Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
27255216
PubMed Central
PMC4891681
DOI
10.1038/srep27161
PII: srep27161
Knihovny.cz E-resources
- MeSH
- Cell Nucleus genetics radiation effects ultrastructure MeSH
- Chromosomes, Plant radiation effects ultrastructure MeSH
- Phylogeny MeSH
- Microscopy MeSH
- Flow Cytometry MeSH
- Plants genetics radiation effects ultrastructure MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Two chromosomal structures, known as monocentric and holocentric chromosomes, have evolved in eukaryotes. Acentric fragments of monocentric chromosomes are unequally distributed to daughter cells and/or lost, while holocentric fragments are inherited normally. In monocentric species, unequal distribution should generate chimeras of cells with different nuclear DNA content. We investigated whether such differences in monocentric species are detectable by flow cytometry (FCM) as (i) a decreased nuclear DNA content and (ii) an increased coefficient of variance (CV) of the G1 peak after gamma radiation-induced fragmentation. We compared 13 monocentric and 9 holocentric plant species. Unexpectedly, monocentrics and holocentrics did not differ with respect to parameters (i) and (ii) in their response to gamma irradiation. However, we found that the proportion of G2 nuclei was highly elevated in monocentrics after irradiation, while holocentrics were negligibly affected. Therefore, we hypothesize that DNA-damaging agents induce cell cycle arrest leading to endopolyploidy only in monocentric and not (or to much lesser extent) in holocentric plants. While current microscope-dependent methods for holocentrism detection are unreliable for small and numerous chromosomes, which are common in holocentrics, FCM can use somatic nuclei. Thus, FCM may be a rapid and reliable method of high-throughput screening for holocentric candidates across plant phylogeny.
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Melters D. P., Paliulis L. V., Korf I. F. & Chan S. W. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 20, 579–593 (2012). PubMed
Bureš P., Zedek F. & Marková M. Plant Genome Diversity Volume 2. (eds Leitch I. et al.) Holocentric chromosomes, 67–82 (Springer-Verlag: Wien,, 2013).
Nordenskiöld H. A study of meiosis in progeny of x-irradiated Luzula purpurea. Hereditas 49, 33–47 (1963).
Sheikh S. A., Kondo K. & Hoshi Y. Study of diffused centromeric nature of Drosera chromosomes. Cytologia 60, 43–47 (1995).
Stear J. & Roth M. Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes Dev. 16, 1498–1508 (2002). PubMed PMC
Lowden M., Flibotte S., Moerman D. & Ahmed S. DNA synthesis generates terminal duplications that seal end-to-end chromosome fusions. Science 332, 468–471 (2011). PubMed PMC
Jankowska M. et al. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma, doi: 10.1007/s00412-015-0524-y (2015). PubMed DOI
Nokkala S., Kuznetsova V., Maryanska-Nadachowska A. & Nokkala C. Holocentric chromosomes in meiosis. I. Restriction of the number of chiasmata in bivalents. Chromosome Res. 12, 733–739 (2004). PubMed
Heckmann S. & Houben A. Plant centromere biology (eds Jiang J. & Birchler J. A.) Holokinetic centromeres, 83–94 (Wiley-Blackwell, Oxford, UK 2013).
Lukhtanov V. et al. Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature 436, 385–389 (2005). PubMed
d’Alençon E. et al. Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. PNAS 107, 7680–7685 (2010). PubMed PMC
Zedek F., Šmerda J., Šmarda P. & Bureš P. Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biol. 10, 265 (2010). PubMed PMC
Lipnerová I., Bureš P., Horová L. & Šmarda P. Evolution of genome size in Carex (Cyperaceae) in relation to chromosome number and genomic base composition. Ann. Bot. 111, 79–94 (2013). PubMed PMC
Escudero M. et al. Genome size stability despite high chromosome number variation in Carex gr. laevigata. Am. J. Bot. 102, 233–238 (2015). PubMed
Marques A. et al. Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. PNAS 112, 13633–13638 (2015). PubMed PMC
Davey J. W. et al. Major Improvements to the Heliconius melpomene Genome Assembly Used to Confirm 10 Chromosome Fusion Events in 6 Million Years of Butterfly Evolution. G3 (Bethesda), doi: 10.1534/g3.115.023655 (2016). PubMed DOI PMC
Escudero M., Hipp A. L., Hansen T. F., Voje K. L. & Luceño M. Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). New Phytol. 195, 237–247 (2012). PubMed
Zedek F. & Bureš P. Evidence for centromere drive in the holocentric chromosomes of Caenorhabditis. PLoS One 7, e30496 (2012). PubMed PMC
Bureš P. & Zedek F. Holokinetic drive: Centromere drive in chromosomes without centromeres. Evolution 68, 2412–2420 (2014). PubMed
Traut W., Sahara K. & Marec F. Sex chromosomes and sex determination in Lepidoptera. Sex Dev. 1, 332–346 (2007). PubMed
Sahara K., Yoshido A. & Traut W. Sex chromosome evolution in moths and butterflies. Chromosome Res. 20, 83–94 (2012). PubMed
Šíchová J. et al. Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis. Biol. J. Linn. Soc., doi: 10.1111/bij.12756 (2016). DOI
Nordenskiöld H. Tetrad analysis and the course of meiosis in three hybrids of Luzula campestris. Hereditas 47, 203–238 (1961).
Mavarez J. et al. Speciation by hybridization in Heliconius butterflies. Nature 441, 868–871 (2006). PubMed
Lukhtanov V. A., Shapoval N. A., Anokhin B. A., Saifitdinova A. F. & Kuznetsova V. G. Homoploid hybrid speciation and genome evolution via chromosome sorting. Proc. Biol. Sci. 22, 282(1807) (2015). PubMed PMC
Mola L. M. & Papeschi A. G. Holokinetic chromosomes at a glance. J. Basic Appl. Genet. 17, 17–33 (2006).
Eichenlaub-Ritter U. & Ruthmann A. Holokinetic composite chromosomes with “diffuse” kinetochores in the micronuclear mitosis of a heterotrichous ciliate. Chromosoma 84, 701–716 (1982).
Godward M. B. E. The Chromosomes of the Algae (ed. Godward M. B. E.) Conjugales, 24–51 (Edward Arnold, London, 1966).
Wrensch D. L., Kethley J. B. & Norton R. A. Mites: Ecological and Evolutionary Analyses of Life-Story Patterns (ed. Houck M. A.) Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes, 282–342 (Chapman and Hall, New York, 1994).
Guerra M. et al. Neocentrics and holokinetics (holocentrics): chromosomes out of the centromeric rules. Cytogenet. Genome Res. 129, 82–96 (2010). PubMed
Otto F. J. & Oldiges H. Flow cytogenetic studies in chromosomes and whole cells for the detection of clastogenic effects. Cytometry 1, 13–17 (1980). PubMed
Otto F. J., Oldiges H., Göhde W. & Jain V. K. Flow cytometric measurement of nuclear DNA content variations as a potential in vivo mutagenicity test. Cytometry 2, 189–191 (1981). PubMed
McMurphy L. M. & Rayburn A. L. Nuclear alterations of maize plants grown in soil contaminated with coal fly ash. Arch. Environ. Con. Tox. 25, 520–524 (1993).
Rayburn A. L. & Wetzel J. B. Flow Cytometric Analyses of Intraplant Nuclear DNA Content Variation Induced by Sticky Chromosomes. Cytometry 49, 36–41 (2002). PubMed
Yamaguchi H. et al. Effects of ion beam irradiation on mutation induction and nuclear DNA content in Chrysanthemum. Breeding Science 60, 398–404 (2010).
Kahrizi Z. A., Kermani M. J. & Amiri M. Effect of gamma rays on nuclear DNA content in different rose genotypes. Int. Res. J. Appl. Basic Sci. 3, 1155–1160 (2012).
Šmarda P. et al. Ecological and evolutionary significance of genomic GC content diversity in monocots. PNAS 111, E4096–E4102 (2014). PubMed PMC
Šmarda P. & Bureš P. Understanding intraspecific variation in genome size in plants. Preslia 82, 41–61 (2010).
Otto F. Methods in cell biology Vol. 33 (eds Crissman H. A. & Darzynkiewicz Z.) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA, 105–110 (Academic Press New York, NY, 1990).
Šmarda P., Bureš P., Šmerda J. & Horová L. Measurements of genomic GC content in plant genomes with flow cytometry: A test for reliability. New Phytol. 193, 513–521 (2012). PubMed
Doležel J., Greilhuber J. & Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2, 2233–2244 (2007). PubMed
Kynast R. G., Joseph J. A., Pellicer J., Ramsay M. M. & Rudall P. J. Chromosome behavior at the base of the angiosperm radiation: karyology of Trithuria submerse (Hydatellaceae, Nymphaeales). Am. J. Bot. 101, 1447–1455 (2014). PubMed
Ivanov A. et al. Endopolyploid cells produced after severe genotoxic damage have the potential to repair DNA double strand breaks. J. Cell Sci. 116, 4095–4106 (2003). PubMed
Erenpreisa J., Cragg M. S., Salmina K., Hausmann M. & Scherthan H. The role of meiotic cohesin REC8 in chromosome segregation in gamma irradiation-induced endopolyploid tumour cells. Exp. Cell Res. 315, 2593–2603 (2009). PubMed
Mirzayans R., Andrais B., Scott A., Wang Y. W. & Murray D. Ionizing radiation-induced responses in human cells with differing TP53 status. Int. J. Mol. Sci. 14, 22409–22435 (2013). PubMed PMC
Adachi S. et al. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. PNAS 108, 10004–10009 (2011). PubMed PMC
Gegas V. C. et al. Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV-B. J. Exp. Bot. 65, 2757–2766 (2014). PubMed PMC
Yamasaki S., Shimada E., Kuwano T., Kawano T. & Noguchi N. Continuous UV-B irradiation induces endoreduplication and peroxidase activity in epidermal cells surrounding trichomes on cucumber cotyledons. J. Radiat. Res. 51, 187–196 (2010). PubMed
Evans L. S. Cell Cycle Kinetics of Endoreduplication in Gamma-Irradiated Root Meristems of Pisum sativum. Am. J. Bot. 65, 1084–1090 (1978).
Yoshiyama K. O., Sakaguchi K. & Kimura S. DNA damage response in plants: conserved and variable response compared to animals. Biology (Basel) 2, 1338–1356 (2013). PubMed PMC
Barow M. Endopolyploidy in seed plants. BioEssays 28, 271–281 (2006). PubMed
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