The evolution of haploidy and diploidy

Otto, Sarah P.; Gerstein, Aleeza C.

doi:10.1016/j.cub.2008.09.039

Cited by 106 publications

(107 citation statements)

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“…This study further emphasizes the role of mitotic recombination in modifying and/or altering phenotypes and diversifying diploid descendants during clonal reproduction without having to go through a sexual cycle (Mandegar and Otto 2007;Otto and Gerstein 2008). It is possible that we could detect additional traits, beyond MMS and thermosensitivity, if tested under appropriate selective conditions.…”

Section: Loss Of Heterozygosity In Candida Albicansmentioning

confidence: 65%

Phenotypic Consequences of a Spontaneous Loss of Heterozygosity in a Common Laboratory Strain of Candida albicans

et al. 2016

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By testing the susceptibility to DNA damaging agents of several Candida albicans mutant strains derived from the commonly used laboratory strain, CAI4, we uncovered sensitivity to methyl methanesulfonate (MMS) in CAI4 and its derivatives, but not in CAF2-1. This sensitivity is not a result of URA3 disruption because the phenotype was not restored after URA3 reintroduction. Rather, we found that homozygosis of a short region of chromosome 3R (Chr3R), which is naturally heterozygous in the MMS-resistant-related strains CAF4-2 and CAF2-1, confers MMS sensitivity and modulates growth polarization in response to MMS. Furthermore, induction of homozygosity in this region in CAF2-1 or CAF4-2 resulted in MMS sensitivity. We identified 11 genes by SNP/comparative genomic hybridization containing only the a alleles in all the MMS-sensitive strains. Four candidate genes, SNF5, POL1, orf19.5854.1, and MBP1, were analyzed by generating hemizygous configurations in CAF2-1 and CAF4-2 for each allele of all four genes. Only hemizygous MBP1a/mbp1b::SAT1-FLIP strains became MMS sensitive, indicating that MBP1a in the homo-or hemizygosis state was sufficient to account for the MMS-sensitive phenotype. In yeast, Mbp1 regulates G1/S genes involved in DNA repair. A second region of homozygosis on Chr2L increased MMS sensitivity in CAI4 (Chr3R homozygous) but not CAF4-2 (Chr3R heterozygous). This is the first example of sign epistasis in C. albicans.KEYWORDS Candida albicans; LOH; MMS susceptibility; MBP1; growth polarization T HE opportunistic fungal pathogen Candida albicans is often isolated as a highly heterozygous diploid; the genome of the reference strain SC5314 has 67,500 single nucleotide polymorphisms (SNPs) (Jones et al. 2004;Braun et al. 2005;Muzzey et al. 2013). SNPs found within regulatory regions can affect transcription levels between the alleles (Staib et al. 2002). Even synonymous SNPs residing in open reading frames (ORFS) can result in differences in the rate and efficiency of messenger RNA (mRNA) translation since poorly used codons delay protein synthesis. These delays may lead to misfolding of the nascent protein or formation of mRNA secondary structures (reviewed in Larriba and Calderone 2008). Recent genome-wide analysis of cis elements on gene expression showed that allele-specific effects are often due to mRNA levels and/or translation efficiency (Muzzey et al. 2014).While the majority of SNPs reside in intergenic regions, more than half of open reading frames contain one or more SNPs. The vast majority (78%) of these are nonsynonymous, implying that a significant fraction of ORFs encode proteins that differ in one or more amino acids (Jones et al. 2004) that may affect crucial properties. Nonconservative amino acid substitutions within an enzyme's catalytic domain could result in an inactive allele (Gómez-Raja et al. 2008). However, many SNPs will cause only minor or insignificant alterations in protein properties.Mitotic recombination or less frequently, chromosome truncation or loss, will reveal ...

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Section: Loss Of Heterozygosity In Candida Albicansmentioning

confidence: 65%

Phenotypic Consequences of a Spontaneous Loss of Heterozygosity in a Common Laboratory Strain of Candida albicans

et al. 2016

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“…Note that this diversity advantage of diploids is different in kind from the advantages based on the differences in number of chromosomes and the efficacy of selection in haploids and diploids discussed previously (14)(15)(16). The characteristics of the genetic variation in diploid populations depend strongly on the speed of environmental change.…”

Section: Resultsmentioning

confidence: 82%

“…In contrast, once mutations of large enough size are available, diploids start reaping the benefits of the larger space of adaptive mutants available to them. In this case, adaptive mutations will invade at a higher rate in diploids than in haploids, even after controlling for the difference in mutation rate that results from a diploid population having twice as many chromosomes as a haploid population of equal size (14).…”

Section: Resultsmentioning

confidence: 99%

Heterozygote advantage as a natural consequence of adaptation in diploids

Sellis¹,

Callahan

Petrov³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

181

200

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Molecular adaptation is typically assumed to proceed by sequential fixation of beneficial mutations. In diploids, this picture presupposes that for most adaptive mutations, the homozygotes have a higher fitness than the heterozygotes. Here, we show that contrary to this expectation, a substantial proportion of adaptive mutations should display heterozygote advantage. This feature of adaptation in diploids emerges naturally from the primary importance of the fitness of heterozygotes for the invasion of new adaptive mutations. We formalize this result in the framework of Fisher's influential geometric model of adaptation. We find that in diploids, adaptation should often proceed through a succession of short-lived balanced states that maintain substantially higher levels of phenotypic and fitness variation in the population compared with classic adaptive walks. In fast-changing environments, this variation produces a diversity advantage that allows diploids to remain better adapted compared with haploids despite the disadvantage associated with the presence of unfit homozygotes. The short-lived balanced states arising during adaptive walks should be mostly invisible to current scans for long-term balancing selection. Instead, they should leave signatures of incomplete selective sweeps, which do appear to be common in many species. Our results also raise the possibility that balancing selection, as a natural consequence of frequent adaptation, might play a more prominent role among the forces maintaining genetic variation than is commonly recognized.A daptation by natural selection is the key process responsible for the fit between organisms and their environments. The invasion of new adaptive mutations is an essential component of this process that fundamentally differs between haploid and diploid populations. In diploids, while a new mutation is still rare, natural selection acts primarily on the mutant heterozygote (1). As a result, only those adaptive mutations that confer a fitness advantage as heterozygotes have an appreciable chance of invading the population ("Haldane's sieve"). However, if the heterozygote of an invading adaptive mutation is fitter than the mutant homozygote, the mutation will not be driven to fixation but, instead, maintained at an intermediate, balanced frequency.We argue that heterozygote advantage should be very common during adaptation in diploids if selection is stabilizing and at least some mutations are large enough to overshoot the optimum. Consider, for example, adaptation through changes in gene expression (Fig. 1A), which is an important, if not the dominant, mechanism of adaptation (2). Here, mutations of small effect (Fig. 1B) will be adaptive when they modify expression in the adaptive direction whether the organism is haploid or diploid. However, mutations of large effect (Fig. 1C) can be nonadaptive in haploids, because they overshoot the optimum, yet be adaptive in diploids, because their phenotypic effect is moderated when heterozygous. These mutations will have heterozy...

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“…For example, population genetic analyses suggest that the equilibrium load of harmful mutations will increase with ploidy level (Otto and Whitton, 2000;Otto and Gerstein, 2009). Data from a variety of plant and animal taxa also suggest that polyploid individuals generally develop more slowly than their diploid counterparts (Cavalier-Smith, 1978;Levin, 1983).…”

Section: A Disadvantage Of Polyploidy?mentioning

confidence: 99%

Can resource costs of polyploidy provide an advantage to sex?

2012

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The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.

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The evolution of haploidy and diploidy

Cited by 106 publications

References 12 publications

Phenotypic Consequences of a Spontaneous Loss of Heterozygosity in a Common Laboratory Strain of Candida albicans

Phenotypic Consequences of a Spontaneous Loss of Heterozygosity in a Common Laboratory Strain of Candida albicans

Heterozygote advantage as a natural consequence of adaptation in diploids

Can resource costs of polyploidy provide an advantage to sex?

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