Chromosomes tell half of the story: The correlation between karyotype rearrangements and genetic diversity in sedges, a group with holocentric chromosomes

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Molecular Ecology (Impact Factor: 6.49). 08/2010; 19(15):3124-38. DOI: 10.1111/j.1365-294X.2010.04741.x
Source: PubMed


Chromosome rearrangements may affect the rate and patterns of gene flow within species, through reduced fitness of structural heterozygotes or by reducing recombination rates in rearranged areas of the genome. While the effects of chromosome rearrangements on gene flow have been studied in a wide range of organisms with monocentric chromosomes, the effects of rearrangements in holocentric chromosomes--chromosomes in which centromeric activity is distributed along the length of the chromosome--have not. We collected chromosome number and molecular genetic data in Carex scoparia, an eastern North American plant species with holocentric chromosomes and highly variable karyotype (2n = 56-70). There are no deep genetic breaks within C. scoparia that would suggest cryptic species differentiation. However, genetic distance between individuals is positively correlated with chromosome number difference and geographic distance. A positive correlation is also found between chromosome number and genetic distance in the western North American C. pachystachya (2n = 74-81). These findings suggest that geographic distance and the number of karyotype rearrangements separating populations affect the rate of gene flow between those populations. This is the first study to quantify the effects of holocentric chromosome rearrangements on the partitioning of intraspecific genetic variance.

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    • "As a result, chromosome fragments that would be acentric (lacking a centromere) and hence lost in organisms with monocentric chromosomes may be inherited in holokinetic organisms. The gametes harboring chromosome fragments are consequently expected to be viable (Hipp et al. 2010). Fusion/fission rearrangements are therefore conventionally accepted as the commonest mechanisms of chromosome evolution in holokinetic groups. "
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    • " Cyperaceae (Hipp 2007; Furness and Rudall 2011), a family comprising most (>90%) of the known angiosperm holokinetics. This indicates that holokinetic drive might be highly effective in this family, which might explain the remarkable variability in chromosome numbers not only between (Fig. 1A), but even within species in Cyperaceae (Roalson 2008; Hipp et. al 2010; Rotreklovà et al. 2011). Notably, in monocentric angiosperms, pseudomonad microsporogenesis is extremely rare, restricted only to the epacrid subfamily Styphelioideae of the family Ericaceae (Furness and Rudall 2011)."
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    ABSTRACT: Similar to how the model of centromere drive explains the size and complexity of centromeres in monocentrics (organisms with localized centromeres), our model of holokinetic drive is consistent with the divergent evolution of chromosomal size and number in holocentrics (organisms with non-localized centromeres) exhibiting holokinetic meiosis (holokinetics). Holokinetic drive is proposed to facilitate chromosomal fission and/or repetitive DNA removal (or any segmental deletion) when smaller homologous chromosomes are preferentially inherited or chromosomal fusion and/or repetitive DNA proliferation (or any segmental duplication) when larger homologs are preferred. The hypothesis of holokinetic drive is supported primarily by the negative correlation between chromosome number and genome size that is documented in holokinetic lineages. The supporting value of two older cross-experiments on holokinetic structural heterozygotes (the rush Luzula elegans and butterflies of the genus Antheraea) that indicate the presence of size-preferential homolog transmission via female meiosis for holokinetic drive is discussed, along with the potential negative consequences of holokinetic drive in comparison with centromere drive. This article is protected by copyright. All rights reserved.
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    • "Undoubtedly there are numerous contributors to heterogeneity in diversifi cation rates within the family. Hypotheses have partly attributed the increase in Poales as a whole to any of several key innovations, for example the sympodial habit, physiological factors that allowed frequent evolution of the C4 photosynthetic pathway, and wind pollination ( Linder and Rudall, 2005 ; Givnish et al., 2010 ). None of these features is so placed to have been a key innovation in the origin and diversifi cation of the SDC+FAEC clade as a whole. "
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