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      Hybridization and the origin of new yeast lineages

      research-article
      FEMS Yeast Research
      Oxford University Press
      hybridization, whole-genome duplication, allopolyploidization, yeast, Saccharomyces, Candida

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          ABSTRACT

          Hybrids originate from the mating of two diverged organisms, resulting in novel lineages that have chimeric genomes. Hybrids may exhibit unique phenotypic traits that are not necessarily intermediate between those present in the progenitors. These unique traits may enable them to thrive in new environments. Many hybrid lineages have been discovered among yeasts in the Saccharomycotina, of which many have industrial or clinical relevance, but this might reflect a bias toward investigating species with relevance to humans. Hybridization has also been proposed to be at the root of the whole-genome duplication in the lineage leading to Saccharomyces cerevisiae. Thus, hybridization seems to have played a prominent role in the evolution of Saccharomycotina yeasts, although it is still unclear how common this evolutionary process has been during the evolution of this and other fungal clades. Similarly, the evolutionary aftermath of hybridization, including implications at the genomic, transcriptional, physiological or ecological levels, remains poorly understood. In this review, I survey recent findings from genomic analysis of yeast hybrids of industrial or clinical relevance, and discuss the evolutionary implications of genomic hybridization for the origin of new lineages, including when such hybridization results in a whole-genome duplication.

          Abstract

          Here, the consequences of hybridization at the genetic and ecological levels are discussed.

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          Most cited references63

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            The significance of responses of the genome to challenge.

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              Polyploidy and genome evolution in plants.

              Plant genomes vary in size and complexity, fueled in part by processes of whole-genome duplication (WGD; polyploidy) and subsequent genome evolution. Despite repeated episodes of WGD throughout the evolutionary history of angiosperms in particular, the genomes are not uniformly large, and even plants with very small genomes carry the signatures of ancient duplication events. The processes governing the evolution of plant genomes following these ancient events are largely unknown. Here, we consider mechanisms of diploidization, evidence of genome reorganization in recently formed polyploid species, and macroevolutionary patterns of WGD in plant genomes and propose that the ongoing genomic changes observed in recent polyploids may illustrate the diploidization processes that result in ancient signatures of WGD over geological timescales.
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                Author and article information

                Contributors
                Journal
                FEMS Yeast Res
                FEMS Yeast Res
                femsyr
                FEMS Yeast Research
                Oxford University Press
                1567-1356
                1567-1364
                13 July 2020
                August 2020
                13 July 2020
                : 20
                : 5
                : foaa040
                Affiliations
                Barcelona Supercomputing Centre (BSC-CNS) , Jordi Girona 29, 08034 Barcelona, Spain
                Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology , Baldiri Reixac 10, 08028 Barcelona, Spain
                Institució Catalana de Recerca i Estudis Avançats (ICREA) , Pg. Lluís Companys 23, 08010 Barcelona, Spain
                Author notes
                Corresponding author: Jordi Girona 29, 08034 Barcelona, Spain. Tel: 34 934011650; E-mail: toni.gabaldon.bcn@ 123456gmail.com
                Author information
                http://orcid.org/0000-0003-0019-1735
                Article
                foaa040
                10.1093/femsyr/foaa040
                7394516
                32658267
                51a53b00-7a43-42f5-bfb3-de5371841efd
                © FEMS 2020.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                : 01 May 2020
                : 10 July 2020
                Page count
                Pages: 8
                Funding
                Funded by: Spanish Ministry of Science and Innovation, DOI 10.13039/501100004837;
                Award ID: PGC2018-099921-B-I00
                Funded by: European Regional Development Fund, DOI 10.13039/501100008530;
                Funded by: Generalitat de Catalunya, DOI 10.13039/501100002809;
                Funded by: AGAUR, DOI 10.13039/501100003030;
                Award ID: SGR423
                Funded by: Horizon 2020, DOI 10.13039/100010661;
                Award ID: ERC-2016-724173
                Award ID: H2020-MSCA-IF-2017-793699
                Award ID: PT17/0009/0023–ISCIII-SGEFI/ERDF
                Categories
                Minireview
                AcademicSubjects/SCI01150
                Mini Review

                Molecular biology
                hybridization,whole-genome duplication,allopolyploidization,yeast,saccharomyces,candida

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