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Interspecific hybridization as a driver of fungal evolution and adaptation

Abstract

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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Fig. 1: Occurrence of interspecific hybridization in fungi.
Fig. 2: Road map to overcoming species boundaries.
Fig. 3: Genome stabilization after hybridization.
Fig. 4: Transcriptional response to hybridization.
Fig. 5: Assembly of protein complexes in fungal interspecific hybrids.

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Acknowledgements

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).

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Glossary

Interspecific hybridization

Defined in this Review as hybridization between two or more genetically isolated populations that can usually be generalized as ‘species’.

Heteroploid

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.

Selfing

Mating between gametes from the same diploid organism.

Conspecific

From the same species.

Heterospecific

From a different species.

Sympatric

Occurring in the same geographical location.

Allopatric

Occurring in a non-overlapping geographical location.

Aneuploid

Under-representation or over-representation of one or more chromosomes in a cell.

Euploidy

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.

Flocculation

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.

Synteny

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

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