Neocentrics and Holokinetics (Holocentrics): Chromosomes out of the Centromeric Rules

Guerra, Marcelo; Cabral, Gabriela; Cuacos, María; González-García, M.; González‐Sánchez, Mónica; Vega, Maximiliano Rodrigo; Puertas, M. J.

doi:10.1159/000314289

Cited by 54 publications

(54 citation statements)

References 225 publications

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“…Cuscuta contains three subgenera, Cuscuta subgenus Cuscuta, Cuscuta subgenus Grammica, and Cuscuta subgenus Monogyna. Only the subgenus Cuscuta and one species in the subgenus Grammica are holocentric, offering an attractive opportunity for comparative genomics (Pazy and Plitmann 1994;Sheikh and Kondo 1995;Guerra et al 2010).…”

Section: Broad Phylogenetic Distribution Of Holocentric Chromosomesmentioning

confidence: 99%

“…In these "monocentric" chromosomes, the centromere is visible as the primary constriction in large metaphase chromosomes. In select taxa, kinetochore proteins bind along the entire length of the chromosomes and microtubules can attach along most of the poleward facing surface (Dernburg 2001;Maddox et al 2004;Guerra et al 2010). First described in cytogenetic experiments dating from 1935 , these "holocentric" chromosomes have also been called diffuse-kinetochore chromosomes, holokinetic chromosomes, and polykinetic chromosomes.…”

Section: Introductionmentioning

confidence: 99%

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Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

et al. 2012

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In most eukaryotes, the kinetochore protein complex assembles at a single locus termed the centromere to attach chromosomes to spindle microtubules. Holocentric chromosomes have the unusual property of attaching to spindle microtubules along their entire length. Our mechanistic understanding of holocentric chromosome function is derived largely from studies in the nematode Caenorhabditis elegans, but holocentric chromosomes are found over a broad range of animal and plant species. In this review, we describe how holocentricity may be identified through cytological and molecular methods. By surveying the diversity of organisms with holocentric chromosomes, we estimate that the trait has arisen at least 13 independent times (four times in plants and at least nine times in animals). Holocentric chromosomes have inherent problems in meiosis because bivalents can attach to spindles in a random fashion. Interestingly, there are several solutions that have evolved to allow accurate meiotic segregation of holocentric chromosomes. Lastly, we describe how extensive genome sequencing and experiments in nonmodel organisms may allow holocentric chromosomes to shed light on general principles of chromosome segregation.

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Section: Broad Phylogenetic Distribution Of Holocentric Chromosomesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

et al. 2012

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“…To ensure a faithful haploidization, the homologous nonsister chromatids remain linked at their termini by chromatin threads after metaphase I until metaphase II, and separate at anaphase II. Thus, an inverted sequence of meiotic sister chromatid separation occurs (Heckmann et al 2014).Similarly, in the Cyperaceae species R. pubera, multiple spindle fibers amphitelically attach to the sister chromatids during MI (Guerra et al 2010;Cabral et al 2014). In mitosis, the chromosomes exhibit a linear holocentromere organization comprising CENH3-containing centromere units enriched in centromeric tandem repeats (named Tyba) and centromeric retroelements.…”

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confidence: 99%

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

et al. 2016

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Centromeres are responsible for the correct segregation of chromosomes during mitosis and meiosis. Holocentric chromosomes, characterized by multiple centromere units along each chromatid, have particular adaptations to ensure regular disjunction during meiosis. Here we show by detecting CENH3, CENP-C, tubulin, and centromeric repeats that holocentromeres may be organized differently in mitosis and meiosis of Rhynchospora pubera. Contrasting to the mitotic linear holocentromere organization, meiotic centromeres show several clusters of centromere units (cluster-holocentromeres) during meiosis I. They accumulate along the poleward surface of bivalents where spindle fibers perpendicularly attach. During meiosis II, the cluster-holocentromeres are mostly present in the midregion of each chromatid. A linear holocentromere organization is restored after meiosis during pollen mitosis. Thus, a not yet described case of a cluster-holocentromere organization, showing a clear centromere restructuration between mitosis and meiosis, was identified in a holocentric organism.KEYWORDS holocentric chromosomes; CENH3; CENP-C; centromere structure/organization; inverted meiosis T HE centromere is the chromosome site responsible for spindle fiber attachment and faithful chromosome segregation during mitosis and meiosis. In general, every eukaryotic chromosome has a centromere on which the kinetochore complex assembles (Cleveland et al. 2003;Burrack and Berman 2012). In most eukaryotes, centromeric nucleosomes contain CENH3 (also known as CENP-A, a histone H3 variant that replaces canonical H3 at the centromere), and usually spans several hundred kilobase pairs often in association with centromere-specific repeats (Steiner and Henikoff 2015).Centromere organization and dynamics vary between mitosis and meiosis (Duro and Marston 2015;Ohkura 2015). During mitosis, sister chromatids are held together by centromere cohesion until metaphase. Simultaneous with the disruption of cohesion, sister chromatids are pulled to opposite poles during anaphase. In contrast, during meiosis, sister centromere cohesion is ensured until metaphase II (Ishiguro and Watanabe 2007). The stepwise regulation of cohesion release during meiosis I (MI) and II (MII) is well studied in organisms with one primary constriction per chromosome (monocentric), ensuring the segregation of homologs at MI followed by the segregation of sister chromatids at MII (Duro and Marston 2015).Contrary to monocentrics, the centromeres of holocentric chromosomes are distributed almost over the entire chromosome length and cohesion occurs along the entire associated sister chromatids (Maddox et al. 2004). Although this does not imply much difference during mitotic divisions, the presence of a holokinetic centromere (holocentromere) imposes obstacles to the dynamics of chromosome segregation in meiosis. Due to their alternative chromosome organization, species with holocentric chromosomes cannot perform the two-step cohesion loss during meiosis typical for monocentric species...

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“…In holocentric chromosomes, CenH3 staining localizes as a band on the edge of each sister chromatid facing toward spindle microtubules (10, 23); we did not observe such a pattern in T. vaginalis. The presence of primary constrictions representing centromeres indicates the monocentric nature of chromosomes in T. vaginalis; furthermore, these structures are absent in holocentric chromosomes (1,16,21). A clearly visible constriction is found on four out of six chromosomes (chromosomes I, III, IV, V) during mitotic metaphase in T. vaginalis (13).…”

Section: Localization Of H3 Variants In Chromatinmentioning

confidence: 94%

Histone H3 Variants in Trichomonas vaginalis

2012

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The parabasalid protist Trichomonas vaginalis is a widespread parasite that affects humans, frequently causing vaginitis in infected women. Trichomonad mitosis is marked by the persistence of the nuclear membrane and the presence of an asymmetric extranuclear spindle with no obvious direct connection to the chromosomes. No centromeric markers have been described in T. vaginalis, which has prevented a detailed analysis of mitotic events in this organism. In other eukaryotes, nucleosomes of centromeric chromatin contain the histone H3 variant CenH3. The principal aim of this work was to identify a CenH3 homolog in T. vaginalis. We performed a screen of the T. vaginalis genome to retrieve sequences of canonical and variant H3 histones. Three variant histone H3 proteins were identified, and the subcellular localization of their epitope-tagged variants was determined. The localization of the variant TVAG_185390 could not be distinguished from that of the canonical H3 histone. The sequence of the variant TVAG_087830 closely resembled that of histone H3. The tagged protein colocalized with sites of active transcription, indicating that the variant TVAG_087830 represented H3.3 in T. vaginalis. The third H3 variant (TVAG_224460) was localized to 6 or 12 distinct spots at the periphery of the nucleus, corresponding to the number of chromosomes in G 1 phase and G 2 phase, respectively. We propose that this variant represents the centromeric marker CenH3 and thus can be employed as a tool to study mitosis in T. vaginalis. Furthermore, we suggest that the peripheral distribution of CenH3 within the nucleus results from the association of centromeres with the nuclear envelope throughout the cell cycle.

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Neocentrics and Holokinetics (Holocentrics): Chromosomes out of the Centromeric Rules

Cited by 54 publications

References 225 publications

Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

Histone H3 Variants in Trichomonas vaginalis

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