Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts

Scannell, Devin R.; Byrne, Kevin; Gordon, Jonathan; Wong, Simon; Wolfe, Kenneth H.

doi:10.1038/nature04562

Cited by 397 publications

(385 citation statements)

References 25 publications

(23 reference statements)

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“…The fates of thousands of duplicated genes are correlated (r ¼ 0.6) in the two species . Postduplication convergence of gene copy number is also found in divergent yeasts (Scannell et al, 2006), and genes from the same metabolic pathway show similar retention/loss trends in Paramecium . Repeated restoration of certain genes to singleton status at a greater-than random frequency suggests that an underlying set of principles of molecular evolution may contribute to the fates of gene and genome duplications .…”

Section: Introductionmentioning

confidence: 80%

Gene copy number evolution during tetraploid cotton radiation

et al. 2010

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Section: Introductionmentioning

confidence: 80%

Gene copy number evolution during tetraploid cotton radiation

et al. 2010

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“…Indeed, after a genome duplication, many gene losses occur independently in different populations. This process is therefore expected to lead rapidly to reproductive isolation by Dobzhansky-Muller incompatibility 32 . Interestingly, species of the P. aurelia complex are extremely similar both morphologically and in terms of ecological environment (and hence they were initially thought to correspond to a single species 31 ).…”

Section: Genome Duplication and Speciationmentioning

confidence: 99%

“…Interestingly, species of the P. aurelia complex are extremely similar both morphologically and in terms of ecological environment (and hence they were initially thought to correspond to a single species 31 ). We therefore propose that the explosion of speciation events that gave rise to the P. aurelia complex is not the result of adaptative evolutionary events (for example the colonization of new ecological niches) but the neutral consequence of the genome duplication 32 .…”

Section: Genome Duplication and Speciationmentioning

confidence: 99%

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Aury

Jaillon

Duret

et al. 2006

Nature

760

836

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The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.Ciliates are unique among unicellular organisms in that they separate germline and somatic functions 1 . Each cell harbours two kinds of nucleus, namely silent diploid micronuclei and highly polyploid macronuclei. The latter are unusual in that they contain an extensively rearranged genome streamlined for expression and divide by a non-mitotic process. Only micronuclei undergo meiosis to perpetuate genetic information; the macronuclei are lost at each sexual generation and develop anew from the micronuclear lineage.In Paramecium the exact number of micronuclear chromosomes (more than 50) and the structures of their centromeres and telomeres remain unknown. During macronuclear development, these chromosomes are amplified to about 800 copies and undergo two types of DNA elimination event. Tens of thousand of short, unique copy elements (internal eliminated sequences) are removed by a precise mechanism that leads to the reconstitution of functional genes 2 .Transposable elements and other repeated sequences are removed by an imprecise mechanism leading either to chromosome fragmentation and de novo telomere addition or to variable internal deletions 3 . These rearrangements occur after a few rounds of endoreplication, leading to some heterogeneity in the sequences abutting the imprecisely eliminated regions 3 . The sizes of the resulting, acentric macronuclear chromosomes range from 50-1,000 kilobases (kb) as measured by pulsed-field gel electrophoresis. Because the sexual process of autogamy results in an entirely homozygous genotype 4 , the macronuclear DNA that was sequenced was genetically homogeneous.The Paramecium genome sequence The Paramecium macronuclear genome sequence was established with the use of a whole-genome shotgun and assembly strategy. Paired-end sequencing of plasmid and bacterial artificial chromosome (BAC) clones provided a coverage of 13 genome equivalents (Supplementary Table S1). We assembled the sequence reads with Arachne 5 in 1,907 contigs connected in 697 scaffolds of size greater than 2 kb, giving a total coverage of 72...

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“…These allopolyploid strains probably experienced their respective interspecific hybridization events on the order of mere hundreds of years ago-corresponding to only a few thousand generations, assuming 50 generations/yr for lager brewing conditions; thus, we are most likely observing among the very earliest genome rearrangements that occur after an interspecific hybridization event. It is possible that we are observing the early stages of genome loss and shuffling after a secondary whole-genome duplication event (i.e., between species that have already undergone genome duplication), and that the loss of much of the S. cerevisiae genome in the Group 1 strains could be analogous to the proposed rapid and precipitous gene loss that occurred in the ancestor of the Saccharomyces clade immediately after it experienced its (presumably) first whole-genome duplication (Byrnes et al 2006;Scannell et al 2006). Note, however, that Scannell et al (2006) and Byrnes et al (2006) predict that the post-duplication gene loss would be passive and involve single genes scattered individually across the genome, whereas we see mostly losses of large contiguous regions.…”

Section: Allopolyploidy As a Window Onto Genome Duplication And Subsementioning

confidence: 99%

“…As described in more detail below, S. pastorianus has been shown to be a hybrid organism, and it is likely that lager yeast arose by "instantaneous speciation" due to an interspecific hybridization event (Martini and Kurztman 1985;Martini and Martini 1987) that occurred during these selective growth conditions. Not only is this mechanism known to be common in angiosperm speciation (Hegarty and Hiscock 2005), but interspecific hybridization (or "allopolyploidy") among the closely related sensu stricto Saccharomyces yeast species is known to occur in both industrial and natural settings (Masneuf et al 1998;Groth et al 1999;de Barros Lopes et al 2002;Liti et al 2005;Gonzalez et al 2007Gonzalez et al , 2008Lopandic et al 2007), and indeed may also have been the mechanism leading to the original whole-genome duplication in the ancestor of the Saccharomyces clade (Scannell et al 2006).…”

mentioning

confidence: 99%

Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus

Dunn¹,

Sherlock²

2008

Genome Res.

258

391

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Inter-specific hybridization leading to abrupt speciation is a well-known, common mechanism in angiosperm evolution; only recently, however, have similar hybridization and speciation mechanisms been documented to occur frequently among the closely related group of sensu stricto Saccharomyces yeasts. The economically important lager beer yeast Saccharomyces pastorianus is such a hybrid, formed by the union of Saccharomyces cerevisiae and Saccharomyces bayanus-related yeasts; efforts to understand its complex genome, searching for both biological and brewing-related insights, have been underway since its hybrid nature was first discovered. It had been generally thought that a single hybridization event resulted in a unique S. pastorianus species, but it has been recently postulated that there have been two or more hybridization events. Here, we show that there may have been two independent origins of S. pastorianus strains, and that each independent group—defined by characteristic genome rearrangements, copy number variations, ploidy differences, and DNA sequence polymorphisms—is correlated with specific breweries and/or geographic locations. Finally, by reconstructing common ancestral genomes via array-CGH data analysis and by comparing representative DNA sequences of the S. pastorianus strains with those of many different S. cerevisiae isolates, we have determined that the most likely S. cerevisiae ancestral parent for each of the independent S. pastorianus groups was an ale yeast, with different, but closely related ale strains contributing to each group’s parentage.

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Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts

Cited by 397 publications

References 25 publications

Gene copy number evolution during tetraploid cotton radiation

Gene copy number evolution during tetraploid cotton radiation

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus

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