Translocations of Chromosome End-Segments and Facultative Heterochromatin Promote Meiotic Ring Formation in Evening Primroses

Golczyk, Hieronim; Massouh, Amid; Greiner, Stephan

doi:10.1105/tpc.114.122655

Cited by 43 publications

(41 citation statements)

References 53 publications

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“…Our analyses of the karyotypes and oocyte meiotic configurations (Supplementary Figs 1 and 3, and data not shown) rule out the classic multi-chromosome ring mechanism (that is, translocation heterozygosity) discovered in Oenothera 19 . However, three other potential molecular mechanisms remain, each of which involves two alleles present in the trans configuration on two haplotypes.…”

Section: Resultsmentioning

confidence: 59%

Widespread maintenance of genome heterozygosity in Schmidtea mediterranea

et al. 2016

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Loss of heterozygosity through inbreeding or mitotic errors leads to reductions in progeny survival and fertility. Loss of heterozygosity is particularly exacerbated in geographically isolated populations, which are prone to inbreeding depression and faster rates of extinction. The regenerative capacities of the hermaphroditic biotype of the planarian Schmidtea mediterranea allowed us to perform a systematic genetic test of Mendelian segregation and study the loss of heterozygosity in the Spiralian superclade in general and planarians in particular. We discovered that ~300 Mb (~37.5%) of the genome retains heterozygosity even after ten generations of inbreeding, and show that these chromosomal regions have low diversity and recombination rates in wild populations. Our genetic and genomic analyses establish S. mediterranea as a genetically tractable system. The research also opens the door to study the evolutionary basis of non-Mendelian mechanisms, the adaptive advantages of chromosome structural heterozygotes and their potential relationship to the robust regenerative capacities of planarians.

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Section: Resultsmentioning

confidence: 59%

Widespread maintenance of genome heterozygosity in Schmidtea mediterranea

et al. 2016

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“…The distribution of differences within each region and the locations of individual genes are shown in Figure S1 and Figure S2. meiotic segregation and sexual reproduction might nevertheless occur is suggested by an atypical form of meiosis known in some species of the genus Oenothera and in certain other plants (Cleland 1972;Holsinger and Ellstrand 1984;Golczyk 2011;Rauwolf et al 2011;Golczyk et al 2014). In these plants and perhaps in some animals (Chinnappa and Victor 1979;Gross et al 2009;Schneider et al 2009), instead of synapsing side by side, chromosomes join end to end to form rings in which paternal and maternal chromosomes alternate.…”

Section: Oenothera-like Meiosismentioning

confidence: 99%

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

et al. 2015

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Rotifers of Class Bdelloidea are common freshwater invertebrates of ancient origin whose apparent asexuality has posed a challenge to the view that sexual reproduction is essential for long-term evolutionary success in eukaryotes and to hypotheses for the advantage of sex. The possibility nevertheless exists that bdelloids reproduce sexually under unknown or inadequately investigated conditions. Although certain methods of population genetics offer definitive means for detecting infrequent or atypical sex, they have not previously been applied to bdelloid rotifers. We conducted such a test with bdelloids belonging to a mitochondrial clade of Macrotrachela quadricornifera. This revealed a striking pattern of allele sharing consistent with sexual reproduction and with meiosis of an atypical sort, in which segregation occurs without requiring homologous chromosome pairs.KEYWORDS clonal erosion; cyclic parthenogenesis; meiosis; monogonont; Oenothera B DELLOID rotifers are minute freshwater invertebrates commonly found in lakes, streams, and ponds and in ephemerally aquatic environments such as rock pools and the water films on moss and lichens where they are able to survive because of their unusual ability to withstand desiccation. Although typically only several tenths of a millimeter in size, bdelloids have ganglia; muscles; reproductive, digestive, excretory, and secretory systems; photosensitive and tactile sensory organs; and structures for crawling, feeding, and swimming. Characterized by their ciliated head and bilateral ovaries and classified in four families and hundreds of morphospecies, their ancient origin is indicated by the considerable synonymous sequence divergence between families and by the finding of bdelloid remains in 35-to 40-million year old amber (Mark Welch et al. 2009).Despite much observation of field and laboratory populations and except for one heavily qualified account of having twice seen a male among many females in a sample from a lake (Wesenberg-Lund 1930), neither males, hermaphrodites, mating, nor meiosis have ever been reported within the class (Birky 2010). The only known mode of bdelloid reproduction is via eggs produced by two mitotic divisions from primary oocytes (Hsu 1956a,b). Most recently, further evidence suggestive of asexuality has come from genomic sequencing of the bdelloid Adineta vaga, showing it to be devoid of homologous chromosome pairs and therefore excluding the possibility of standard meiosis (Flot et al. 2013). Nevertheless, the possibility remains that bdelloids reproduce sexually under unknown or inadequately investigated conditions, employing a form of meiosis known in certain plants in which segregation occurs without homologous chromosome pairs-a possibility that can be tested by methods of population genetics.For any two individuals in a population descended from a common ancestor without sexual reproduction or any other sort of genetic transfer between individuals, the phylogenetic distance between a sequence in one individual and its Librar...

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“…, Golczyk et al. ). Because many of these species were originally formed via the hybridization of two parental species (Cleland , Dietrich et al.…”

Section: Introductionmentioning

confidence: 98%

“…PTH is a genetic system that occurs in eight plant families and is most diverse in the Onagraceae where it has independently evolved >20 times (Holsinger andEllstrand 1984, Johnson et al 2011). In such species, self-fertilization results in clonally related seeds because offspring inherit their parental genomes without meiotic recombination or segregation of chromosomes (Cleland 1972, Rauwolf et al 2008, Golczyk et al 2014. Because many of these species were originally formed via the hybridization of two parental species (Cleland 1972, Dietrich et al 1997, the lack of recombination and segregation results in "permanent" heterozygotes.…”

Section: Introductionmentioning

confidence: 99%

Fitness consequences of occasional outcrossing in a functionally asexual plant (Oenothera biennis)

Maron

Johnson

Hastings

et al. 2018

Ecology

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Many clonal organisms occasionally outcross, but the long-term consequences of such infrequent events are often unknown. During five years, representing three to five plant generations, we followed 16 experimental field populations of the forb, Oenothera biennis, originally planted with the same 18 original genotypes. Oenothera biennis usually self fertilizes, which, due to its genetic system (permanent translocation heterozygosity), results in seeds that are clones of the maternal plant. However, rare outcrossing produces genetically novel offspring (but without recombination or increased heterozygosity). We sought to understand whether novel genotypes produced through natural outcrossing had greater fecundity or different multigenerational dynamics compared to our original genotypes. We further assessed whether any differences in fitness or abundances through time between original and novel genotypes were exaggerated in the presence vs. absence of insect herbivores. Over the course of the experiment, we genotyped >12,500 plants using microsatellite DNA markers to identify and track the frequency of specific genotypes and estimated fecundity on a subset (>3,000) of plants. The effective outcrossing rate was 7.3% in the first year and ultimately 50% of the plants were of outcrossed origin by the final year of the experiment. Lifetime fruit production per plant was on average 32% higher across all novel genotypes produced via outcrossing compared to the original genotypes, and this fecundity advantage was significantly enhanced in populations lacking herbivores. Among 43 novel genotypes that were abundant enough to phenotype with replication, plants produced nearly 30% more fruits than the average of their specific two parental genotypes, and marginally more fruits (8%) than their most fecund parent. Mean per capita fecundity of novel genotypes predicted their relative frequencies at the end of the experiment. Novel genotypes increased more dramatically in herbivore-present compared to suppressed populations (45% vs. 27% of all plants), countering the increased competition from dandelions (Taraxacum officinale) that resulted from herbivore suppression. Increased interspecific competition likely also lead to the lower realized fitness of novel vs. original genotypes in herbivore-suppressed populations. These results demonstrate that rare outcrossing and the generation of novel genotypes can create high-fecundity progeny, with the biotic environment influencing the dynamical outcome of such advantages.

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Translocations of Chromosome End-Segments and Facultative Heterochromatin Promote Meiotic Ring Formation in Evening Primroses

Cited by 43 publications

References 53 publications

Widespread maintenance of genome heterozygosity in Schmidtea mediterranea

Widespread maintenance of genome heterozygosity in Schmidtea mediterranea

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

Fitness consequences of occasional outcrossing in a functionally asexual plant (Oenothera biennis)

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