Mutation Accumulation in an Asexual Relative of Arabidopsis

Lovell, John T; Williamson, R.; Wright, Stephen I.; McKay, John; Sharbel, Timothy F.

doi:10.1371/journal.pgen.1006550

Cited by 64 publications

(64 citation statements)

References 32 publications

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“…6% recombinants per population, is sufficient to eliminate mutations in hexaploids via purifying selection (Hojsgaard & Hörandl, 2015;Hodac & al., subm.). Likewise, in apomictic Boechera, a more detailed genomic analysis revealed mutation accumulation in non-coding regions only, but not in conserved coding regions (Lovell & al., 2017). Selection for "a little bit of sex", especially in high TAXON 67 (6) • December 2018: 1066-1081 Hörandl • Classification of asexual organisms polyploids with their high mutation rates, might act against the establishment of long-term obligate asexual lineages (Hojsgaard & Hörandl, 2015).…”

Section: Adventitious Embryony: See Sporophytic Apomixismentioning

confidence: 99%

The classification of asexual organisms: Old myths, new facts, and a novel pluralistic approach

Hörandl

2018

TAXON

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Organisms reproducing via asexuality harbor a great diversity of lineages, morphotypes and ecotypes. However, classification of asexual taxa does not fit into contemporary species concepts, and hence the diversity of apomictic plant complexes is not well reflected in taxonomy. Plants reproducing via apomixis (i.e., asexual seed formation = agamospermy) exemplify the theoretical and practical problems of classification. Obligately asexual organisms do not form reproductive communities, but they do constitute ancestor-descendant lineages. From the conceptual side, evolutionary lineage concepts would fit best for species delimitation. Recent research showed that these lineages are not necessarily threatened by rapid extinction and do have persistence in time and space. Facultative sexuality and low levels of residual recombination counteract the accumulation of deleterious mutations due to the lack of recombination (Muller's ratchet). Apomictic lineages do have adaptive potential, which is demonstrated by the ability to occupy large distribution areas and to experience ecological niche shifts. The challenge for classification of asexual lineages, however, is to find operational criteria for species delimitation. Current practices of species delimitation can be grouped into four main principles: (1) the sexuals-first principle means that obligate sexual progenitor species are classified separately from their apomictic derivatives.(2) The all-in-one principle merges sexual progenitors and highly facultative apomictic derivatives into one species, whereby the apomicts often represent autopolyploids without differentiated phenotypes. (3) The cluster concept applies to allopolyploid complexes with facultative apomixis and a huge diversity of genotypes and morphotypes; here the main genetic clusters are treated as species. (4) Almost obligate apomictic lineages are being classified as agamospecies. The four principles reflect quite well evolutionary traits and diversity of lineages. Finally, a recommendation for a workflow is given, following this gradient from obligate sexuality to obligate apomixis.

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Section: Adventitious Embryony: See Sporophytic Apomixismentioning

confidence: 99%

The classification of asexual organisms: Old myths, new facts, and a novel pluralistic approach

Hörandl

2018

TAXON

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“…; Lovell et al. ) taxa. While these results represent important steps toward understanding the genomic consequences of asexuality, the evolutionary mechanisms (e.g., deleterious mutation accumulation versus mitonuclear coevolution) underlying these observations remain unclear, in large part because the extent to which accumulated mutations are actually deleterious in asexuals has not been evaluated.…”

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confidence: 99%

“…The prediction that asexual lineages should experience a higher rate of accumulation of harmful mutations has found support from animal (Neiman et al 2010;Henry et al 2012) and plant (Voigt-Zielinski et al 2012;Hollister et al 2015;Lovell et al 2017) taxa. While these results represent important steps toward understanding the genomic consequences of asexuality, the evolutionary mechanisms (e.g., deleterious mutation accumulation versus mitonuclear coevolution) underlying these observations remain unclear, in large part because the extent to which accumulated mutations are actually deleterious in asexuals has not been evaluated.…”

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confidence: 99%

Radical amino acid mutations persist longer in the absence of sex

et al. 2018

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Harmful mutations are ubiquitous and inevitable, and the rate at which these mutations are removed from populations is a critical determinant of evolutionary fate. Closely related sexual and asexual taxa provide a particularly powerful setting to study deleterious mutation elimination because sexual reproduction should facilitate mutational clearance by reducing selective interference between sites and by allowing the production of offspring with different mutational complements than their parents. Here, we compared the rate of removal of conservative (i.e., similar biochemical properties) and radical (i.e., distinct biochemical properties) nonsynonymous mutations from mitochondrial genomes of sexual versus asexual Potamopyrgus antipodarum, a New Zealand freshwater snail characterized by coexisting and ecologically similar sexual and asexual lineages. Our analyses revealed that radical nonsynonymous mutations are cleared at higher rates than conservative changes and that sexual lineages eliminate radical changes more rapidly than asexual counterparts. These results are consistent with reduced efficacy of purifying selection in asexual lineages allowing harmful mutations to remain polymorphic longer than in sexual lineages. Together, these data illuminate some of the population-level processes contributing to mitochondrial mutation accumulation and suggest that mutation accumulation could influence the outcome of competition between sexual and asexual lineages.

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“…It can be hypothesized that global deregulations of gene expression varies due to the different hybrid origins of apomixis in Boechera (Sharbel and Mitchell-Olds, 2001;Koch et al, 2003;Dobes et al, 2004a;Dobes et al, 2004b;Kiefer et al, 2009;Kiefer and Koch, 2012;Lovell et al, 2013). Furthermore, recent studies supported higher rates of mutation accumulation in apomictic as compared to sexual Boechera (Lovell et al, 2017) Still, if broad deregulations of gene expression due to genomic effects are causative or only correlated with apomixis is to date not fully understood. The rather small number of DEGs identified here, however suggests a small number of genes to be sufficient to mediate the switch from sexual reproduction to apomixis.…”

Section: Commonly and Differentially Regulated Genes In Apomictic Andmentioning

confidence: 99%

Differential gene expression indicates involvement of F-box proteins and E3 ligases in sexualversusapomictic germline specification inBoechera

Zühl¹,

Ibberson²,

Schmidt³

2018

Preprint

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Author contributionAS conceived the project. AS and LZ planned the experiments. LZ conducted the experiments with support of DI and AS. LZ conducted the data analysis. LZ, AS, and DI interpreted the data.LZ and AS wrote the manuscript. All authors approved the manuscript. One sentence summaryA comprehensive tissue type-specific transcriptional analysis using laser-assisted microdissection combined with RNA-Seq identifies 45 genes consistently differentially expressed during germline specification in different sexual versus apomictic Boechera accessions, indicating roles of protein degradation related to cell cycle, transcriptional and posttranscriptional regulatory processes, and stress response for apomixis. ABSTRACTGermline specification is the first step during sexual and apomictic plant reproduction. This takes place in a specialized domain of the reproductive flower tissues, the nucellus of the ovule.In each case, a sporophytic cell is determined to initiate germline development. These cells, the megaspore mother cell (MMC) or apomictic initial cell (AIC) in sexual plants and apomicts, respectively, differ in their developmental fate. While the MMC undergoes meiosis, the AIC aborts or omits meiosis to form the female gametophyte. Although these distinct developmental processes have long been described, little is known about the gene regulatory basis involved.To elucidate gene regulatory networks underlying sexual and apomictic germline specification, we conducted tissue-specific transcriptional profiling using laser-assisted microdissection and RNA-Seq. We compared the transcriptomes of the nucellar tissues harbouring the MMC or AIC between different accessions of Boechera. The six accessions we used represented four species and two ploidy levels, allowing us to distinguish between differences in gene expression caused by the genetic background or the reproductive mode.Comparative data analysis revealed widely overlapping gene expression patterns in apomictic versus sexual Boechera accessions. Nevertheless, 45 significantly differentially expressed genes were identified, which potentially play a role for determination of sexual versus apomictic reproductive mode. Interestingly, based on annotations, these include F-box proteins and E3 ligases that might relate to genes previously described as regulators important for sexual or apomictic reproduction. Thus, our findings provide new insight into the transcriptional basis of sexual and apomictic germline specification.

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Mutation Accumulation in an Asexual Relative of Arabidopsis

Cited by 64 publications

References 32 publications

The classification of asexual organisms: Old myths, new facts, and a novel pluralistic approach

The classification of asexual organisms: Old myths, new facts, and a novel pluralistic approach

Radical amino acid mutations persist longer in the absence of sex

Differential gene expression indicates involvement of F-box proteins and E3 ligases in sexualversusapomictic germline specification inBoechera

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