoran, P. et al. Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma. Genome Res. 26, 486–498 (2016). By investigating 92 Neurospora genomes, the authors identify many cases of adaptive introgressions in the mat locus.
Sun, Y. et al. Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma. PLoS Genet. 8, e1002820 (2012).
Peter, J. et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature 556, 339–344 (2018).
Langdon, Q. K. et al. Fermentation innovation through complex hybridization of wild and domesticated yeasts. Nat. Ecol. Evol. 3, 1576–1586 (2019).
Magwene, P. M. et al. Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 108, 1987–1992 (2011).
Pryszcz, L. P. et al. The genomic aftermath of hybridization in the opportunistic pathogen Candida metapsilosis. PLOS Genet. 11, e1005626 (2015).
Vishnoi, A., Sethupathy, P., Simola, D., Plotkin, J. B. & Hannenhalli, S. Genome-wide survey of natural selection on functional, structural, and network properties of polymorphic sites in Saccharomyces paradoxus. Mol. Biol. Evol. 28, 2615–2627 (2011).
Taylor, S. A. & Larson, E. L. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3, 170–177 (2019).
Lancaster, S. M., Payen, C., Smukowski Heil, C. & Dunham, M. J. Fitness benefits of loss of heterozygosity in Saccharomyces hybrids. Genome Res. 29, 1685–1692 (2019).
Smukowski Heil, C. S. et al. Loss of heterozygosity drives adaptation in hybrid yeast. Mol. Biol. Evol. 34, 1596–1612 (2017). In this article, the authors demonstrate how LOH can be adaptive in experimentally evolved populations of hybrid yeast.
Zhang, Z. et al. Recombining your way out of trouble: the genetic architecture of hybrid fitness under environmental stress. Mol. Biol. Evol. 37, 167–182 (2020).
Smukowski Heil, C. S. et al. Temperature preference can bias parental genome retention during hybrid evolution. PLoS Genet. 15, e1008383 (2019).
Mixão, V. & Gabaldón, T. Genomic evidence for a hybrid origin of the yeast opportunistic pathogen Candida albicans. BMC Biol. 18, 48 (2020).
Liang, S. H. & Bennett, R. J. The impact of gene dosage and heterozygosity on the diploid pathobiont Candida albicans. J. Fungi 6, 10 (2020).
Ford, C. B. et al. The evolution of drug resistance in clinical isolates of Candida albicans. eLife 2015, 1–27 (2015).
Selmecki, A. M. et al. Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–352 (2015).
Pavelka, N. et al. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468, 321–325 (2010).
Yang, F. et al. Aneuploidy enables cross-adaptation to unrelated drugs. Mol. Biol. Evol. 36, 1768–1782 (2019).
Gilchrist, C. & Stelkens, R. Aneuploidy in yeast: segregation error or adaptation mechanism? Yeast 36, 525–539 (2019).
Yona, A. H. et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl Acad. Sci. USA 109, 21010–21015 (2012).
Hu, G. et al. Variation in chromosome copy number influences the virulence of Cryptococcus neoformans and occurs in isolates from AIDS patients. BMC Genomics 12, 526 (2011).
van den Broek, M. et al. Chromosomal copy number variation in Saccharomyces pastorianus is evidence for extensive genome dynamics in industrial lager brewing strains. Appl. Environ. Microbiol. 81, 6253–6267 (2015).
Van De Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).
Basse, C. W. Mitochondrial inheritance in fungi. Curr. Opin. Microbiol. 13, 712–719 (2010).
Olson, Å. & Stenlid, J. Mitochondrial control of fungal hybrid virulence. Nature 411, 438 (2001).
Giordano, L., Sillo, F., Garbelotto, M. & Gonthier, P. Mitonuclear interactions may contribute to fitness of fungal hybrids. Sci. Rep. 8, 1706 (2018).
Barr, C. M., Neiman, M. & Taylor, D. R. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol. 168, 39–50 (2005).
Chou, J. Y., Hung, Y. S., Lin, K. H., Lee, H. Y. & Leu, J. Y. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 8, e1000432 (2010).
Lee, H.-Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073 (2008).
Jhuang, H.-Y., Lee, H.-Y. & Leu, J.-Y. Mitochondrial-nuclear co-evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO Rep. 18, 87–101 (2017).
Hou, J., Friedrich, A., Gounot, J. S. & Schacherer, J. Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast. Nat. Commun. 6, 1–8 (2015).
Baker, E. et al. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol. Biol. Evol. 32, 2818–2831 (2015).
Mertens, S. et al. A large set of newly created interspecific Saccharomyces hybrids increases aromatic diversity in lager beers. Appl. Environ. Microbiol. 81, 8202–8214 (2015).
Baker, E. C. P. et al. Mitochondrial DNA and temperature tolerance in lager yeasts. Sci. Adv. 5, eaav1869 (2019).
Li, X. C., Peris, D., Hittinger, C. T., Sia, E. A. & Fay, J. C. Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast. Sci. Adv. 5, eaav1848 (2019).
Grover, C. E. et al. Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol. 196, 966–971 (2012).
Yoo, M.-J., Liu, X., Pires, J. C., Soltis, P. S. & Soltis, D. E. Nonadditive gene expression in polyploids. Annu. Rev. Genet. 48, 485–517 (2014).
Steige, K. A. & Slotte, T. Genomic legacies of the progenitors and the evolutionary consequences of allopolyploidy. Curr. Opin. Plant Biol. 30, 88–93 (2016).
Bird, K. A., VanBuren, R., Puzey, J. R. & Edger, P. P. The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytol. 220, 87–93 (2018).
Edger, P. P. et al. Origin and evolution of the octoploid strawberry genome. Nat. Genet. 51, 541–547 (2019).
De Smet, R. & Van de Peer, Y. Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr. Opin. Plant Biol. 15, 168–176 (2012).
Landry, C. R. et al. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171, 1813–1822 (2005).
Takahasi, K. R., Matsuo, T. & Takano-Shimizu-Kouno, T. Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc. Natl Acad. Sci. USA 108, 15276–15281 (2011).
Zhu, W. et al. Altered chromatin compaction and histone methylation drive non-additive gene expression in an interspecific Arabidopsis hybrid. Genome Biol. 18, 1–16 (2017).
Lopez-Maestre, H. et al. Identification of misexpressed genetic elements in hybrids between Drosophila-related species. Sci. Rep. 7, 1–13 (2017).
Wu, Y. et al. Transcriptome shock in an interspecific F1 triploid hybrid of Oryza revealed by RNA sequencing. J. Integr. Plant Biol. 58, 150–164 (2016).
Cox, M. P. et al. An interspecific fungal hybrid reveals cross-kingdom rules for allopolyploid gene expression patterns. PLoS Genet. 10, e1004180 (2014). In this article, the authors describe how the transcriptional response to hybridization is conserved between fungi and plants, and how this reflects conservation of the mutational processes underlying eukaryotic gene regulatory evolution.
Olesen, K., Felding, T., Gjermansen, C. & Hansen, J. The dynamics of the Saccharomyces carlsbergensis brewing yeast transcriptome during a production-scale lager beer fermentation. FEMS Yeast Res. 2, 563–573 (2002).
Horinouchi, T. et al. Genome-wide expression analysis of Saccharomyces pastorianus orthologous genes using oligonucleotide microarrays. J. Biosci. Bioeng. 110, 602–607 (2010).
Hovhannisyan, H. et al. Integrative omics analysis reveals a limited transcriptional shock after yeast interspecies hybridization. Front. Genet. 11, 404 (2020).
Sriswasdi, S., Takashima, M., ichiroh Manabe, R., Ohkuma, M. & Iwasaki, W. Genome and transcriptome evolve separately in recently hybridized Trichosporon fungi. Commun. Biol. 2, 1–9 (2019).
Sriswasdi, S. et al. Global deceleration of gene evolution following recent genome hybridizations in fungi. Genome Res. 26, 1081–1090 (2016).
Bolat, I., Romagnoli, G., Zhu, F., Pronk, J. T. & Daran, J. M. Functional analysis and transcriptional regulation of two orthologs of ARO10, encoding broad-substrate-specificity 2-oxo-acid decarboxylases, in the brewing yeast Saccharomyces pastorianus CBS1483. FEMS Yeast Res. 13, 505–517 (2013).
Hovhannisyan, H., Saus, E., Ksiezopolska, E. & Gabaldón, T. The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis. mSphere 5, e00282-20 (2020).
Metzger, B. P. H., Wittkopp, P. J. & Coolon, J. D. Evolutionary dynamics of regulatory changes underlying gene expression divergence among Saccharomyces species. Genome Biol. Evol. 9, 843–854 (2017).
Kellis, M., Patterson, N., Endrizzi, M., Birren, B. & Lander, E. S. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423, 241–254 (2003).
Wu, J. et al. Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus. BMC Genomics 19, 586 (2018).
Yoo, M. J., Szadkowski, E. & Wendel, J. F. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110, 171–180 (2013).
Campbell, M. A. et al. Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy. Mycologia 109, 715–729 (2017).
Krieger, G., Lupo, O., Levy, A. A. & Barkai, N. Independent evolution of transcript abundance and gene regulatory dynamics. Genome Res. 30, 1000–1011 (2020).
Tirosh, I. & Barkai, N. Inferring regulatory mechanisms from patterns of evolutionary divergence. Mol. Syst. Biol. 7, 530 (2011).
Metzger, B. P. H. et al. Contrasting frequencies and effects of cis- and trans-regulatory mutations affecting gene expression. Mol. Biol. Evol. 33, 1131–1146 (2016).
Yang, B. & Wittkopp, P. J. Structure of the transcriptional regulatory network correlates with regulatory divergence in Drosophila. Mol. Biol. Evol. 34, 1352–1362 (2017).
Li, X. C. & Fay, J. C. Cis-regulatory divergence in gene expression between two thermally divergent yeast species. Genome Biol. Evol. 9, 1120–1129 (2017).
Christiaens, J. F. et al. Functional divergence of gene duplicates through ectopic recombination. EMBO Rep. 13, 1145–1151 (2012).
Hewitt, S. K., Donaldson, I. J., Lovell, S. C. & Delneri, D. Sequencing and characterisation of rearrangements in three S. pastorianus strains reveals the presence of chimeric genes and gives evidence of breakpoint reuse. PLoS ONE 9, e92203 (2014).
Dunn, B. et al. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet. 9, e1003366 (2013).
Dandage, R. et al. Frequent assembly of chimeric complexes in the protein interaction network of an interspecies hybrid. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msaa298 (2020).
Leducq, J.-B. et al. Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genet. 8, e1003161 (2012).
Piatkowska, E. M., Naseeb, S., Knight, D. & Delneri, D. Chimeric protein complexes in hybrid species generate novel phenotypes. PLoS Genet. 9, e1003836 (2013).
Zamir, L. et al. Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility. Proc. Natl Acad. Sci. USA 109, E406–E414 (2012).
Hornsey, I. S. A History of Beer and Brewing (Royal Society of Chemistry, 2003).
Steensels, J., Gallone, B., Voordeckers, K. & Verstrepen, K. J. Domestication of Industrial Microbes. Curr. Biol. 29, R381–R393 (2019).
Gallone, B. et al. Origins, evolution, domestication and diversity of Saccharomyces beer yeasts. Curr. Opin. Biotechnol. 49, 148–155 (2018).
Salazar, A. N. et al. Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization. BMC Genomics 20, 916 (2019).
Okuno, M. et al. Next-generation sequencing analysis of lager brewing yeast strains reveals the evolutionary history of interspecies hybridization. DNA Res. 23, dsv037 (2016).
Walther, A., Hesselbart, A. & Wendland, J. Genome sequence of Saccharomyces carlsbergensis, the world’s first pure culture lager yeast. G3 4, 783–793 (2014).
Monerawela, C., James, T. C., Wolfe, K. H. & Bond, U. Loss of lager specific genes and subtelomeric regions define two different Saccharomyces cerevisiae lineages for Saccharomyces pastorianus group I and II strains. FEMS Yeast Res. 15, fou008 (2015).
Steensels, J. et al. Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol. Rev. 38, 947–995 (2014).
Dzialo, M. C., Park, R., Steensels, J., Lievens, B. & Verstrepen, K. J. Physiology, ecology and industrial applications of aroma formation in yeast. FEMS Microbiol. Rev. 41, S95–S128 (2017).
Goold, H. D. et al. Yeast’s balancing act between ethanol and glycerol production in low-alcohol wines. Microb. Biotechnol. 10, 264–278 (2017).
Bellon, J. R., Schmid, F., Capone, D. L., Dunn, B. L. & Chambers, P. J. Introducing a new breed of wine yeast: interspecific hybridisation between a commercial Saccharomyces cerevisiae wine yeast and Saccharomyces mikatae. PLoS ONE 8, e62053 (2013).
Jetti, K. D., Gns, R. R., Garlapati, D. & Nammi, S. K. Improved ethanol productivity and ethanol tolerance through genome shuffling of Saccharomyces cerevisiae and Pichia stipitis. Int. Microbiol. 22, 247–254 (2019).
Peris, D. et al. Synthetic hybrids of six yeast species. Nat. Commun. 11, 1–11 (2020).
Depotter, J. R. L., Seidl, M. F. & Wood, T. A. Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Curr. Opin. Microbiol. 32, 7–13 (2016).
Brasier, C. M., Cooke, D. E. L. & Duncan, J. M. Origin of a new Phytophthora pathogen through interspecific hybridization. Proc. Natl Acad. Sci. USA 96, 5878–5883 (1999).
Hessenauer, P. et al. Hybridization and introgression drive genome evolution of Dutch elm disease pathogens. Nat. Ecol. Evol. 4, 626–638 (2020). This article describes how humans can facilitate hybridization between fungal species and in this way lead to new, highly virulent plant pathogens.
Steenwyk, J. L. et al. Pathogenic allodiploid hybrids of Aspergillus fungi. Curr. Biol. 30, 2495–2507 (2020).
Pfaller, M. A. & Diekema, D. J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133–163 (2007).
Ropars, J. et al. Gene flow contributes to diversification of the major fungal pathogen Candida albicans. Nat. Commun. 9, 1–10 (2018).
Mixão, V. et al. Whole-genome sequencing of the opportunistic yeast pathogen Candida inconspicua uncovers its hybrid origin. Front. Genet. 10, 383 (2019).
Pryszcz, L. P., Németh, T., Gacser, A. & Gabaldón, T. Genome comparison of Candida Orthopsilosis clinical strains reveals the existence of hybrids between two distinct subspecies. Genome Biol. Evol. 6, 1069–1078 (2014).
Schröder, M. S. et al. Multiple origins of the pathogenic yeast Candida orthopsilosis by separate hybridizations between two parental species. PLoS Genet. 12, e1006404 (2016).
Glawe, D. A. The powdery mildews: a review of the world’s most familiar (yet poorly known) plant pathogens. Annu. Rev. Phytopathol. 46, 27–51 (2008).
Wicker, T. et al. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat. Genet. 45, 1092–1096 (2013).
Menardo, F. et al. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat. Genet. 48, 201–205 (2016).
Walker, A. S., Bouguennec, A., Confais, J., Morgant, G. & Leroux, P. Evidence of host-range expansion from new powdery mildew (Blumeria graminis) infections of triticale (×Triticosecale) in France. Plant Pathol. 60, 207–220 (2011).
Troch, V., Audenaert, K., Bekaert, B., Höfte, M. & Haesaert, G. Phylogeography and virulence structure of the powdery mildew population on its ‘new’ host triticale. BMC Evol. Biol. 12, 76 (2012).
Shen, X. X. et al. Tempo and mode of genome evolution in the budding yeast subphylum. Cell 175, 1533–1545 (2018).
Gallone, B. et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166, 1397–1410 (2016).
Dujon, B. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22, 375–387 (2006).
Gryganskyi, A. P. et al. Phylogenetic and phylogenomic definition of Rhizopus species. G3 8, 2007–2018 (2018).
Wu, G. et al. Genus-wide comparative genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human skin. PLoS Genet. 11, e1005614 (2015).
Bovers, M. et al. Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res. 6, 599–607 (2006).
Libkind, D. et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc. Natl Acad. Sci. USA 108, 14539–14544 (2011).
Peŕez-Través, L., Lopes, C. A., Querol, A. & Barrio, E. On the complexity of the Saccharomyces bayanus taxon: Hybridization and potential hybrid speciation. PLoS ONE 9, e93729 (2014).
Borneman, A. R., Zeppel, R., Chambers, P. J. & Curtin, C. D. Insights into the Dekkera bruxellensis genomic landscape: comparative genomics reveals variations in ploidy and nutrient utilisation potential amongst wine isolates. PLoS Genet. 10, e1004161 (2014).
Louis, V. L. et al. Pichia sorbitophila, an interspecies yeast hybrid, reveals early steps of genome resolution after polyploidization. G3 2, 299–311 (2012).
Saubin, M. et al. Investigation of genetic relationships between Hanseniaspora species found in grape musts revealed interspecific hybrids with dynamic genome structures. Front. Microbiol. 10, 2960 (2020).
Neafsey, D. E. et al. Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res. 20, 938–946 (2010).
Staats, M., van Baarlen, P. & van Kan, J. A. L. Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Mol. Biol. Evol. 22, 333–346 (2004).
Inderbitzin, P., Davis, R. M., Bostock, R. M. & Subbarao, K. V. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS ONE 6, e18260 (2011).
Nikulin, J., Krogerus, K. & Gibson, B. Alternative Saccharomyces interspecies hybrid combinations and their potential for low-temperature wort fermentation. Yeast 35, 113–127 (2018).
Magalhães, F., Krogerus, K., Vidgren, V., Sandell, M. & Gibson, B. Improved cider fermentation performance and quality with newly generated Saccharomyces cerevisiae×Saccharomyces eubayanus hybrids. J. Ind. Microbiol. Biotechnol. 44, 1203–1213 (2017).
Bizaj, E. et al. A breeding strategy to harness flavor diversity of Saccharomyces interspecific hybrids and minimize hydrogen sulfide production. FEMS Yeast Res. 12, 456–465 (2012).
Peris, D. et al. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnol. Biofuels 10, 78 (2017).
Winans, M. J. et al. Saccharomyces arboricola and its hybrids’ propensity for sake production: interspecific hybrids reveal increased fermentation abilities and a mosaic metabolic profile. Fermentation 6, 14 (2020).
Varavallo, M. A. et al. Isolation of recombinant strains with enhanced pectinase production by protoplast fusion between Penicillium expansum and Penicillium griseoroseum. Brazilian J. Microbiol. 38, 52–57 (2007).
Kaur, B., Oberoi, H. S. & Chadha, B. S. Enhanced cellulase producing mutants developed from heterokaryotic Aspergillus strain. Bioresour. Technol. 156, 100–107 (2014).
Guo, X., Wang, R., Chen, Y. & Xiao, D. Intergeneric yeast fusants with efficient ethanol production from cheese whey powder solution: construction of a Kluyveromyces marxianus and Saccharomyces cerevisiae AY-5 hybrid. Eng. Life Sci. 12, 656–661 (2012).
Ye, M., Yue, T., Yuan, Y. & Wang, L. Production of yeast hybrids for improvement of cider by protoplast electrofusion. Biochem. Eng. J. 81, 162–169 (2013).
Patil, N. S., Patil, S. M., Govindwar, S. P. & Jadhav, J. P. Molecular characterization of intergeneric hybrid between Aspergillus oryzae and Trichoderma harzianum by protoplast fusion. J. Appl. Microbiol. 118, 390–398 (2015).
Deng, Z. et al. Enhanced phytoremediation of multi-metal contaminated soils by interspecific fusion between the protoplasts of endophytic Mucor sp. CBRF59 and Fusarium sp. CBRF14. Soil. Biol. Biochem. 77, 31–40 (2014).
Li, Y. et al. A genome-scale phylogeny of fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny. Curr. Biol. https://doi.org/10.1016/j.cub.2021.01.074 (2020).
Leducq, J.-B. et al. Mitochondrial recombination and introgression during speciation by hybridization. Mol. Biol. Evol. 34, 1947–1959 (2017).
K.J.V. acknowledges funding from KU Leuven, European Research Council (ERC) Consolidator Grant CoG682009, Vlaams Instituut voor Biotechnologie (VIB), Fonds voor Wetenschappelijk Onderzoek – Vlaanderen (FWO) and Vlaanderen Agentschap Innoveren & Ondernemen (VLAIO). J.S. acknowledges funding from FWO (grant number 12W3918N).
The authors declare no competing interests.
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- Interspecific hybridization
Defined in this Review as hybridization between two or more genetically isolated populations that can usually be generalized as ‘species’.
The presence of an abnormal chromosome number in a cell, resulting from either aneuploidy or euploidy.
- Gene flow
Transfer of genetic material from one population to another.
Mating between gametes from the same diploid organism.
From the same species.
From a different species.
Occurring in the same geographical location.
Occurring in a non-overlapping geographical location.
Under-representation or over-representation of one or more chromosomes in a cell.
Chromosomal variation involving the entire set of chromosomes in a cell; for example, polyploidy, the presence of multiple copies of the entire set of chromosomes.
A reversible, asexual, calcium-dependent process in which cells adhere to form flocs consisting of thousands of cells.
- Homoeologue expression bias
Unequal contribution of one homoeologue to the total gene expression.
- Subgenome dominance
Genome-wide expression skewed towards one subgenome.
- Homoeologous genes
Corresponding parent orthologues in the hybrid.
- Orthologous genes
Homologous genes (those deriving from the same ancestral sequence) that arise from speciation.
- Cis-regulatory elements
Non-coding regions, such as promoters, transcription factor-binding sites and terminators, which are near genes and are thus linked to a single subgenome.
- Trans-regulatory elements
Elements such as transcription factors, chromatin regulators and signalling molecules which interact with cis elements but act independently of their own genomic location and are therefore shared by subgenomes residing in the same nucleus.
- Subgenome homogenization
A process in which subgenomes in a hybrid become more uniform due to genome stabilization, such as by gene conversion.
- Chimeric genes
Genes consisting of a fusion of the 5′ part of one parent gene to the 3′ end of the other parent gene.
Co-occurrence of loci on the same chromosome among two species, with or without a conserved order.
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Steensels, J., Gallone, B. & Verstrepen, K.J. Interspecific hybridization as a driver of fungal evolution and adaptation. Nat Rev Microbiol 19, 485–500 (2021). https://doi.org/10.1038/s41579-021-00537-4