Abstract

Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]. They have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary constriction corresponding to centromere observed in monocentric chromosomes [2]; ii. possess multiple kinetochores dispersed along the chromosomal axis so that microtubules bind to chromosomes along their entire length and move broadside to the pole from the metaphase plate [3]. These chromosomes are also termed holokinetic, because, during cell division, chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes [4–6]. Holocentric chromosomes evolved several times during both animal and plant evolution and are currently reported in about eight hundred diverse species, including plants, insects, arachnids and nematodes [7,8]. As a consequence of their diffuse kinetochores, holocentric chromosomes may stabilize chromosomal fragments favouring karyotype rearrangements [9,10]. However, holocentric chromosome may also present limitations to crossing over causing a restriction of the number of chiasma in bivalents [11] and may cause a restructuring of meiotic divisions resulting in an inverted meiosis [12].

Highlights

  • Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]

  • A detailed molecular analysis of the structure of holocentric chromosomes is currently available for the nematode Caenorhabditis elegans only [16,17], whereas the presence of true holokinetic nature has been confirmed in other taxa by the evidence that experimentally induced chromosome fragments continue to attach to the spindle and segregate correctly [3]

  • Similar effects have been reported by other plant-produced molecules, such as caffeine and ethanol [19,20]. In view of their ability to favour the inheritance of chromosomal fragments, holocentrism has been associated to recurrent changes in the karyotypes of some aphid species and in particular in the peach potato aphid Myzus persicae, where both inter- and intra-individual rearranged karyotypes have been observed [21,22]

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Summary

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Citation: Mandrioli M, Manicardi GC (2020) Holocentric chromosomes. PLoS Genet 16(7): e1008918. https://doi.org/10.1371/journal. pgen.1008918 Funding: The authors received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.

Evolution of holocentric chromosomes
Structure of holocentric chromosomes
Holocentric chromosomes in arthropods
Holocentric chromosomes in nematodes
Holocentric chromosomes in plants
Findings
Future directions
Full Text
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