DNA and proteins of plant centromeres

https://doi.org/10.1016/j.pbi.2003.09.007Get rights and content

Abstract

In plants, as in all eukaryotes, centromeres are chromatin domains that govern the transmission of nuclear chromosomes to the next generation of cells/individuals. The DNA composition and sequence organization of centromeres has recently been elucidated for a few plant species. Although there is little sequence conservation among centromeres, they usually contain tandem repeats and retroelements. The occurrence of neocentromeres reinforces the idea that the positions of centromeres are determined epigenetically. In contrast to centromeric DNA, structural and transient kinetochoric proteins are highly conserved among eukaryotes. Candidate sequences have been identified for a dozen putative kinetochore protein homologues, and some have been localized to plant centromeres. The kinetochore protein CENH3, which substitutes histone H3 within centromeric nucleosomes, co-immunoprecipitates preferentially with centromeric sequences. The mechanism(s) of centromere assembly and the functional implication of (peri-)centromeric modifications of chromatin remain to be elucidated.

Introduction

The centromere of monocentric chromosomes is morphologically recognizable as the primary constriction. Centromeres are essential for the correct segregation of sister chromatids into daughter cells during mitosis and meiosis II, and of homologous chromosomes during meiosis I. In all eukaryotes, centromeres are responsible for chromatid cohesion from S-phase until anaphase, for spindle fiber attachment during metaphase and for chromosome movement during early metaphase and in anaphase. A proteinaceous kinetochore assembles at active centromeres and enables chromosome movement [1]. We review recent developments that have improved our knowledge of the DNA and protein composition and functional aspects of plant centromeres and neocentromeres, including epigenetic modifications within (peri-)centromeres. For previous reviews on plant centromeres see 2., 3., 4..

Section snippets

DNA composition of plant centromeres

In contrast to telomeres, centromeres are not specified by highly conserved DNA sequences. Centromeric sequences have been described for several eukaryotes. Except for the approximately 125-bp centromeres of budding yeast [5], whose functional importance was verified by mutation analyses, the functional importance of centromeric sequences is at least controversial. In Vicia faba and Tradescantia paludosa it has not yet been possible to detect centromere-specific repeats [6], whereas such

Protein composition of plant kinetochores

Contrary to centromeric DNA, structural and functional kinetochore proteins are highly conserved between yeast and metazoa. Almost fifty proteins are constitutively or transiently associated with S. cerevisiae centromeres (see also [39]), and more than 20 kinetochore proteins (KPs) are known to occur in human centromeres and neocentromeres [40]. The KPs of human neocentromeres are free of detectable centromeric alphoid satellite sequences [40]. The occurrence of neocentromeres (about 50 are

Pericentromere-specific chromatin modifications

Specific post-translational modifications of histone H3 at pericentromeres are known to occur in metazoa and plants. In plants, serine 10 ([61]; Figure 1) and 28 [62] of H3 are strongly phosphorylated at pericentromeres during mitosis and during the second meiotic division from prophase until telophase. During the first meiotic division, this modification occurs along entire chromosomes (as is the case for monocentric animal chromosomes during all nuclear divisions). Single chromatids that

Neocentromeres

Most plant neocentromeres differ from those described for humans [70] and Drosophila melanogaster [71] because they occur on chromosomes that have a normal centromere. Plant neocentromeres, which are best known in maize and rye, appear during meiosis rather than during mitosis. Maize neocentromeres occur in terminal heterochromatic domains called knobs, which are composed mainly of tandem repeats that differ from those of regular centromeres 20., 72.. Neocentric activity results in preferential

Conclusions

Centromeric repetitive sequences are not highly conserved and may not be sufficient (e.g. the inactive centromeres of some human dicentric chromosomes) or necessary (e.g. neocentromeres) for the assembly of functional kinetochores. Nevertheless, clusters of tandem repeats that are interspersed with retroelements are typical features of the regular centromeres of most studied plants. Whether RNA interference [69•] and/or stretching of centromeric chromatin, caused by the bi-orientation of sister

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • •

    of special interest

  • ••

    of outstanding interest

Acknowledgements

We thank K Dawe, TR Endo, R ten Hoopen, E Schroeder-Reiter and R Rieger for helpful discussion, and G Wanner for providing the electron micrograph. This work was supported by grants from the Deutsche Forschungsgemeinschaft to AH and IS.

References (101)

  • M Yang et al.

    The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation

    Proc Natl Acad Sci USA

    (1999)
  • H Saitoh et al.

    CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate

    Cell

    (1992)
  • N.S Heiss et al.

    Dyskerin localizes to the nucleolus and its mislocalization is unlikely to play a role in the pathogenesis of dyskeratosis congenita

    Hum Mol Genet

    (1999)
  • W Saunders et al.

    The Saccharomyces cerevisiae kinesin-related motor Kar3p acts at preanaphase spindle poles to limit the number and length of cytoplasmic microtubules

    J Cell Biol

    (1997)
  • J.B Rattner et al.

    CENP-F is a ca. 400 kDa kinetochore protein that exhibits a cell-cycle dependent localization

    Cell Motil Cytoskeleton

    (1993)
  • S.S Taylor et al.

    The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase

    J Cell Biol

    (1998)
  • Choo KHA: The centromere. Oxford: Oxford University Press;...
  • M Murata

    Telomeres and centromeres in plants

    Curr Genomics

    (2002)
  • L Clarke et al.

    The structure and function of yeast centromeres

    Annu Rev Genet

    (1985)
  • A Houben et al.

    Molecular-cytogenetic characterization of a higher plant centromere/kinetochore complex

    Theor Appl Genet

    (1996)
  • J.M Martinez-Zapater et al.

    A highly repeated DNA sequence in Arabidopsis thaliana

    Mol Gen Genet

    (1986)
  • J.S Heslop-Harrison et al.

    Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes

    Plant Cell

    (1999)
  • T Pelissier et al.

    Athila, a new retroelement from Arabidopsis thaliana

    Plant Mol Biol

    (1995)
  • N Kumekawa et al.

    The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 5

    DNA Res

    (2000)
  • N Kumekawa et al.

    The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 4

    DNA Res

    (2001)
  • T Hosouchi et al.

    Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3

    DNA Res

    (2002)
  • S.E Hall et al.

    Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains

    Genome Res

    (2003)
  • X Sun et al.

    Sequence analysis of a functional Drosophila centromere

    Genome Res

    (2003)
  • L Aragon-Alcaide et al.

    A cereal centromeric sequence

    Chromosoma

    (1996)
  • J Jiang et al.

    A conserved repetitive DNA element located in the centromeres of cereal chromosomes

    Proc Natl Acad Sci USA

    (1996)
  • G.G Presting et al.

    A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes

    Plant J

    (1998)
  • S Hudakova et al.

    Sequence organization of barley centromeres

    Nucleic Acids Res

    (2001)
  • E.V Ananiev et al.

    Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions

    Proc Natl Acad Sci USA

    (1998)
  • F Dong et al.

    Rice (Oryza sativa) centromeric regions consist of complex DNA

    Proc Natl Acad Sci USA

    (1998)
  • J.T Miller et al.

    Retrotransposon-related DNA sequences in the centromeres of grass chromosomes

    Genetics

    (1998)
  • J.T Miller et al.

    Cloning and characterization of a centromere-specific repetitive DNA element from Sorghum bicolor

    Theor Appl Genet

    (1998)
  • K Nonomura et al.

    The centromere composition of multiple repetitive sequences on rice chromosome 5

    Chromosoma

    (2001)
  • T Langdon et al.

    Retrotransposon evolution in diverse plant genomes

    Genetics

    (2000)
  • K.N Fukui et al.

    Physical arrangement of retrotransposon-related repeats in centromeric regions of wheat

    Plant Cell Physiol

    (2001)
  • Z Cheng et al.

    Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon

    Plant Cell

    (2002)
  • K Nagaki et al.

    Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres

    Genetics

    (2003)
  • F Gindullis et al.

    Construction and characterization of a BAC library for the molecular dissection of a single wild beet centromere and sugar beet (Beta vulgaris) genome analysis

    Genome

    (2001)
  • M.G Francki

    Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.)

    Genome

    (2001)
  • V.A Saunders et al.

    The pericentromeric heterochromatin of the grass Zingeria biebersteiniana (2n = 4) is composed of Zbcen1-type tandem repeats that are intermingled with accumulated dispersedly organized sequences

    Genome

    (2001)
  • K Nagaki et al.

    A novel repetitive sequence of sugar cane, SCEN family, locating on centromeric regions

    Chromosome Res

    (1998)
  • B.T Page et al.

    Characterization of a maize chromosome 4 centromeric sequence: evidence for an evolutionary relationship with the B chromosome centromere

    Genetics

    (2001)
  • C.X Zhong et al.

    Centromeric retroelements and satellites interact with maize kinetochore protein CENH3

    Plant Cell

    (2002)
  • P Zhang et al.

    The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction

    Chromosoma

    (2001)
  • E Kaszas et al.

    Meiotic transmission rates correlate with physical features of rearranged centromeres in maize

    Genetics

    (1998)
  • Endo TR, Nasuda S: Are centromeric repeats necessary for the function of barley? In Structure and Function of Plant...

    • Cited by (91)

    • Differences in gene expression profiles at the early stage of Solanum lycopersicum infection with mild and severe variants of potato spindle tuber viroid

      2020, Virus Research
      Citation Excerpt :

      A strong down-regulation of expression of the gene coding the kinetochore/centromere protein (Zw10) was also observed only in PSTVd-S23 infection (Table S5). In all eukaryotic organisms, centromeres are responsible for the attachment of the spindle fiber during the metaphase and the movement of chromosomes in the metaphase and the anaphase (Houben and Schubert, 2003). In Drosophila melanogaster, the protein is encoded by the zw10 gene, whose homologue has been identified in A. thaliana (Starr et al., 1997).

    • Identification of centromeric regions on the linkage map of cotton using centromere-related repeats

      2014, Genomics
      Citation Excerpt :

      Additionally, no tandem repeat was found in this 93.9-kb fragment. Because retrotransposons and satellites are the dominant elements in the plant centromere [25], we next focused on identifying retroelements in this BAC. Four retrotransposons, named GhCR1–4 (KF517432–KF517435), were predicted by LTR_FINDER [26], spanning 35.2 kb in this BAC (Table 1).

    • Different evolutionary patterns among intronless genes in maize genome

      2014, Biochemical and Biophysical Research Communications
      Citation Excerpt :

      Interestingly, the number of ORFans in the region of centromere on each chromosome was significantly higher than that of ABE group (one-way ANOVA, p < 0.05). This dramatic difference may be because centromeric DNA sequences have no homolog in other species [26–28]. Thus, some maize-specific genes in the region of centromere may play important role in segregating chromosomes into daughter cells.

    • KNL1 and NDC80 represent new universal markers for the detection of functional centromeres in plants

      2024, Chromosome Research

    • Plasticity of parental CENH3 incorporation into the centromeres in wheat × barley F1 hybrids

      2024, Frontiers in Plant Science

    • Meiotic instability and irregular chromosome pairing underpin heat-induced infertility in bread wheat carrying the Rht-B1b or Rht-D1b Green Revolution genes

      2024, New Phytologist
    View all citing articles on Scopus
    View full text
    Copyright © 2003 Elsevier Ltd. All rights reserved.