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The Centromere Histone Is Conserved and Associated with Tandem Repeats Sharing a Conserved 19-bp Box in the Holocentromere of Meloidogyne Nematodes

Despot-Slade, Evelin; Mravinac, Brankica; Širca, Saša; Castagnone-Sereno, Philippe; Plohl, Miroslav; Meštrović, Nevenka (2021) The Centromere Histone Is Conserved and Associated with Tandem Repeats Sharing a Conserved 19-bp Box in the Holocentromere of Meloidogyne Nematodes. Molecular biology and evolution, 38 (5). pp. 1943-1965. ISSN 0737-4038

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Abstract

Although centromeres have conserved function, centromere-specific histone H3 (CenH3) and centromeric DNA evolve rapidly. The centromere drive model explains this phenomenon as a consequence of the conflict between fast-evolving DNA and CenH3, suggesting asymmetry in female meiosis as a crucial factor. We characterized evolution of the CenH3 protein in three closely related, polyploid mitotic parthenogenetic species of the Meloidogyne incognita group, and in the distantly related meiotic parthenogen Meloidogyne hapla. We identified duplication of the CenH3 gene in a putative sexual ancestral Meloidogyne. We found that one CenH3 (αCenH3) remained conserved in all extant species, including in distant Meloidogyne hapla, whereas the other evolved rapidly and under positive selection into four different CenH3 variants. This pattern of CenH3 evolution in Meloidogyne species suggests the subspecialization of CenH3s in ancestral sexual species. Immunofluorescence performed on mitotic Meloidogyne incognita revealed a dominant role of αCenH3 on its centromere, whereas the other CenH3s have lost their function in mitosis. The observed αCenH3 chromosome distribution disclosed cluster-like centromeric organization. The ChIP-Seq analysis revealed that in M. incognita αCenH3-associated DNA dominantly comprises tandem repeats, composed of divergent monomers which share a completely conserved 19-bp long box. Conserved αCenH3-associated DNA is also confirmed in the related mitotic Meloidogyne incognita group species suggesting preservation of both centromere protein and DNA constituents. We hypothesize that the absence of centromere drive in mitosis might allow for CenH3 and its associated DNA to achieve an equilibrium in which they can persist for long periods of time.

Item Type: Article
Uncontrolled Keywords: holocentromere ; evolution ; nematode ; mitotic parthenogenesis ; CenH3 ; gene duplication ; centromeric DNA
Subjects: NATURAL SCIENCES > Biology
Divisions: Division of Molecular Biology
Projects:
Project titleProject leaderProject codeProject type
Centromerna genomika beskralježnjakaPlohl, MiroslavIP-2014-09-3183HRZZ
Depositing User: Brankica Mravinac
Date Deposited: 13 May 2021 09:51
Last Modified: 10 Aug 2021 10:31
URI: http://fulir.irb.hr/id/eprint/6408
DOI: 10.1093/molbev/msaa336

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