Aborting meiosis overcomes hybrid sterility

AbstractHybrids between species or diverged lineages contain fundamentally novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends. Here, we explored to what extent and how an aborted meiosis followed by a return-to-growth (RTG) promotes recombination across a panel of 20 yeast diploid backgrounds with different genomic structures and levels of sterility. Genome analyses of 284 clones revealed that RTG promoted recombination and generated extensive regions of loss-of-heterozygosity in sterile hybrids with either a defective meiosis or a heavily rearranged karyotype, whereas RTG recombination was reduced by high sequence divergence between parental subgenomes. The RTG recombination preferentially occurred in regions with local sequence homology and in meiotic recombination hotspots. The loss-of-heterozygosity had a profound impact on sexual and asexual fitness, and enabled genetic mapping of phenotypic differences in sterile lineages where linkage or association analyses failed. We propose that RTG gives sterile hybrids access to a natural route for genome recombination and adaptation.One sentence summaryAborting meiosis followed by a return to mitotic growth promotes evolution by genome wide-recombination in sterile yeast hybrids.

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Aborting meiosis allows recombination in sterile diploid yeast hybrids

Nature Communications ◽

10.1038/s41467-021-26883-8 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Simone Mozzachiodi ◽

Lorenzo Tattini ◽

Agnes Llored ◽

Agurtzane Irizar ◽

Neža Škofljanc ◽

...

Keyword(s):

Loss Of Heterozygosity ◽

Meiotic Recombination ◽

Sequence Divergence ◽

Phenotypic Differences ◽

Recombination Hotspots ◽

Genome Recombination ◽

High Sequence Divergence ◽

Genome Analyses ◽

Meiotic Recombination Hotspots ◽

Sterile Hybrids

AbstractHybrids between diverged lineages contain novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends. Here, we explore to what extent an aborted meiosis followed by a return-to-growth (RTG) promotes recombination across a panel of 20 Saccharomyces cerevisiae and S. paradoxus diploid hybrids with different genomic structures and levels of sterility. Genome analyses of 275 clones reveal that RTG promotes recombination and generates extensive regions of loss-of-heterozygosity in sterile hybrids with either a defective meiosis or a heavily rearranged karyotype, whereas RTG recombination is reduced by high sequence divergence between parental subgenomes. The RTG recombination preferentially arises in regions with low local heterozygosity and near meiotic recombination hotspots. The loss-of-heterozygosity has a profound impact on sexual and asexual fitness, and enables genetic mapping of phenotypic differences in sterile lineages where linkage analysis would fail. We propose that RTG gives sterile yeast hybrids access to a natural route for genome recombination and adaptation.

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Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

eLife ◽

10.7554/elife.35468 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 18

Author(s):

Colin D Meiklejohn ◽

Emily L Landeen ◽

Kathleen E Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Sequence Divergence ◽

Meiotic Drive ◽

Hybrid Male ◽

Local Sequence

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that a known drive element recently migrated between species and, rather than contributing to interspecific divergence, caused a strong reduction in local sequence divergence, undermining the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

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A high-resolution map of non-crossover events reveals impacts of genetic diversity on mammalian meiotic recombination

10.1101/428987 ◽

2018 ◽

Cited By ~ 5

Author(s):

Ran Li ◽

Emmanuelle Bitoun ◽

Nicolas Altemose ◽

Robert W Davies ◽

Benjamin Davies ◽

...

Keyword(s):

Genetic Diversity ◽

Meiotic Recombination ◽

Sequence Divergence ◽

Dna Double Strand Breaks ◽

Strand Breaks ◽

High Sequence Divergence ◽

Local Sequence ◽

High Resolution Map ◽

The Impact ◽

Hybrid Mice

During meiotic recombination in most mammals, hundreds of programmed DNA Double-Strand Breaks (DSBs) occur across all chromosomes in each cell at sites bound by the protein PRDM9. Faithful DSB repair using the homologous chromosome is essential for fertility, yielding either non-crossovers, which are frequent but difficult to detect, or crossovers. In certain hybrid mice, high sequence divergence causes PRDM9 to bind each homologue at different sites, 'asymmetrically', and these mice exhibit meiotic failure and infertility, by unknown mechanisms. To investigate the impact of local sequence divergence on recombination, we intercrossed two mouse subspecies over five generations and deep-sequenced 119 offspring, whose high heterozygosity allowed detection of thousands of crossover and non-crossover events with unprecedented power and spatial resolution. Both crossovers and non-crossovers are strongly depleted at individual asymmetric sites, revealing that PRDM9 not only positions DSBs but also promotes their homologous repair by binding to the unbroken homologue at each site. Unexpectedly, we found that non-crossovers containing multiple mismatches repair by a different mechanism than single-mismatch sites, which undergo GC-biased gene conversion. These results demonstrate that local genetic diversity profoundly alters meiotic repair pathway decisions via at least two distinct mechanisms, impacting genome evolution and Prdm9-related hybrid infertility.

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Genome Analyses of Three Strains of Rhodobacter sphaeroides: Evidence of Rapid Evolution of Chromosome II

Journal of Bacteriology ◽

10.1128/jb.01498-06 ◽

2006 ◽

Vol 189 (5) ◽

pp. 1914-1921 ◽

Cited By ~ 47

Author(s):

M. Choudhary ◽

Xie Zanhua ◽

Y. X. Fu ◽

S. Kaplan

Keyword(s):

Rhodobacter Sphaeroides ◽

Dna Sequences ◽

Rapid Evolution ◽

Size Variation ◽

Sequence Divergence ◽

High Sequence Divergence ◽

Different Strains ◽

Genome Analyses ◽

Chromosome Ii ◽

Chromosomal Sequences

ABSTRACT Three strains of Rhodobacter sphaeroides of diverse origin have been under investigation in our laboratory for their genome complexities, including the presence of multiple chromosomes and the distribution of essential genes within their genomes. The genome of R. sphaeroides 2.4.1 has been completely sequenced and fully annotated, and now two additional strains (ATCC 17019 and ATCC 17025) of R. sphaeroides have been sequenced. Thus, genome comparisons have become a useful approach in determining the evolutionary relationships among different strains of R. sphaeroides. In this study, the concatenated chromosomal sequences from the three strains of R. sphaeroides were aligned, using Mauve, to examine the extent of shared DNA regions and the degree of relatedness among their chromosome-specific DNA sequences. In addition, the exact intra- and interchromosomal DNA duplications were analyzed using Mummer. Genome analyses employing these two independent approaches revealed that strain ATCC 17025 diverged considerably from the other two strains, 2.4.1 and ATCC 17029, and that the two latter strains are more closely related to one another. Results further demonstrated that chromosome II (CII)-specific DNA sequences of R. sphaeroides have rapidly evolved, while CI-specific DNA sequences have remained highly conserved. Aside from the size variation of CII of R. sphaeroides, variation in sequence lengths of the CII-shared DNA regions and their high sequence divergence among strains of R. sphaeroides suggest the involvement of CII in the evolution of strain-specific genomic rearrangements, perhaps requiring strains to adapt in specialized niches.

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Structural characterization and duplication modes of pseudogenes in plants

Scientific Reports ◽

10.1038/s41598-021-84778-6 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Flavia Mascagni ◽

Gabriele Usai ◽

Andrea Cavallini ◽

Andrea Porceddu

Keyword(s):

Evolutionary Rate ◽

Populus Trichocarpa ◽

Sequence Divergence ◽

Strand Break ◽

Whole Genome ◽

Flanking Sequence ◽

Plant Genomes ◽

High Sequence Divergence ◽

Flanking Regions

AbstractWe identified and characterized the pseudogene complements of five plant species: four dicots (Arabidopsis thaliana, Vitis vinifera, Populus trichocarpa and Phaseolus vulgaris) and one monocot (Oryza sativa). Retroposition was considered of modest importance for pseudogene formation in all investigated species except V. vinifera, which showed an unusually high number of retro-pseudogenes in non coding genic regions. By using a pipeline for the classification of sequence duplicates in plant genomes, we compared the relative importance of whole genome, tandem, proximal, transposed and dispersed duplication modes in the pseudo and functional gene complements. Pseudogenes showed higher tendencies than functional genes to genomic dispersion. Dispersed pseudogenes were prevalently fragmented and showed high sequence divergence at flanking regions. On the contrary, those deriving from whole genome duplication were proportionally less than expected based on observations on functional loci and showed higher levels of flanking sequence conservation than dispersed pseudogenes. Pseudogenes deriving from tandem and proximal duplications were in excess compared to functional loci, probably reflecting the high evolutionary rate associated with these duplication modes in plant genomes. These data are compatible with high rates of sequence turnover at neutral sites and double strand break repairs mediated duplication mechanisms.

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Strong genetic subdivision in Leptobrachium hendricksoni (Anura: Megophryidae) in Southeast Asia

Amphibia-Reptilia ◽

10.1163/15685381-17000102 ◽

2018 ◽

Vol 39 (1) ◽

pp. 99-111

Author(s):

Gordon Draškić ◽

Sansareeya Wangkulangkul ◽

Iñigo Martínez-Solano ◽

Judit Vörös

Keyword(s):

Southeast Asia ◽

Sequence Divergence ◽

Population Divergence ◽

Geological History ◽

Base Pairs ◽

Sea Levels ◽

Phylogenetic Studies ◽

High Sequence Divergence ◽

Southern Thailand ◽

Rising Sea Levels

Many biodiversity hotspots are located in areas with a complex geological history, like Southeast Asia, where species diversity may still be far underestimated, especially in morphologically conservative groups like amphibians. Recent phylogenetic studies on the frog genusLeptobrachiumfrom Southeast Asia revealed the presence of deeply divergent mitochondrial clades inLeptobrachium hendricksonifrom Malaysia and Sumatra but populations from Thailand have not been studied so far. In this study, we re-evaluate patterns of intraspecific genetic diversity inL. hendricksonibased on the analysis of combined sequences of mitochondrial 12S and 16S genes (1310 base pairs) including for the first time samples from southern Thailand. Thai populations ofL. hendricksoniformed a distinct clade with respect to populations from central and southern Malaysia and Sumatra. High sequence divergence between lineages from Thailand, Malaysia and Sumatra suggests the possible presence of cryptic species inL. hendricksoni. Divergence withinL. hendricksonidates back to the late Miocene, around 6 Mya, when lineages from Thailand, north Malaysia and Sumatra split from a lineage in south Malaysia, at about the same time as rising sea levels isolated the Thai-Malay peninsula. Subsequent splits took place later in the Pliocene, around 4.5 and 2.6 Mya. Our results highlight the role of geological history in promoting population divergence and speciation.

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Parthenogenesis as a Solution to Hybrid Sterility: The Mechanistic Basis of Meiotic Distortions in Clonal and Sterile Hybrids

Genetics ◽

10.1534/genetics.119.302988 ◽

2020 ◽

Vol 215 (4) ◽

pp. 975-987 ◽

Cited By ~ 1

Author(s):

Dmitrij Dedukh ◽

Zuzana Majtánová ◽

Anatolie Marta ◽

Martin Pšenička ◽

Jan Kotusz ◽

...

Keyword(s):

Gene Flow ◽

Molecular Mechanisms ◽

Hybrid Sterility ◽

Triploid Hybrid ◽

Interspecific Gene Flow ◽

Homologous Chromosomes ◽

Specific Manner ◽

Bivalent Formation ◽

Mechanistic Basis ◽

Sterile Hybrids

Hybrid sterility is a hallmark of speciation, but the underlying molecular mechanisms remain poorly understood. Here, we report that speciation may regularly proceed through a stage at which gene flow is completely interrupted, but hybrid sterility occurs only in male hybrids whereas female hybrids reproduce asexually. We analyzed gametogenic pathways in hybrids between the fish species Cobitis elongatoides and C. taenia, and revealed that male hybrids were sterile owing to extensive asynapsis and crossover reduction among heterospecific chromosomal pairs in their gametes, which was subsequently followed by apoptosis. We found that polyploidization allowed pairing between homologous chromosomes and therefore partially rescued the bivalent formation and crossover rates in triploid hybrid males. However, it was not sufficient to overcome sterility. In contrast, both diploid and triploid hybrid females exhibited premeiotic genome endoreplication, thereby ensuring proper bivalent formation between identical chromosomal copies. This endoreplication ultimately restored female fertility but it simultaneously resulted in the obligate production of clonal gametes, preventing any interspecific gene flow. In conclusion, we demonstrate that the emergence of asexuality can remedy hybrid sterility in a sex-specific manner and contributes to the speciation process.

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Modulation of Prdm9-controlled meiotic chromosome asynapsis overrides hybrid sterility in mice

eLife ◽

10.7554/elife.34282 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 27

Author(s):

Sona Gregorova ◽

Vaclav Gergelits ◽

Irena Chvatalova ◽

Tanmoy Bhattacharyya ◽

Barbora Valiskova ◽

...

Keyword(s):

Meiotic Chromosome ◽

Hybrid Sterility ◽

Double Strand Breaks ◽

Dna Double Strand Breaks ◽

Strand Breaks ◽

Recombination Hotspots ◽

Chromosome Synapsis ◽

Reproductive Isolation Mechanisms ◽

Meiotic Recombination Hotspots ◽

Isolation Mechanisms

Hybrid sterility is one of the reproductive isolation mechanisms leading to speciation. Prdm9, the only known vertebrate hybrid-sterility gene, causes failure of meiotic chromosome synapsis and infertility in male hybrids that are the offspring of two mouse subspecies. Within species, Prdm9 determines the sites of programmed DNA double-strand breaks (DSBs) and meiotic recombination hotspots. To investigate the relation between Prdm9-controlled meiotic arrest and asynapsis, we inserted random stretches of consubspecific homology on several autosomal pairs in sterile hybrids, and analyzed their ability to form synaptonemal complexes and to rescue male fertility. Twenty-seven or more megabases of consubspecific (belonging to the same subspecies) homology fully restored synapsis in a given autosomal pair, and we predicted that two or more DSBs within symmetric hotspots per chromosome are necessary for successful meiosis. We hypothesize that impaired recombination between evolutionarily diverged chromosomes could function as one of the mechanisms of hybrid sterility occurring in various sexually reproducing species.

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Comparative Genomics ofCryptosporidium

International Journal of Genomics ◽

10.1155/2013/832756 ◽

2013 ◽

Vol 2013 ◽

pp. 1-8 ◽

Cited By ~ 17

Author(s):

Aurélien J. Mazurie ◽

João M. Alves ◽

Luiz S. Ozaki ◽

Shiguo Zhou ◽

David C. Schwartz ◽

...

Keyword(s):

Genome Organization ◽

Distinct Species ◽

Genome Sequences ◽

Cryptosporidium Hominis ◽

Gene Deletions ◽

Structural Alterations ◽

Phenotypic Differences ◽

Apicomplexan Parasites ◽

Sequence Identity ◽

Local Sequence

Until recently, the apicomplexan parasites,Cryptosporidium hominisandC. parvum, were considered the same species. However, the two parasites, now considered distinct species, exhibit significant differences in host range, infectivity, and pathogenicity, and their sequenced genomes exhibit only 95–97% identity. The availability of the complete genome sequences of these organisms provides the potential to identify the genetic variations that are responsible for the phenotypic differences between the two parasites. We compared the genome organization and structure, gene composition, the metabolic and other pathways, and the local sequence identity between the genes of these twoCryptosporidiumspecies. Our observations show that the phenotypic differences betweenC. hominisandC. parvumare not due to gross genome rearrangements, structural alterations, gene deletions or insertions, metabolic capabilities, or other obvious genomic alterations. Rather, the results indicate that these genomes exhibit a remarkable structural and compositional conservation and suggest that the phenotypic differences observed are due to subtle variations in the sequences of proteins that act at the interface between the parasite and its host.

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