Evolution of holocentric chromosomes: Drivers, diversity, and deterrents

ABSTRACT Prior to microtubule capture, sister centromeres resolve from one another, coming to rest on opposite surfaces of the condensing chromosome. Subsequent assembly of sister kinetochores at each sister centromere generates a geometry favorable for equal levels of segregation of chromatids. The holocentric chromosomes of Caenorhabditis elegans are uniquely suited for the study of centromere resolution and subsequent kinetochore assembly. In C. elegans, only two proteins have been identified as being necessary for centromere resolution, the kinase AIR-2 (prophase only) and the centromere protein HCP-4/CENP-C. Here we found that the loss of proteins involved in chromosome cohesion bypassed the requirement for HCP-4/CENP-C but not for AIR-2. Interestingly, the loss of cohesin proteins also restored the localization of HCP-6 to the kinetochore. The loss of the condensin II protein HCP-6 or MIX-1/SMC2 impaired centromere resolution. Furthermore, the loss of HCP-6 or MIX-1/SMC2 resulted in no centromere resolution when either nocodazole or RNA interference (RNAi) of the kinetochore protein KNL-1 perturbed spindle-kinetochore interactions. This result suggests that normal prophase centromere resolution is mediated by condensin II proteins, which are actively recruited to sister centromeres to mediate the process of resolution.

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Evidence for Centromere Drive in the Holocentric Chromosomes of Caenorhabditis

PLoS ONE ◽

10.1371/journal.pone.0030496 ◽

2012 ◽

Vol 7 (1) ◽

pp. e30496 ◽

Cited By ~ 19

Author(s):

František Zedek ◽

Petr Bureš

Keyword(s):

Holocentric Chromosomes ◽

Centromere Drive

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Endopolyploidy is a common response to UV-B stress in natural plant populations, but its magnitude may be affected by chromosome type

Annals of Botany ◽

10.1093/aob/mcaa109 ◽

2020 ◽

Vol 126 (5) ◽

pp. 883-889 ◽

Cited By ~ 1

Author(s):

František Zedek ◽

Klára Plačková ◽

Pavel Veselý ◽

Jakub Šmerda ◽

Petr Šmarda ◽

...

Keyword(s):

Photosynthetic Apparatus ◽

Ultraviolet B ◽

Holocentric Chromosomes ◽

Sample Collection ◽

Plant Populations ◽

Chromosomal Structure ◽

Natural Plant ◽

Forest Clearing ◽

Common Response ◽

Low Sensitivity

Abstract Background and Aims Ultraviolet-B radiation (UV-B) radiation damages the DNA, cells and photosynthetic apparatus of plants. Plants commonly prevent this damage by synthetizing UV-B-protective compounds. Recent laboratory experiments in Arabidopsis and cucumber have indicated that plants can also respond to UV-B stress with endopolyploidy. Here we test the generality of this response in natural plant populations, considering their monocentric or holocentric chromosomal structure. Methods We measured the endopolyploidy index (flow cytometry) and the concentration of UV-B-protective compounds in leaves of 12 herbaceous species (1007 individuals) from forest interiors and neighbouring clearings where they were exposed to increased UV-B radiation (103 forest + clearing populations). We then analysed the data using phylogenetic mixed models. Key Results The concentration of UV-B protectives increased with UV-B doses estimated from hemispheric photographs of the sky above sample collection sites, but the increase was more rapid in species with monocentric chromosomes. Endopolyploidy index increased with UV-B doses and with concentrations of UV-B-absorbing compounds only in species with monocentric chromosomes, while holocentric species responded negligibly. Conclusions Endopolyploidy seems to be a common response to increased UV-B in monocentric plants. Low sensitivity to UV-B in holocentric species might relate to their success in high-UV-stressed habitats and corroborates the hypothesized role of holocentric chromosomes in plant terrestrialization.

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Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution

Science Advances ◽

10.1126/sciadv.aau3648 ◽

2019 ◽

Vol 5 (6) ◽

pp. eaau3648 ◽

Cited By ~ 12

Author(s):

Jason Hill ◽

Pasi Rastas ◽

Emily A. Hornett ◽

Ramprasad Neethiraj ◽

Nathan Clark ◽

...

Keyword(s):

Chromosome Number ◽

Chromosome Evolution ◽

Chromosome Structure ◽

Holocentric Chromosomes ◽

Chromosome Counts ◽

Pieris Napi ◽

Haploid Chromosome Number ◽

Genome Wide ◽

The Face ◽

Chromosome Level

Chromosome evolution presents an enigma in the mega-diverse Lepidoptera. Most species exhibit constrained chromosome evolution with nearly identical haploid chromosome counts and chromosome-level gene collinearity among species more than 140 million years divergent. However, a few species possess radically inflated chromosomal counts due to extensive fission and fusion events. To address this enigma of constraint in the face of an exceptional ability to change, we investigated an unprecedented reorganization of the standard lepidopteran chromosome structure in the green-veined white butterfly (Pieris napi). We find that gene content in P. napi has been extensively rearranged in large collinear blocks, which until now have been masked by a haploid chromosome number close to the lepidopteran average. We observe that ancient chromosome ends have been maintained and collinear blocks are enriched for functionally related genes suggesting both a mechanism and a possible role for selection in determining the boundaries of these genome-wide rearrangements.

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Monocentric chromosomes in Juncus (Juncaceae) and implications for the chromosome evolution of the family

Botanical Journal of the Linnean Society ◽

10.1093/botlinnean/boz065 ◽

2019 ◽

Vol 191 (4) ◽

pp. 475-483 ◽

Cited By ~ 6

Author(s):

Marcelo Guerra ◽

Tiago Ribeiro ◽

Leonardo P Felix

Keyword(s):

In Situ Hybridization ◽

Fluorescent In Situ Hybridization ◽

Chromosome Evolution ◽

Holocentric Chromosomes ◽

Mitotic Chromosomes ◽

Restricted Area ◽

Rdna Sites ◽

The Family ◽

Meiotic Analyses

Abstract Holocentric chromosomes are rare among angiosperms, but have been suggested to be shared by all or most of the species of Cyperaceae and Juncaceae. However, no clear demonstration of the centromere type in Juncus, the largest genus of Juncaceae, has so far been published. Thus, we conducted a detailed chromosomal investigation of four Juncus spp. aiming to identify their centromere type. Mitotic chromosomes were analysed using the fluorochromes CMA and DAPI, fluorescent in situ hybridization (FISH) with rDNA probes and immunodetection of histones H3 phosphorylated at serine 10 (H3-S10ph) and H2A phosphorylated at threonine 133 (H2A-T133ph). DAPI-stained chromosomes of all species displayed typical primary constrictions, which were not related to AT-poor CMA+ heterochromatin or rDNA sites (usually negatively stained with DAPI). Immunodetection with H3-S10ph and H2A-T133ph revealed hyperphosphorylation of pericentromeric and centromeric regions, respectively, in a restricted area, as observed in monocentric chromosomes. Meiotic analyses in J. microcephalus showed no indication of inverted meiosis, commonly found in plants with holocentric chromosomes. Since the species investigated here belong to four different sections of Juncus and all of them display typical monocentric chromosomes, it seems that this kind of centromere is common in the genus and may represent the standard centromere organization for Juncus. If Juncus has monocentric chromosomes, there is no reason to hypothesize that other genera of Juncaceae for which centromeres have not been carefully investigated have holocentric chromosomes.

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