Abstract
The maize B chromosome typically undergoes nondisjunction during the second microspore division. For normal A chromosomes, the r-X1 deficiency in maize can induce nondisjunction during the second megaspore and first microspore divisions. However, it is not known whether the r-X1 deficiency also induces nondisjunction of the maize B chromosome during these cell divisions. To answer this question, chromosome numbers were determined in the progeny of r-X1/R-r female parents carrying two B chromosomes. Some of the r-X1-lacking progeny (21.2%) contained zero or two B chromosomes. However, a much higher percentage of the r-X1-containing progeny (43.4%) exhibited zero or two B chromosomes, but none displayed more than two B chromosomes. Thus, the results indicated that the r-X1 deficiency could also induce nondisjunction of the B chromosome during the second megaspore division; moreover, the B chromosome in itself could undergo nondisjunction during the same division. In addition, pollen grains from plants with two B chromosomes lacking or exhibiting the r-X1 deficiency were compared via pollen fluorescence in situ hybridization (FISH) using a B chromosome-specific probe. The results revealed that the r-X1 deficiency could induce the occurrence of B chromosome nondisjunction during the first microspore division and that the B chromosome in itself could undergo nondisjunction during the same division at a lower frequency. Our data shed more light on the behavior of the maize B chromosome during cell division.
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Abbreviations
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- FISH:
-
Fluorescence in situ hybridization
- FITC:
-
Fluorescein isothiocyanate
- RFLP:
-
Restriction fragment length polymorphism
References
Camacho JPM (2005) B chromosome. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286. https://doi.org/10.1016/B978-012301463-4/50006-1
Carlson WR (1973) A procedure for localizing genetic factors controlling mitotic nondisjunction in the B chromosome of maize. Chromosoma 42(2):127–136. https://doi.org/10.1007/BF00320935
Carlson WR (1988) B chromosomes as a model system for nondisjunction. In: Alan R (ed) Aneuploidy, part B: induction and test system. Liss, New York, pp 199–207
Carlson WR, Roseman RR (1992) A new property of the maize B chromosome. Genetics 131(1):211–223
Cheng YM (2010) Evolution of the heterochromatic regions on maize B long arm based on the sequence structure of CL-repeat variants. Chromosom Res 18(5):605–619. https://doi.org/10.1007/s10577-010-9136-9
Cheng YM, Feng YR, Lin YP, Peng SF (2016) Cytomolecular characterization and origin of de novo formed maize B chromosome variants. Chromosom Res 24(2):183–195. https://doi.org/10.1007/s10577-015-9516-2
Chiavarino AM, Rosato M, Manzanero S, Jiménez G, González-Sánchez M, Puertas MJ (2000) Chromosome nondisjunction and instabilities in tapetal cells are affected by B chromosomes in maize. Genetics 155(2):889–897
Han F, Gao Z, Yu W, Birchler JA (2007) Minichromosome analysis of chromosome pairing, disjunction, and sister chromatid cohesion in maize. Plant Cell 19(12):3853–3863. https://doi.org/10.1105/tpc.107.055905
Holm C, Stearns T, Botstein D (1989) DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol 9(1):159–168. https://doi.org/10.1128/MCB.9.1.159
Jones RN, Rees H (1982) B chromosomes. Academic Press, London
Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: so what? Ann Bot 101(6):767–775. https://doi.org/10.1093/aob/mcm167
Kermicle JL (1970) Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66(1):69–85
Kuwada Y (1915) Ueber die Chromosomenzahl von Zea Mays L. Bot Mag Tokyo 29(342):83–89. 10.15281/jplantres1887.29.342_83
Lin BY (1977) A squash technique for studying the cytology of maize endosperm and other tissues. Stain Technol 52(4):197–201. https://doi.org/10.3109/10520297709116775
Lin BY (1978) Regional control of nondisjunction of the B-chromosome in maize. Genetics 90(3):613–627
Lin BY (1979) Two new B-10L translocations involved in the control of nondisjunction of the B chromosome in maize. Genetics 92(3):931–945
Lin BY (1987) Cytological evidence of terminal deficiencies produced by the r-X1 deficiency in maize. Genome 29(5):718–721. https://doi.org/10.1139/g87-123
Lin BY, Coe EH Jr (1986) Monosomy and trisomy induced by the r-Xl deletion in maize, and associated effects on endosperm development. Can J Genet Cytol 28(5):831–834. https://doi.org/10.1139/g86-115
Lin BY, Marquette K, Sallee P (1990) Characterization of deficiencies generated by r-X1 in maize. J Hered 81:359–364
Lin BY, Peng SF, Chen YJ, Chen HS, Kao CF (1997) Physical mapping of RFLP markers on four chromosome arms in maize using terminal deficiencies. Mol Gen Genet 256(5):509–516. https://doi.org/10.1007/s004380050595
Longley AE (1927) Supernumerary chromosomes in Zea mays. J Agric Res 35:769–784
Randolph LF (1941) Genetic characteristics of the B chromosomes in maize. Genetics 26(6):608–631
Rhoades MM (1968) Studies on the cytological basis of crossing over. In: Peacock WJ, Brock RD (eds) Replication and recombination of genetic material. Australian Acad Sci, Canberra, pp 229–241
Rhoades MM, Dempsey E (1972) On the mechanism of chromatin loss induced by the B chromosome of maize. Genetics 71(1):73–96
Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32(4):391–409
Roman H (1948) Directed fertilization in maize. Proc Natl Acad Sci U S A 34(2):36–42. https://doi.org/10.1073/pnas.34.2.36
Rusche ML, Mogensen HL, Shi L, Keim P, Rougier M, Chaboud A, Dumas C (1997) B chromosome behavior in maize pollen as determined by a molecular probe. Genetics 147(4):1915–1921
Shadley G, Weber DF (1990) Recovery of B-A translocations from monosomic plants containing one B chromosome. Maize Genet News Lett 64:92–93
Shi L, Zhu T, Mogensen HL, Keim P (1996) Sperm identification in maize by fluorescence in situ hybridization. Plant Cell 8(5):815–821. https://doi.org/10.1105/tpc.8.5.815
Simcox KD, Shadley JD, Weber DF (1987) Detection of the time of occurrence of nondisjunction induced by the r-X1 deficiency in Zea mays L. Genome 29(5):782–785. https://doi.org/10.1139/g87-131
Staub RW (1987) Leaf striping correlated with the presence of B chromosomes in maize. J Hered 78(2):71–74. https://doi.org/10.1093/oxfordjournals.jhered.a110339
Ward E (1973) Nondisjunction: localization of the controlling site in the maize B chromosome. Genetics 73(3):387–391
Weber DF (1983) Monosomic analysis in diploid crop plants. In: Swaminathan MS, Gupta PK, Sinha U (eds) Cytogenetics of crop plants. Macmillan India Limited, New Delhi, pp 351–378
Weber DF, Chao L (1994) The r-X1 deficiency system induces nondisjunction in the early embryo in maize. Maydica 39:29–33
Yu W, Han F, Gao Z, Vega JM, Birchler JA (2007) Construction and behavior of engineered minichromosomes in maize. Proc Natl Acad Sci U S A 104(21):8924–8929. https://doi.org/10.1073/pnas.0700932104
Zhao ZY, Weber DF (1988) Analysis of nondisjunction induced by the r-X1 deficiency during microsporogenesis in Zea mays L. Genetics 119(4):975–980
Zheng YZ, Roseman RR, Carlson WR (1999) Time course study of the chromosome-type breakage-fusion-bridge cycle in maize. Genetics 153(3):1435–1444
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This work was supported by grants from the Ministry of Science and Technology, Taiwan (MOST 104-2311-B-005-012-MY3).
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Responsible Editor: Jiming Jiang
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Supplementary Fig. S1
The three types of maize ears used in this study. (a) A self-pollinated r-X1/R-r ear, in which the self-colored kernels lack the r-X1 deficiency, and the mottled kernels carry this deficiency. (b) A self-pollinated r/r ear. (c) An F1 ear from a cross of r-X1/R-r plants as the female parents with r/r males, whose colorless kernels harbor the r-X1 deficiency (GIF 436 kb)
Supplementary Fig. S2
Root-tip chromosomes of the inbred W22 line containing two B chromosomes. Arrows denote the B chromosome; the bar represents 10 μm (GIF 211 kb)
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Tseng, SH., Peng, SF. & Cheng, YM. Analysis of B chromosome nondisjunction induced by the r-X1 deficiency in maize. Chromosome Res 26, 153–162 (2018). https://doi.org/10.1007/s10577-017-9567-7
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DOI: https://doi.org/10.1007/s10577-017-9567-7