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Holocentric Chromosomes

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Plant Genome Diversity Volume 2

Abstract

In contrast to the “normal type” of monocentric mitotic chromosomes, where spindle attachment is restricted to a single kinetochore, holocentric chromosomes are chromosomes to which spindle microtubules attach along the whole length through kinetochores that cover a substantial part of their poleward surfaces during mitosis. In addition, holocentric sister chromatids are interconnected along their whole lengths before anaphase disjunction, unlike monocentric chromatids, which cohere only in the pericentromeric area. The morphological distinctions between monocentric and holocentric chromosomes are associated with differences in chromatin structure and modified mitosis or meiosis, as well as karyotype evolution of the holocentrics themselves. In this chapter, we will survey these aspects of holocentrism and also discuss some hypotheses on the origin of holocentric chromosomes, their patterns of occurrence and methods of verification, particularly among plants.

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Notes

  1. 1.

    To avoid confusion with the more narrowly defined term “holokinetic”, which describes meiotic chromosome behaviour as the opposite of telokinetic behaviour, we prefer to use the term “holocentric” to indicate the opposite of the monocentric chromosomal nature.

  2. 2.

    A similar state, sometimes considered to be transitional between monocentrism and holocentrism, is the formation of a neocentromere, a chromosomal region that differs in its sequence and structure but can function like a centromere in meiotic chromosomes. However, the neocentromere in plants is more likely just an aberrant structure that occurs occasionally in some individuals or populations (Dawe and Hiatt 2004). The majority of plant neocentromeres are the outcome of meiotic drive (Dawe and Hiatt 2004), which is one of the possible mechanisms that has been suggested to explain the origin of holocentric chromosomes (see Sect. 12.8).

  3. 3.

    Holocentric chromosomes have been studied in detail only in the economically important nutmeg tree Myristica fragrans. Although chromosome counts have been reported for seven additional species in Myristicaceae, accounting for approximately 2% of the species richness of the family (Bolkhovskikh et al. 1969; Goldblatt and Johnson 2010), the lack of detailed cytological analysis means that the presence of holocentric chromosomes is unclear.

  4. 4.

    Although holocentrism has been experimentally confirmed several times in the genus Luzula, it has been proposed to exist but not satisfactorily proven in the genus Juncus (Godward 1985) and other monotypic genera of Juncaceae (but see Sect. 12.7.3). In addition, in the closely related family Thurniaceae (comprising four species of Thurnia and Prionium), there is currently no karyological research so it is unknown whether holocentric chromosomes are present here (Bolkhovskikh et al. 1969; Goldblatt and Johnson 2010).

  5. 5.

    This represents the third most species-rich monocot family after orchids and grasses. Numerous studies from the latter half of the twentieth century reported localized centromeres in Cyperaceae from S Asia, but these studies were rightfully doubted by Greilhuber (1995), who considered them to be based on chromosomal constrictions observed during mitotic prophase or metaphase, when chromosomes are not entirely contracted. Holocentrism has since been definitively confirmed experimentally in several taxa and should thus be considered as a family synapomorphy (Greilhuber 1995).

  6. 6.

    The subfamily Chionographioideae comprises two monotypic genera—Chionographis and Chamaelirium. Given the presence of holocentric chromosomes in Chionographis, it has been suggested that Chamaelirium luteum may also possess such chromosomes. However, cytological studies have so far failed to show whether the 18 chromosomes, which are very small compared with other species in Melanthiaceae, are holocentric or monocentric (Thomas Meagher, personal communication).

  7. 7.

    The putative holocentrism reported by Chakravorti (1948a, b) in the families Zingiberaceae and Musaceae from the monocots was not confirmed in later studies.

  8. 8.

    Holocentrism is present in the Cuscuta subgenus Cuscuta, whereas monocentrism has been confirmed in the subgenus Monogyna. Recently, holocentric chromosomes were also found in some taxa of the subgenus Grammica (Guerra et al. 2010), in which monocentrism was expected. In the subgenus Grammica, the sizes of the genomes and chromosomes are highly divergent (McNeal et al. 2007), which could indirectly suggest the presence of holocentrism (see Sect. 12.7.1).

  9. 9.

    In Aldrovanda, a related monotypic genus of Droseraceae, chromosomes are very small and isodiametric without any apparent primary constriction, but their holocentric nature has never been satisfactorily confirmed. The monotypic genus Dionaea from the same family, however, possesses monocentric chromosomes, as does Drosophyllum, a monotypic genus recently separated into a different monotypic family.

  10. 10.

    The unclear centromeric status reported by Vaarama (1954) in the moss Pleurozium schreberi which is sometimes considered to be holocentric, is actually neocentromeric activity (Dawe and Hiatt 2004).

  11. 11.

    In mitosis, the sister chromatids are clearly defined both in holocentrics and monocentrics as two identical (daughter) chromatids derived from duplication (replication) of one and the same chromosome during of the cell cycle [see e.g., King RC, Stansfield WD, Mulligan PK (2006) A dictionary of genetics. 7th Ed. Oxford Univ. Press, Oxford]. In meiosis, the term “sister” regarding to patchwork chromatids recombined via crossover is not so easy to define in holocentrics as in monocentrics where connection of centromeres defines which two chromatids are sister while those which are not joined by a common centromere are non-sister (= homolog) chromatids [see e.g., Brooker RJ (2009) Genetics: analysis & principles. 3rd Ed. McGraw-Hill Irwin, New York, p. 49, 821]. In holocentrics, the “majority rule” defines sister and non-sister chromatids meaning that sister chromatids share longer identical segments originated via replication, while non-sister chromatids share shorter absolutely identical segments. From a practical viewpoint, the terms “sister” and “non-sister” well fitted to mitotic chromosomes are universally conserved by such additional criteria (common centromere or “majority rule”) for any type (mitosis or meiosis, holocentric or monocentric) or phase (pre- or postrecombinational) of cell division to overcome the difficulty that no original sister chromatids are present anymore after recombination.

  12. 12.

    As a consequence of the fission or fusion of chromosomes, trivalents are sometimes formed during meiosis: two fragments are homologous to one non-fragmented chromosome, or one fused chromosome is homologous to the two non-fused ones. Two types of segregation are possible in this case. In the first case (telokinetic meiosis), the larger chromosome migrates to one pole, whereas the two shorter chromosomes migrate to the other pole during meiosis I. In the second case (holokinetic meiosis), two triads of individual chromatids segregate. This specific situation, if observed, could be also used to identify the holokinetic or telokinetic type of meiosis.

  13. 13.

    In plants, telokinetic meiosis was reported in Luzula elegans by Malheiros et al. (1947), who suggested that during anaphase I and II, the kinetic activity is restricted to both ends of each chromosome. This species was later analysed more precisely by Östergren (1949), who claimed that L. elegans chromosomes undergo inverted meiosis (i.e., holokinetic behaviour). The holokinetic chromosomal behaviour has also been reported in other species of Luzula (Nordenskiöld 1962, 1963; Braselton 1971, 1981).

  14. 14.

    Such a low chromosome number has been found in only five other angiosperms: Zingeria biebersteiniana, Colpodium versicolor, Brachycome dichromosomatica, Haplopappus gracilis, and Ornithogalum tenuifolium (Cremonini 2005).

  15. 15.

    The gain or loss of a particular chromosome or chromosomes due to non-disjunction during irregular meiotic chromosomal segregation.

  16. 16.

    In some holocentric taxa, the wide range of intraspecific variation may also be associated with true aneuploidy, for example, in Eleocharis uniglumis s. l. (2n = 44−51, 53−56, 59−89, 92; Strandhede 1965b, 1966; Bureš 1998), where the chromosome number and DNA content are linearly correlated (Bureš and Kneřová unpubl.). Other examples of true aneuploidy in Carex are reviewed by Hipp et al. (2009).

  17. 17.

    The presence of more than one cytotype in the species was documented in more than 100 species of Carex and many other taxa of Cyperaceae (Roalson 2008; Hipp et al. 2009).

  18. 18.

    Karyotypic orthoselection occurs when a particular type of chromosomal rearrangement is present recurrently in a phylogenetic lineage (White 1973). In this case, the presence of fission or fusion is assumed to have occurred.

  19. 19.

    In those species with the largest chromosomes, Ty1-copia LTR retrotransposons (assuming that all were full-length) might form up to 70% of the genomic DNA (Zedek et al. 2010)

  20. 20.

    The pseudomonad pollen formation was shown to be synapomorphic for the more derived clades of Cyperaceae, but absent in the early diverging clade of the subfamily Mapanioideae (Simpson et al. 2003).

  21. 21.

    In addition to these three main size categories, giant (A0) and tiny chromosomes are present in this genus in Luzula elegans (= L. purpurea) and L. pilosa, respectively. See inner box in Fig. 12.3.

  22. 22.

    An extremely high intraspecific and intraplant variation in chromosome number was found by Kuta et al. (2004) in the cultivated seedlings of Luzula multiflora, in which the somatic chromosome number varied 6.83-fold (from 12 to 84), whereas the DNA content varied just 1.04-fold (from 1.796 to 1.864 pg). This observation suggests a high frequency of agmatoploidy even during ontogenesis; however, other studies have not documented such chromosome variation in this species (Nordenskiöld 1951; Kirschner 1992; Bačič et al. 2007). Because samples were based on seeds obtained from the Botanical Garden of Stuttgart (Kuta et al. 2004), testing whether that observed pattern is also present in natural populations or among progeny cultivated from the seeds collected from wild plants of this species would be appropriate.

  23. 23.

    The probable presence of such fragile points on the chromosomes of Carex has also been speculated by Luceño (1994).

  24. 24.

    Considering that terminal blocks of heterochromatin exhibiting “centromeric activity” in telokinetic (holocentric) germline chromosomes of the nematode Parascaris univalens originated by the segmental amplification of repeats derived from telomeric repeats (Niedermaier and Moritz 2000).

  25. 25.

    Tandem repeats (including the telomeric repeat TTAGGC) are indeed dispersed at multiple internal sites of the holocentric chromosomes of the nematode Caenorhabditis elegans, although they are more abundant at the ends (C. elegans Sequencing Consortium 1998).

  26. 26.

    Actually, this observation would be true in animals, which are usually gonochoric. In plants, the male sterility of structural heterozygotes (individuals possessing different types of homologous centromeres) should not decrease population fitness because these male-sterile individuals have to produce sexual progeny exclusively via outcrossing, which would thus counterbalance the eventual inbreeding depression that originates due to the selfing of hermaphrodites. In other words, a pattern similar to gynodioecy would result.

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Acknowledgments

Our study was supported by the Czech Science Foundation (Grant no. GACR206/09/1405) and by the Ministry of Education, Youth and Sports of the Czech Republic (Grants no. MSM0021622416, and LC06073).

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  1. Department of Botany & Zoology, Masaryk University, Kotlářská 2, Brno 611 37, Brno, 621 00, Czech Republic

    Prof. RNDr. Petr Bureš Ph.D. (Faculty of Science)

  2. Department of Botany and Zoology, Masaryk University, Brno, Czech Republic

    Dr. František Zedek (Faculty of Science) & Dr. Michaela Marková (Faculty of Science)

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  1. Inst. Botanik und Botanischer Garten, Universität Wien, Rennweg 14, Wien, 1030, Austria

    Johann Greilhuber

  2. Inst. Experimental Botany, Dept. Plant Biotechnology, ASCR Olomouc, Sokolovska 6, Olomouc, 772 00, Czech Republic

    Jaroslav Dolezel

  3. Dept. Botany, Iowa State University, Ames, 50011-1024, Iowa, USA

    Jonathan F. Wendel

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Bureš, P., Zedek, F., Marková, M. (2013). Holocentric Chromosomes. In: Greilhuber, J., Dolezel, J., Wendel, J. (eds) Plant Genome Diversity Volume 2. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1160-4_12

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