Karyotype Evolution in Holocentric Organisms

Abstract

Holocentric chromosomes are characterised by the presence of kinetochoric activity along the chromosome length. This atypical chromosomal architecture has evolved independently in a wide array of lineages across the tree of life. Different mechanisms have been developed to overcome meiotic problems posed by holocentry, such as inverted meiosis and restricted kinetochore activity. Although holocentric karyotypes present potential advantages through the fission and fusion events that characterise chromosome evolution in several holocentric lineages, there is no consistent evidence of increased diversification rates in holocentric lineages relative to monocentric lineages. The extended kinetochore in holocentric chromosomes has been hypothesised to enable a unique type of meiotic drive, ‘holocentric drive’, analogous to the meiotic drive of monocentric chromosomes. However, much research remains to understand holocentrism, especially elucidating the mechanism and evolutionary implications of meiosis in unrelated holocentric lineages.

Key Concepts

  • Monocentric chromosomes are distinct from holocentric chromosomes during mitotic segregation, in which chromosomes generally adopt a V shape in the former and segregate parallel to the equatorial plate in the latter.
  • Holocentric chromosomes are present in distantly related plant and animal lineages, suggesting several independent origins of holocentry.
  • Monocentry appears to be ancestral in eukaryotes, and evolutionary transitions appear to have occurred from monocentric to holocentric, and vice versa.
  • Reversions from holocentric to monocentric chromosomes appear to have occurred more frequently than transitions from monocentry to holocentry.
  • Although holocentric chromosomes would seem like an adaptive advantage, there is no clear pattern when compared to monocentric lineages, as both types could present different evolutionary advantages.

Keywords: Centromere; chromosome evolution; holocentric chromosomes; holokinetic chromosomes; kinetochore; meiosis

Figure 1. Mitosis (a) and meiosis (b) in monocentric and holocentric organisms. (a) During segregation, holocentric chromosomes migrate parallel to one another; monocentric chromosomes adopt a V shape as they migrate to the poles, dragged along by their centromeres. (b) In monocentric and holocentric chromosomes that present restricted kinetochoric activity (i.e. telokinetic and C. elegans chromosomes), chromosomes segregate during meiosis I and chromatids in meiosis II. By contrast, in holocentric organisms with inverted meiosis (i.e. truly holokinetic chromosomes), the order is reversed, the chromatids segregate in meiosis I and chromosomes in meiosis II. Note how C. elegans kinetochore (red line) adopts a characteristic cup shape along the active centromeres. Also, in early anaphase, a ring of chromokinesin (yellow line) is formed in the equatorial plate of C. elegans oocytes, from which noncentromeric microtubules push the chromosomes to each pole.
close

References

Brook AJ (1981) The Biology of Desmids. Blackwell Scientific Publications: Oxford.

Bureš P and Zedek F (2014) Holokinetic drive: centromere drive in chromosomes without centromeres. Evolution (N. Y) 68: 2412–2420. DOI: 10.1111/evo.12437.

Bureš P, Zedek F and Marková M (2013) Holocentric chromosomes. In: Greilhuber J, Dolezel J and Wendel JF (eds) Plant Genome Diversity, vol. 2, pp 187–208. Springer: Vienna. DOI: 10.1007/978‐3‐7091‐1160‐4.

Burrack LS, Applen SE and Berman J (2011) The requirement for the Dam1 complex is dependent upon the number of kinetochore proteins and microtubules. Current Biology 21: 889–896. DOI: 10.1016/j.cub.2011.04.002.

Cabral G, Marques A, Schubert V, Pedrosa‐Harand A and Schlögelhofer P (2014) Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes. Nature Communications 5: 5070. DOI: 10.1038/ncomms6070.

Cayouette J and Morisset P (1986) Chromosome studies on Carex paleacea Wahl., C. nigra (L.) Teichard, and C. aquatilis Wahl. in northeastern North America. Cytologia 51: 857–883.

Cheerambathur DK and Desai A (2014) Linked in: formation and regulation of microtubule attachments during chromosome segregation. Current Opinion in Cell Biology 26: 113–122. DOI: 10.1016/j.ceb.2013.12.005.

Davies EW (1956) Cytology, evolution and origin of the aneuploid series in the genus Carex. Hereditas 42: 349–365. DOI: 10.1111/j.1601‐5223.1956.tb03022.x.

Dawe RK and Hiatt EN (2004) Plant neocentromeres: fast, focused, and driven. Chromosome Research 12: 655–669. DOI: 10.1023/B:CHRO.0000036607.74671.db.

Drinnenberg IA, DeYoung D, Henikoff S and Malik HS (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. eLife 3. DOI: 10.7554/eLife.03676.

Dumont J, Oegema K and Desai A (2010) A kinetochore‐independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nature Cell Biology 12: 894–901. DOI: 10.1038/ncb2093.

Earnshaw WC (2015) Discovering centromere proteins: from cold white hands to the A, B, C of CENPs. Nature Reviews. Molecular Cell Biology 16: 443–449. DOI: 10.1038/nrm4001.

Escudero M, Hipp AL, Hansen TF, Voje KL and Luceño M (2012) Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). The New Phytologist 195: 237–247. DOI: 10.1038/s41598‐017‐08525‐6.

Escudero M, Martín‐Bravo S, Mayrose I, et al. (2014) Karyotypic changes through dysploidy persist longer over evolutionary time than polyploid changes. PLoS One 9: e85266. DOI: 10.1371/journal.pone.0085266.

Escudero M, Márquez‐Corro JI and Hipp AL (2016) The phylogenetic origins and evolutionary history of holocentric chromosomes. Systematic Botany 41: 580–585. DOI: 10.1600/036364416X692442.

Faulkner JS (1972) Chromosome studies on Carex section Acutae in North‐West Europe. Botanical Journal of the Linnean Society 65: 271–301.

Grell KG and Ruthmann A (1964) Über die karyologie des radiolars Aulacantha scolymantha und die feinstruktur seiner chromosomen. Chromosoma 15: 185–211. DOI: 10.1007/BF00285729.

Heilborn O (1924) Chromosome numbers and dimensions, species‐formation and phylogeny in the genus Carex. Hereditas 5: 129–212. DOI: 10.1111/j.1601‐5223.1924.tb03128.x.

Henikoff S, Ahmad K and Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science (80‐.) 293: 1098–1102. DOI: 10.1126/science.1062939.

Hipp AL, Escudero M and Chung K‐S (2013) Holocentric chromosomes. In: Maloy S and Hughes K (eds) Brenner's Encyclopedia of Genetics, pp 499–501. Elsevier: Amsterdam. DOI: 10.1016/B978‐0‐12‐374984‐0.00723‐3.

Hirano T (2016) Condensin‐based chromosome organization from bacteria to vertebrates. Cell 164: 847–857. DOI: 10.1016/j.cell.2016.01.033.

Horne AS (1930) Nuclear division in the Plasmodiophorales. Annals of Botany 44: 199–231. DOI: 10.1093/oxfordjournals.aob.a090213.

Hughes‐Schrader S and Ris H (1941) The diffuse spindle attachment of coccids, verified by the mitotic behavior of induced chromosome fragments. The Journal of Experimental Zoology 87: 429–456. DOI: 10.1002/jez.1400870306.

King GC (1960) The cytology of the Desmids: the chromosomes. The New Phytologist 59: 65–72. DOI: 10.1111/j.1469‐8137.1960.tb06203.x.

Kolodin P, Cempírková H, Bureš P, et al. (2018) Holocentric chromosomes may be an apomorphy of Droseraceae. Plant Systematics and Evolution 304: 1289–1296. DOI: 10.1007/s00606‐018‐1546‐8.

Král J, Kováč L, Št'áhlavský F, Lonský P and L'uptáčik P (2008) The first karyotype study in palpigrades, a primitive order of arachnids (Arachnida: Palpigradi). Genetica 134: 79–87. DOI: 10.1007/s10709‐007‐9221‐y.

Kynast RG, Joseph JA, Pellicer J, Ramsay MM and Rudall PJ (2014) Chromosome behavior at the base of the angiosperm radiation: karyology of Trithuria submersa (Hydatellaceae, Nymphaeales). American Journal of Botany 101: 1447–1455. DOI: 10.3732/ajb.1400050.

Lécher R (1973) Microtubules, spindle and diffuse kinetochores in the Protozoan Aulacantha. Chromosomes Today 4: 225–234.

Luceño M (1994) Cytotaxonomic studies in Iberian, Balearic, North African, and Macaronesian species of Carex (Cyperaceae). II. Canadian Journal of Botany 72: 587–596.

Maddox PS, Oegema K, Desai A and Cheeseman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Research 12: 641–653. DOI: 10.1023/B:CHRO.0000036588.42225.2f.

Mahanty HK (1970) A cytological study of the Zingiberales with special reference to their taxonomy. Cytologia (Tokyo) 35: 13–49. DOI: 10.1508/cytologia.35.13.

Maiato H, DeLuca J, Salmon ED and Earnshaw WC (2004) The dynamic kinetochore‐microtubule interface. Journal of Cell Science 117: 5461–5477. DOI: 10.1242/jcs.01536.

Malik HS and Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138: 1067–1082. DOI: 10.1016/j.cell.2009.08.036.

Marques A and Pedrosa‐Harand A (2016) Holocentromere identity: from the typical mitotic linear structure to the great plasticity of meiotic holocentromeres. Chromosoma 125: 669–681. DOI: 10.1007/s00412‐016‐0612‐7.

Márquez‐Corro JI, Escudero M and Luceño M (2018) Do holocentric chromosomes represent an evolutionary advantage? A study of paired analyses of diversification rates of lineages with holocentric chromosomes and their monocentric closest relatives. Chromosome Research 26: 139–152. DOI: 10.1007/s10577‐017‐9566‐8.

Márquez‐Corro JI, Martín‐Bravo S, Spalink D, Luceño M and Escudero M (2019) Inferring hypothesis‐based transitions in clade‐specific models of chromosome number evolution in sedges (Cyperaceae). Molecular Phylogenetics and Evolution 135: 203–209. DOI: 10.1016/j.ympev.2019.03.006.

McEwen BF and Dong Y (2010) Contrasting models for kinetochore microtubule attachment in mammalian cells. Cellular and Molecular Life Sciences 67: 2163–2172. DOI: 10.1007/s00018‐010‐0322‐x.

Melters DP, Paliulis LV, Korf IF and Chan SWL (2012) Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Research. DOI: 10.1007/s10577‐012‐9292‐1.

Mola LM and Papeschi AG (2006) Holocentric chromosomes at a glance. Journal of Basic & Applied Genetics 17: 17–33.

Monen J, Maddox PS, Hyndman F, Oegema K and Desai A (2005) Differential role of CENP‐A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nature Cell Biology 7: 1248–1255. DOI: 10.1038/ncb1331.

Moraes ICR, Lermontova I and Schubert I (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Molecular Biology 75: 253–261. DOI: 10.1007/s11103‐010‐9723‐3.

Nagaki K, Kashihara K and Murata M (2005) Visualization of diffuse centromeres with centromere‐specific histone H3 in the holocentric plant Luzula nivea. Plant Cell 17: 1886–1893. DOI: 10.1105/tpc.105.032961.

Neumann P, Navrátilová A, Schroeder‐Reiter E, et al. (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genetics 8: e1002777. DOI: 10.1371/journal.pgen.1002777.

Neumann P, Pavlíková Z, Koblížková A, et al. (2015) Centromeres off the hook: massive changes in centromere size and structure following duplication of CenH3 gene in Fabeae species. Molecular Biology and Evolution 32: 1862–1879. DOI: 10.1093/molbev/msv070.

Nordenskiöld H (1962) Studies of meiosis in Luzula purpurea. Hereditas 48: 503–519. DOI: 10.1111/j.1601‐5223.1962.tb01828.x.

Pérez R, Panzera F, Page J, Suja JA and Rufas JS (1997) Meiotic behaviour of holocentric chromosomes: orientation and segregation of autosomes in Triatoma infestans (Heteroptera). Chromosome Research 5: 47–56. DOI: 10.1023/A:1018493419208.

Schrader F (1935) Notes on the mitotic behavior of long chromosomes. Cytologia (Tokyo) 6: 422–430.

Shakes DC, Wu J, Sadler PL, et al. (2009) Spermatogenesis‐specific features of the meiotic program in Caenorhabditis elegans. PLoS Genetics 5: e1000611. DOI: 10.1371/journal.pgen.1000611.

Stear JH and Roth MB (2002) Characterization of HCP‐6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes & Development 16: 1498–1508. DOI: 10.1101/gad.989102.

Strandhede S‐O (1965) Chromosome studies in Eleocharis, subser. Palustres I. Meiosis in some forms with 15 chromosomes. Hereditas 53: 47–62. DOI: 10.1111/j.1601‐5223.1965.tb01979.x.

Vershinina AO and Lukhtanov VA (2017) Evolutionary mechanisms of runaway chromosome number change in Agrodiaetus butterflies. Scientific Reports 7: 8199. DOI: 10.1038/s41598‐017‐08525‐6.

Viera A, Page J and Rufas JS (2009) Inverted meiosis: The true bugs as a model to study. Meiosis 5: 137–156. DOI: 10.1159/000166639.

Wahl HA (1940) Chromosome numbers and meiosis in the genus Carex. American Journal of Botany 27: 458–470. DOI: 10.1002/j.1537‐2197.1940.tb14707.x.

Zedek F and Bureš P (2019) Pest arthropods with holocentric chromosomes are more resistant to sterilizing ionizing radiation. Radiation Research 191: 255–261. DOI: 10.1667/RR15208.1.

Zedek F and Bureš P (2018) Holocentric chromosomes: from tolerance to fragmentation to colonization of the land. Annals of Botany 121: 9–16. DOI: 10.1093/aob/mcx118.

Zedek F, Veselý P, Horová L and Bureš P (2016) Flow cytometry may allow microscope‐independent detection of holocentric chromosomes in plants. Scientific Reports 6: 27161. DOI: 10.1038/srep27161.

Further Reading

Heckmann S and Houben A (2013) Holokinetic centromeres. In: Plant Centromere Biology, pp 83–94. Wiley‐Blackwell: Oxford, UK. DOI: 10.1002/9781118525715.ch7.

Schvarzstein M, Wignall SM and Villeneuve AM (2010) Coordinating cohesion, co‐orientation, and congression during meiosis: lessons from holocentric chromosomes. Genes & Development 24: 219–228. DOI: 10.1101/gad.1863610.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Márquez‐Corro, José Ignacio, Martín‐Bravo, Santiago, Pedrosa‐Harand, Andrea, Hipp, Andrew L, Luceño, Modesto, and Escudero, Marcial(Oct 2019) Karyotype Evolution in Holocentric Organisms. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028758]