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Parental genome separation and asynchronous centromere division in interspecific F1 hybrids inLathyrus

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Abstract

Chromosomes were studied in root-tip metaphase cells of several F1 interspecificLathyrus hybrids including:L. hirsutus × L. cassius (H × C),L. cassius × L. hirsutus (C × H),L. cassius × L. odoratus (C × O), and their parents, all with 2n = 2x = 14. Two types of morphologically distinct centromeres were identified in the hybrids on the basis of the degree of contraction of the primary constriction. At least 12 well-defined centromeres were seen in all cells ofL. hirsutus, L. cassius andL. odoratus, and about 80% of cells had 14. The hybrids were more variable than the species. H × O contained between six and 14 welldefined centromeres, while cells of H × C, C × H and C × O all had seven well-defined and seven weakly defined centromeres. These were used as markers to plot their spatial disposition in two dimensions on metaphase spreads. In H × C, C × H and C × O the two types of centromeres showed a significant tendency to occupy two spatially distinct and concentrically arranged domains on the metaphase plate (P < 0.005). Owing to shortage of material subsequent work was restricted to H × C and C × H. Six or seven chromosomes of one parental genome were selectively labelled byin situ hybridization using biotinylated total genomic DNA from either parent as a probe. Moreover, there was a very strong correlation between centromere type and genomic origin (P < 0.001). Clearly the tendency for spatial segregation of parental genomes into concentrically arranged domains previously noted in several F1 interspecific sexual hybrids between grasses can occur strongly in dicots. The present work onLathyrus also included the first comparative study of the spatial arrangement of parental genomes in reciprocal hybrids. Significantly,L. cassius chromosomes tended to surroundL. hirsutus chromosomes in both H × C and C × H. Thus, the polarity of concentric parental genome separation was not determined as a maternal effect.

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References

  • Appels R, Dvorák J (1982) The wheat ribosomal DNA spacer region: its structure and variation in populations and among species.Theor Appl Genet 63: 337–348.

    Google Scholar 

  • Avivi L, Feldman M, Brown M (1982) An ordered arrangement of chromosomes in the somatic nucleus of common wheatTriticum aestivum. II. Spatial arrangements between chromosomes of different genomes.Chromosoma 86: 17–26.

    Google Scholar 

  • Bailey JP, Bennett ST, Bennett MD, Stace CA (1993) Genomicin situ hybridization identifies parental chromosomes in the wild grass hybrid ×Festulpia hubbardii.Heredity 71: 413–420.

    Google Scholar 

  • Bammi RK (1962) ‘Complement fractionation’ in a natural hybrid betweenRubus procerus Muell. andR. laciniatus Willd.Nature 208: 608.

    Google Scholar 

  • Bennett MD (1982) Nucleotypic basis of the spatial ordering of chromosomes in eukaryotes and the implications of order for genome evolution and phenotypic variation. In: Dover GA, Flavell RB, eds.Genome Evolution. London: Academic Press, pp 239–261.

    Google Scholar 

  • Bennett MD (1983) The spatial distribution of chromosomes. In: Brandham PE, Bennett MD, eds.Kew Chromosome Conference II. London: Allen & Unwin, pp 71–79.

    Google Scholar 

  • Bennett MD (1984) Nuclear architecture and its manipulation. In: Gustafson JP, ed.Gene Manipulation In Plant Improvement. New York: Plenum Press, pp 469–502.

    Google Scholar 

  • Bennett MD (1988) Parental genome separation in F1 hybrids between grass species. In: Brandham PE, ed.Kew Chromosome Conference III. London: HMSO, pp 195–208.

    Google Scholar 

  • Bennett ST, Bennett MD (1992) Spatial separation of ancestral genomes in the wild grassMilium montianum Parl.Ann Bot 70: 111–118.

    Google Scholar 

  • Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms.Phil Trans R Soc Lond 274: 227–274.

    Google Scholar 

  • Bennett ST, Kenton AY, Bennett MD (1992) Genomicin situ hybridization reveals the allopolyploid nature ofMilium montianum (Gramineae).Chromosoma 101: 420–424.

    Google Scholar 

  • Borden J, Manuelidis L (1988) Movement of the X chromosome in epilepsy.Science 242: 1687–1691.

    PubMed  Google Scholar 

  • Brandriff BF, Gordon LA, Segraves R, Pinkel D (1991) The male-derived genome after sperm-egg fusion: spatial distribution of chromosomal DNA and paternal—maternal genomic association.Chromosoma 100: 262–266.

    PubMed  Google Scholar 

  • Brinkley BR, Valdivia MM, Tousson A, Balczon R (1989) The kinetochore: structure and molecular organization. In: Hyams JS, Brinkley BR, eds.Mitosis: Molecules and Mechanisms. London: Academic Press, pp 77–118.

    Google Scholar 

  • Constabel F, Weber G, Kirkpatrick JW (1977) Sur la compatibilité des chromosomes dans les hybrides intergénériques de cellules deGlycine max × Vicia hajastana.C R Acad Sci Paris 285: 319–322.

    Google Scholar 

  • Earnshaw WC, Bernat RB (1991) Chromosomal passengers: Toward an integrated view of mitosis.Chromosoma 100: 139–146.

    PubMed  Google Scholar 

  • Finch RA (1983) Tissue-specific elimination of alternative whole parental genomes in one barley hybrid.Chromosoma 88: 386–393.

    Google Scholar 

  • Finch RA, Bennett MD (1983) The mechanism of somatic chromosome elimination inHordeum. In: Brandham PE, Bennett MD, eds.Kew Chromosome Conference II. London: Allen & Unwin, pp 147–154.

    Google Scholar 

  • Finch RA, Smith JB, Bennett MD (1981)Hordeum andSecale mitotic genomes lie apart in a hybrid.J Cell Sci 52: 391–403.

    PubMed  Google Scholar 

  • Flavell RB, Sardana R, Jackson S, O'Dell M (1990) The molecular basis of variation affecting gene expression: evidence from studies on the ribosomal RNA gene loci of wheat. In: Gustafson JP, ed.Gene Manipulation in Plant Improvement II. 19th Stadler Genetics Symposium. New York: Plenum Press, pp 419–430.

    Google Scholar 

  • Geber G, Schweizer D (1988) Cytochemical heterochromatin differentiation inSinapis alba (Cruciferae) using a simple airdrying technique for producing chromosome spreads.Pl Syst Evol 158: 97–106.

    Google Scholar 

  • Gilissen LJW, van Staveran MJ, Verhoeven, HA, Sree Ramunlu K (1992) Somatic hybridization between potato andNicotiana plumbaginifolia. 1. Spontaneous biparental chromosome elimination and production of asymmetric hybrids.Theor Appl Genet 84: 73–80.

    Google Scholar 

  • Gleba YY, Parokonny AS, Kotov V, Negrutiu I, Momot V (1987) Spatial separation of parental genomes in hybrids of somatic plant cells.Proc Natl Acad Sci USA 84: 3709–3713.

    Google Scholar 

  • Graves JAM, Zelesco PA (1988) Chromosome segregation from cell hybrids. V. Does segregation result from asynchronous centromere separation?Genome 30: 124–128.

    PubMed  Google Scholar 

  • Hägale K, Oschmann B (1987) Non-reciprocal gonadal dysgenesis in hybrids of the chironomid midgeChironomus thummi.Chromosoma 96: 50–54.

    PubMed  Google Scholar 

  • Hochstrasser M, Sedat JW (1987) Three-dimensional organization ofDrosophila melanogaster interphase nuclei. II. Chromosomal spatial organization and gene regulation.J Cell Biol 104: 1455–1470.

    PubMed  Google Scholar 

  • Holm C, Stearns T, Botstein D (1989) DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage.Mol Cell Biol 9: 159–168.

    PubMed  Google Scholar 

  • Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of theNicotiana tabacum L. genome by molecular cytogenetics.Mol Gen Genet 240: 159–169.

    PubMed  Google Scholar 

  • Kubai DF (1987) Nonrandom chromosome arrangements in germ line nuclei ofSciara coprophila males: the basis for nonrandom chromosome segregation on the meiosis I spindle.J Cell Biol 105: 2433–2466.

    PubMed  Google Scholar 

  • Kupicha FK (1983) The infrageneric structure ofLathyrus.Notes RBG Edin 41: 209–244.

    Google Scholar 

  • Leitch AR, Schwarzacher T, Mosgöller W, Bennett MD, Heslop-Harrison JS (1991) Parental genomes are separated throughout the cell cycle in a plant hybrid.Chromosoma 101: 206–213.

    Google Scholar 

  • Linde-Laursen I, Jensen J (1984) Separate location of parental chromosomes in squashed metaphases of hybrids betweenHordeum vulgare L. and four polyploid, alien species.Hereditas 100: 67–73.

    Google Scholar 

  • Linde-Laursen I, Jensen J (1991) Genome and chromosome disposition at somatic metaphase in aHordeum × Psathyrostachys hybrid.Heredity 66: 203–210.

    Google Scholar 

  • Madan K, Lindhout D, Palan A (1987) Premature centromere division (PCD): a dominantly inherited cytogenetic anomaly.Hum Genet 77: 193–196.

    PubMed  Google Scholar 

  • Manuelidis L (1985) Individual interphase chromosome domains revealed byin situ hybridization.Hum Genet 71: 288–293.

    PubMed  Google Scholar 

  • Murray BG, Hammett KRW (1989)L. chloranthus × L. chrysanthus: a new interspecific hybrid.Bot Gaz 150: 469–476.

    Google Scholar 

  • Murray BG, Hammett KRW, Herrick JF (1993) Relationships betweenLathyrus cassius, L. odoratus andL. hirsutus assessed by experimental hybridization, analysis of meiotic pairing and DNA:DNA hybridization.Int Plant Sci 154: 163–168.

    Google Scholar 

  • Parokonny AS, Kenton A, Gleba YY, Bennett MD (1994) The fate of recombinant chromosomes and genome interaction inNicotiana asymmetric hybrids and their sexual progeny.Theor Appl Genet (in press).

  • Pohler W, Clauss E (1984) Differences in chromosomal stability, chromosome pairing, and rhythm of nuclear division between the parental genomes in an amphidiploid hybrid from the crossHordeum vulgare L. ×Secale montanum Guss.Arch Züchtungforsch Berl 14: 214–224.

    Google Scholar 

  • Pohler W, Clauss E (1988) Genomic allocycly — a hypothesis originally developed for triticale proved valid forHordeum × Secale hybrids.Tag. -Ber Akad Landwirtsch-Wiss DDR, Berlin 266: 105–114.

    Google Scholar 

  • Rudd NL, Teshima IE, Martin RH, Sisken JE, Weksberg R (1983) A dominantly inherited cytogenetic anomaly: a possible cell division mutant.Hum Genet 65: 117–122.

    PubMed  Google Scholar 

  • Schwarzacher T, Leitch AR, Bennett MD, Heslop-Harrison JS (1989)In situ localization of parental genomes in a wide hybrid.Ann Bot 64: 315–324.

    Google Scholar 

  • Schwarzacher T, Heslop-Harrison JS, Anamthawat-Jónsson K, Finch RA, Bennett MD (1992) Parental genome separation in reconstructions of somatic and premeiotic metaphases ofHordeum vulgare × H. bulbosum.J Cell Sci 101: 13–24.

    Google Scholar 

  • Schwarzacher-Robinson T, Finch RA, Smith JB, Bennett MD (1987) Genotypic control of centromere positions of parental genomes inHordeum × Secale hybrid metaphases.J Cell Sci 87: 291–304.

    Google Scholar 

  • Sumner AT (1991) Scanning electron microscopy of mammalian chromosomes from prophase to telophase.Chromosoma 100: 410–418.

    PubMed  Google Scholar 

  • Tomkins D, Hunter A, Roberts M (1979) Cytogenetic findings in Roberts — SC phocomelia syndrome(s).Am J Med Genet 4: 17–26.

    PubMed  Google Scholar 

  • Vig BK (1983) Sequence of centromere separation: occurrence, possible significance, and control.Cancer Genet Cytogenet 8: 249–274.

    PubMed  Google Scholar 

  • Vig BK, Athwal RS (1989) Sequence of centromere separation: separation in a quasi-stable mouse—human somatic cell hybrid.Chromosoma 98: 167–173.

    PubMed  Google Scholar 

  • Yacobi YS, Levanony H, Feldman M (1985a) An ordered arrangement of bivalents at first meiotic metaphase of wheat. I. Hexaploid wheat.Chromosoma 91: 347–354.

    Google Scholar 

  • Yacobi YS, Levanony H, Feldman M (1985b) An ordered arrangement of bivalents at first meiotic metaphase of wheat. II. Tetraploid wheat.Chromosoma 91: 355–358.

    Google Scholar 

  • Yanagida M (1989) Gene products required for chromosome separation.J Cell Sci (Suppl)12: 213–229.

    Google Scholar 

  • Zelesco PA, Graves JAM (1988) Chromosome segregation from cell hybrids. IV. Movement and position of segregant set chromosomes in early-phase interspecific cell hybrids.J Cell Sci 89: 49–56.

    PubMed  Google Scholar 

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Author notes

  1. B. G. Murray

    Present address: School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland, New Zealand

  2. M. A. Callimassia

    Present address: Medical Genetics, Churchill Hospital, OX3 7LJ, Oxford, UK

Authors and Affiliations

  1. Jodrell Laboratory, Royal Botanic Gardens, TW9 3DS, Kew, Richmond, Surrey, UK

    M. A. Callimassia, B. G. Murray & M. D. Bennett

  2. Horticulture and Food Research Institute of New Zealand, Private Bag 92169, Auckland, New Zealand

    K. R. W. Hammett

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Callimassia, M.A., Murray, B.G., Hammett, K.R.W. et al. Parental genome separation and asynchronous centromere division in interspecific F1 hybrids inLathyrus . Chromosome Res 2, 383–397 (1994). https://doi.org/10.1007/BF01552798

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  • DOI: https://doi.org/10.1007/BF01552798

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