Unambiguous chromosome identification reveals the factors impacting irregular chromosome behaviors in allotriploid AAC Brassica.
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
04 Oct 2024
04 Oct 2024
Historique:
received:
10
04
2024
accepted:
31
08
2024
medline:
4
10
2024
pubmed:
4
10
2024
entrez:
4
10
2024
Statut:
epublish
Résumé
The major irregular chromosome pairing and mis-segregation were detected during meiosis through unambiguous chromosome identification and found that allotriploid Brassica can undergo meiosis successfully and produce mostly viable aneuploid gametes. Triploids have played a crucial role in the evolution of species by forming polyploids and facilitating interploidy gene transfer. It is widely accepted that triploids cannot undergo meiosis normally and predominantly produce nonfunctional aneuploid gametes, which restricts their role in species evolution. In this study, we demonstrated that natural and synthetic allotriploid Brassica (AAC), produced by crossing natural and synthetic Brassica napus (AACC) with Brassica rapa (AA), exhibits basically normal chromosome pairing and segregation during meiosis. Homologous A chromosomes paired faithfully and generally segregated equally. Monosomic C chromosomes were largely retained as univalents and randomly entered daughter cells. The primary irregular meiotic behaviors included associations of homoeologs and 45S rDNA loci at diakinesis, as well as homoeologous chromosome replacement and premature sister chromatid separation at anaphase I. Preexisting homoeologous arrangements altered meiotic behaviors in both chromosome irregular pairing and mis-segregation by increasing the formation of A-genomic univalents and A-C bivalents, as well as premature sister chromatid separation and homologous chromosome nondisjunction. Meiotic behaviors depended significantly on the genetic background and heterozygous homoeologous rearrangement. AAC triploids mainly generated aneuploid gametes, most of which were viable. These results demonstrate that allotriploid Brassica containing an intact karyotype can proceed through meiosis successfully, broadening our current understanding of the inheritance and role in species evolution of allotriploid.
Identifiants
pubmed: 39365356
doi: 10.1007/s00122-024-04734-6
pii: 10.1007/s00122-024-04734-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
245Subventions
Organisme : National Natural Science Foundation of China
ID : 31560302，31871239
Organisme : National Natural Science Foundation of China
ID : 32260337
Organisme : National Natural Science Foundation of China
ID : 32260508
Organisme : Inner Mongolia Key Technology Research Plan
ID : 2020GG0080
Organisme : Inner Mongolia Natural Science Foundation
ID : 2020ZD09
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Armstrong K, Keller W (1982) Chromosome pairing in haploids of Brassica oleracea. Can J Genet Cytol 24:735–739
doi: 10.1139/g82-079
Attia T, Busso C, Röbbelen G (1987) Digenomic triploids for an assessment of chromosome relationships in the cultivated diploid Brassica species. Genome 29:326–330
doi: 10.1139/g87-053
Baroux C, Pecinka A, Fuchs J, Kreth G, Schubert I, Grossniklaus U (2017) Non-random chromosome arrangement in triploid endosperm nuclei. Chromosoma 126:115–124
pubmed: 26892012
doi: 10.1007/s00412-016-0578-5
Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129:1–22
pubmed: 33874422
doi: 10.1111/j.1469-8137.1995.tb03005.x
Brock RD, Pryor AJ (1996) An unstable minichromosome generates variegated oil yellow maize seedlings. Chromosoma 104:575–584
pubmed: 8662250
doi: 10.1007/BF00352297
Cao Y, Zhao K, Xu J, Wu L, Hao F, Sun M, Dong J, Chao G, Zhang H, Gong X, Chen Y, Chen C, Qian W, Pires JC, Edger PP, Xiong Z (2023) Genome balance and dosage effect drive allopolyploid formation in Brassica. Proc Natl Acad Sci USA 120:e2217672120
pubmed: 36989303
pmcid: 10083598
doi: 10.1073/pnas.2217672120
De Storme N, Mason A (2014) Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance. Curr Plant Biol 1:10–33
doi: 10.1016/j.cpb.2014.09.002
Farco GE, Dematteis M (2014) Meiotic behavior and pollen fertility in triploid and tetraploid natural populations of Campuloclinium macrocephalum (Eupatorieae, Asteraceae). Plant Syst Evol 300:1843–1852
doi: 10.1007/s00606-014-1011-2
Gaebelein R, Alnajar D, Koopmann B, Mason AS (2019) Hybrids between Brassica napus and B. nigra show frequent pairing between the B and A/C genomes and resistance to blackleg. Chromosome Res 27:221–236
pubmed: 31280459
doi: 10.1007/s10577-019-09612-2
Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417
pubmed: 18024568
pmcid: 2174891
doi: 10.1105/tpc.107.054346
Garnier-Géré PH, Naciri-Graven Y, Bougrier S, Magoulas A, Héral M, Kotoulas G, Hawkins A, Gérard A (2002) Influences of triploidy, parentage and genetic diversity on growth of the Pacific oyster Crassostrea gigas reared in contrasting natural environments. Mol Ecol 11:1499–1514
pubmed: 12144669
doi: 10.1046/j.1365-294X.2002.01531.x
Ge XH, Li ZY (2007) Intra- and intergenomic homology of B-genome chromosomes in trigenomic combinations of the cultivated Brassica species revealed by GISH analysis. Chromosome Res 15:849–861
pubmed: 17899408
doi: 10.1007/s10577-007-1168-4
Gonzalo A, Lucas MO, Charpentier C, Sandmann G, Lloyd A, Jenczewski E (2019) Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus. Nat Commun 10:2354
pubmed: 31142748
pmcid: 6541637
doi: 10.1038/s41467-019-10010-9
Grandont L, Cuñado N, Coriton O, Huteau V, Eber F, Chèvre AM, Grelon M, Chelysheva L, Jenczewski E (2014) Homoeologous chromosome sorting and progression of meiotic recombination in Brassica napus: Ploidy does matter. Plant Cell 26:1448–1463
pubmed: 24737673
pmcid: 4036564
doi: 10.1105/tpc.114.122788
Han F, Gao Z, Yu W, Birchler JA (2007) Minichromosome analysis of chromosome pairing, disjunction, and sister chromatid cohesion in maize. Plant Cell 19:3853–3863
pubmed: 18083907
pmcid: 2217637
doi: 10.1105/tpc.107.055905
Harlan JR, deWet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390
doi: 10.1007/BF02860830
Hasegawa T, Harada N, Ikeda K, Ishii T, Hokuto I, Kasai K, Tanaka M, Fukuzawa R, Niikawa N, Matsuo N (1999) Digynic triploid infant surviving for 46 days. Am J Med Genet 87:306–310
pubmed: 10588835
doi: 10.1002/(SICI)1096-8628(19991203)87:4<306::AID-AJMG5>3.0.CO;2-6
He L, Braz GT, Torres GA, Jiang J (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513
pubmed: 30242479
doi: 10.1007/s00412-018-0682-9
Henry IM, Dilkes BP, Tyagi AP, Lin HY, Comai L (2009) Dosage and parent-of-origin effects shaping aneuploid swarms in A. thaliana. Heredity (Edinb) 103:458–468
pubmed: 19603060
doi: 10.1038/hdy.2009.81
Henry IM, Dilkes BP, Young K, Watson B, Wu H, Comai L (2005) Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics 170:1979–1988
pubmed: 15944363
pmcid: 1449780
doi: 10.1534/genetics.104.037788
Higgins EE, Howell EC, Armstrong SJ, Parkin IAP (2021) A major quantitative trait locus on chromosome A9, BnaPh1, controls homoeologous recombination in Brassica napus. New Phytol 229:3281–3293
pubmed: 33020949
doi: 10.1111/nph.16986
Hu F, Fan J, Qin Q, Huo Y, Wang Y, Wu C, Liu Q, Li W, Chen X, Liu C, Tao M, Wang S, Zhao R, Luo K, Liu S (2019) The sterility of allotriploid fish and fertility of female autotriploid fish. Front Genet 10:377
pubmed: 31105746
pmcid: 6498098
doi: 10.3389/fgene.2019.00377
Husband BC (2004) The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biol J Linn Soc 82:537–546
doi: 10.1111/j.1095-8312.2004.00339.x
Husband BC, Sabara HA (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol 161:703–713
pubmed: 33873724
doi: 10.1046/j.1469-8137.2004.00998.x
Iliopoulos D, Vassiliou G, Sekerli E, Sidiropoulou V, Tsiga A, Dimopoulou D, Voyiatzis N (2005) Long survival in a 69, XXX triploid infant in Greece. Genet Mol Res 4:755–759
pubmed: 16475122
Jenczewski E, Frédérique E, Agnès G, Huet S, Anne Marie C (2003) PrBn, a major gene controlling homeologous pairing in oilseed rape (Brassica napus) haploids. Genetics 164:645–653
pubmed: 12807785
pmcid: 1462591
doi: 10.1093/genetics/164.2.645
Jørgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting AK (2011) Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae). BMC Evol Biol 11:346
pubmed: 22126410
pmcid: 3247304
doi: 10.1186/1471-2148-11-346
Kamstra SA, Jong JHD, Jacobsen E, Ramanna MS, Kuipers AGJ (2004) Meiotic behaviour of individual chromosomes in allotriploid Alstroemeria hybrids. Heredity (Edinb) 93:15–21
pubmed: 15100711
doi: 10.1038/sj.hdy.6800465
Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci USA 101:13554–13559
pubmed: 15342909
pmcid: 518793
doi: 10.1073/pnas.0403659101
Kerzendorfer C, Vignard J, Pedrosa-Harand A, Siwiec T, Akimcheva S, Jolivet S, Sablowski R, Armstrong S, Schweizer D, Mercier R, Schlögelhofer P (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J Cell Sci 119:2486–2496
pubmed: 16763194
doi: 10.1242/jcs.02967
Kishimoto T, Yamakawa M, Nakazawa D, Amano J, Kuwayama S, Nakano M (2014) Meiotic chromosome pairing in intergeneric hybrids of colchicaceous ornamentals revealed by genomic in situ hybridization (GISH). Euphytica 200:251–257
doi: 10.1007/s10681-014-1152-y
Kolář F, Čertner M, Suda J, Schönswetter P, Husband BC (2017) Mixed-ploidy species: progress and opportunities in polyploid research. Trends Plant Sci 22:1041–1055
pubmed: 29054346
doi: 10.1016/j.tplants.2017.09.011
Kosmala A, Zwierzykowska E, Zwierzykowski Z (2006) Chromosome pairing in triploid intergeneric hybrids of Festuca pratensis with Lolium multiflorum, revealed by GISH. J Appl Genet 47:215–220
pubmed: 16877799
doi: 10.1007/BF03194626
Kovalsky IE, Roggero Luque JM, Elías G, Fernández SA, Solís Neffa VG (2018) The role of triploids in the origin and evolution of polyploids of Turnera sidoides complex (Passifloraceae, Turneroideae). J Plant Res 131:77–89
pubmed: 28831641
doi: 10.1007/s10265-017-0974-9
Ksiazczyk T, Taciak M, Zwierzykowski Z (2010) Variability of ribosomal DNA sites in Festuca pratensis, Lolium perenne, and their intergeneric hybrids, revealed by FISH and GISH. J Appl Genet 51:449–460
pubmed: 21063062
doi: 10.1007/BF03208874
Lavia GI, Ortiz AM, Robledo G, Fernandez A, Seijo G (2011) Origin of triploid Arachis pintoi (Leguminosae) by autopolyploidy evidenced by FISH and meiotic behaviour. Ann Bot 108:103–111
pubmed: 21693666
pmcid: 3119619
doi: 10.1093/aob/mcr108
Leflon M, Eber F, Letanneur JC, Chelysheva L, Coriton O, Huteau V, Ryder CD, Barker G, Jenczewski E, Chèvre AM (2006) Pairing and recombination at meiosis of Brassica rapa (AA) × Brassica napus (AACC) hybrids. Theor Appl Genet 113:1467–1480
pubmed: 16983552
doi: 10.1007/s00122-006-0393-0
Leflon M, Grandont L, Eber F, Huteau V, Coriton O, Chelysheva L, Jenczewski E, Chèvre AM (2010) Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 22:2253–2264
pubmed: 20622148
pmcid: 2929096
doi: 10.1105/tpc.110.075986
Li YJ, Gao YC, Zhou H, Ma HY, Li JQ, Arai K (2015) Meiotic chromosome configurations in triploid progeny from reciprocal crosses between wild-type diploid and natural tetraploid loach Misgurnus anguillicaudatus in China. Genetica 143:555–562
pubmed: 26130482
doi: 10.1007/s10709-015-9853-2
Loidl J (1995) Meiotic chromosome pairing in triploid and tetraploid Saccharomyces cerevisiae. Genetics 139:1511–1520
pubmed: 7789756
pmcid: 1206480
doi: 10.1093/genetics/139.4.1511
Lu C, Kato M (2001) Fertilization fitness and relation to chromosome number in interspecific progeny between Brassica napus and B. rapa: A comparative study using natural and resynthesized B. napus. Breed Sci 51:73–81
doi: 10.1270/jsbbs.51.73
Maguire MP (1987) Meiotic behavior of a tiny fragment chromosome that carries a transposed centromere. Genome 29:744–747
pubmed: 3436523
doi: 10.1139/g87-126
Mason AS, Pires JC (2015) Unreduced gametes: meiotic mishap or evolutionary mechanism. Trends Genet 31:5–10
pubmed: 25445549
doi: 10.1016/j.tig.2014.09.011
McClintock B (1929) A cytological and genetical study of triploid maize. Genetics 14:180–222
pubmed: 17246573
pmcid: 1201029
doi: 10.1093/genetics/14.2.180
Mikkelsen TR, Jensen J, Jørgensen RB (1996) Inheritance of oilseed rape (Brassica napus) RAPD markers in a backcross progeny with Brassica campestris. Theor Appl Genet 92:492–497
pubmed: 24166276
doi: 10.1007/BF00223698
Morinaga T (1929) Interspecific hybridization in Brassica I. The cytology of F 1 hybrids of B. napella and various other species with 10 chromosomes. Cytologia 1:16–27
doi: 10.1508/cytologia.1.16
Namai H (1976) Cytogenetic and breeding studies on transfer of economic characters by means of interspecific and intergeneric crossing in the tribe Brassiceae of Cruciferae. Mem Fac Agr, Tokyo Univ Educ 22:101–171
Nicolas SD, Leflon M, Monod H, Eber F, Coriton O, Huteau V, Chevre AM, Jenczewski E (2009) Genetic regulation of meiotic cross-overs between related genomes in Brassica napus haploids and hybrids. Plant Cell 21:373–385
pubmed: 19190241
pmcid: 2660629
doi: 10.1105/tpc.108.062273
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437
pubmed: 11092833
doi: 10.1146/annurev.genet.34.1.401
Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781
pubmed: 16020789
pmcid: 1456786
doi: 10.1534/genetics.105.042093
Parkin IA, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38:1122–1131
pubmed: 18470236
doi: 10.1139/g95-149
Pelé A, Falque M, Trotoux G, Eber F, Nègre S, Gilet M, Huteau V, Lodé M, Jousseaume T, Dechaumet S, Morice J, Poncet C, Coriton O, Martin OC, Rousseau-Gueutin M, Chèvre A-M (2017) Amplifying recombination genome-wide and reshaping crossover landscapes in Brassicas. PLoS Genet 13:e1006794
pubmed: 28493942
pmcid: 5444851
doi: 10.1371/journal.pgen.1006794
Pendinen G, Spooner DM, Jiang J, Gavrilenko T (2012) Genomic in situ hybridization reveals both auto- and allopolyploid origins of different North and Central American hexaploid potato (Solanum sect. Petota) species. Genome 55:407–415
pubmed: 22594521
doi: 10.1139/g2012-027
Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1:e13
doi: 10.4081/pb.2010.e13
Petukhova GV, Romanienko PJ, Camerini-Otero RD (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev Cell 5:927–936
pubmed: 14667414
doi: 10.1016/S1534-5807(03)00369-1
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501
doi: 10.1146/annurev.ecolsys.29.1.467
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639
doi: 10.1146/annurev.ecolsys.33.010802.150437
Rhoades MM (1940) Studies of a telocentric chromosome in maize with reference to the stability of its centromere. Genetics 25:483–520
pubmed: 17246983
pmcid: 1209104
doi: 10.1093/genetics/25.5.483
Samans B, Chalhoub B, Snowdon RJ (2017) Surviving a genome collision: genomic signatures of allopolyploidization in the recent crop species Brassica napus. Plant Genome. https://doi.org/10.3835/plantgenome2017.02.0013
doi: 10.3835/plantgenome2017.02.0013
pubmed: 29293818
Sandfaer J (1975) The occurrence of spontaneous triploids in different barley varieties. Hereditas 80:149–153
doi: 10.1111/j.1601-5223.1975.tb01511.x
Sevilleno SS, An HR, Cabahug-Braza RAM, Ahn Y-J, Hwang Y-J (2023) Cytogenetic study and pollen viability of Phalaenopsis Queen Beer ‘Mantefon.’ Plants (Basel) 12:2828
pubmed: 37570982
Sharpe AG, Parkin IA, Keith DJ, Lydiate DJ (1995) Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 38:1112–1121
pubmed: 18470235
doi: 10.1139/g95-148
Sheltzer JM, Amon A (2011) The aneuploidy paradox: costs and benefits of an incorrect karyotype. Trends Genet 27:446–453
pubmed: 21872963
pmcid: 3197822
doi: 10.1016/j.tig.2011.07.003
St Charles J, Hamilton ML, Petes TD (2010) Meiotic chromosome segregation in triploid strains of Saccharomyces cerevisiae. Genetics 186:537–550
pubmed: 20697121
doi: 10.1534/genetics.110.121533
Szadkowski E, Eber F, Huteau V, Lodé M, Coriton O, Jenczewski E, Chèvre AM (2011) Polyploid formation pathways have an impact on genetic rearrangements in resynthesized Brassica napus. New Phytol 191:884–894
pubmed: 21517871
doi: 10.1111/j.1469-8137.2011.03729.x
Szadkowski E, Eber F, Huteau V, Lodé M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux MJ, Delourme R, King GJ, Chalhoub B, Jenczewski E, Chèvre AM (2010) The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol 186:102–112
pubmed: 20149113
doi: 10.1111/j.1469-8137.2010.03182.x
Toda E, Okamoto T (2016) Formation of triploid plants via possible polyspermy. Plant Signal Behav 11:e1218107
pubmed: 27617495
pmcid: 5058460
doi: 10.1080/15592324.2016.1218107
Toda E, Okamoto T (2020) Polyspermy in angiosperms: Its contribution to polyploid formation and speciation. Mol Reprod Dev 87:374–379
pubmed: 31736192
doi: 10.1002/mrd.23295
Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homologous recombination in four mapping populations of Brassica napus L. Genetics 169:967–979
pubmed: 15520255
pmcid: 1449096
doi: 10.1534/genetics.104.033209
Wang J, Huo B, Liu W, Li D, Liao L (2017) Abnormal meiosis in an intersectional allotriploid of Populus L. and segregation of ploidy levels in 2x × 3x progeny. PLoS ONE 12:e0181767
pubmed: 28732039
pmcid: 5521839
doi: 10.1371/journal.pone.0181767
Xiong Z, Gaeta RT, Edger PP, Cao Y, Zhao K, Zhang S, Pires JC (2021) Chromosome inheritance and meiotic stability in allopolyploid Brassica napus. G3 (Bethesda) 11:jkaa011
pubmed: 33704431
doi: 10.1093/g3journal/jkaa011
Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci USA 108:7908–7913
pubmed: 21512129
pmcid: 3093481
doi: 10.1073/pnas.1014138108
Xiong Z, Pires JC (2011) Karyotype and identification of all homoeologous chromosomes of allopolyploid Brassica napus and its diploid progenitors. Genetics 187:37–49
pubmed: 21041557
pmcid: 3018299
doi: 10.1534/genetics.110.122473
Yang Y, Wei X, Shi G, Wei F, Braynen J, Zhang J, Tian B, Cao G, Zhang X (2017) Molecular and cytological analyses of A and C genomes at meiosis in synthetic allotriploid Brassica hybrids (ACC) between B. napus (AACC) and B. oleracea (CC). J Plant Biol 60:181–188
doi: 10.1007/s12374-016-0221-2
Yang Y, Yan G, Li Z, Yuan J, Wei X, Wei F, Tian B, Xie Z, Shi G, Zhang X, Cao G (2020) Cytological atlas at meiosis reveals insights into pollen fertility in synthetic Brassica allotriploids between allotetraploid B. carinata and diploid B. rapa. Plant Physiol Biochem 148:237–245
pubmed: 31981876
doi: 10.1016/j.plaphy.2020.01.003
Zhang C, Li Q, Zhu L, He W, Yang C, Zhang H, Sun Y, Zhou L, Sun Y, Zhu S, Wu C, Tao M, Zhou Y, Zhao R, Tang C, Liu S (2021) Abnormal meiosis in fertile and sterile triploid cyprinid fish. Sci China Life Sci 64:1917–1928
pubmed: 33893980
doi: 10.1007/s11427-020-1900-7
Zhang X, Cao Q, Zhou P, Jia G (2017) Meiotic chromosome behavior of the male-fertile allotriploid lily cultivar ‘Cocossa.’ Plant Cell Rep 36:1641–1653
pubmed: 28741131
doi: 10.1007/s00299-017-2180-6
Zheng YZ, Roseman RR, Carlson WR (1999) Time course study of the chromosome-type breakage-fusion-bridge cycle in maize. Genetics 153:1435–1444
pubmed: 10545471
pmcid: 1460833
doi: 10.1093/genetics/153.3.1435
Zoshchuk NV, Badaeva ED, Zelenin AV (2003) History of modern chromosomal analysis. Differential staining of plant chromosomes. Ontogenez 34:5–18
pubmed: 12625068
Zwierzykowski Z, Lukaszewski AJ, Naganowska B, Lesniewska A (1999) The pattern of homoeologous recombination in triploid hybrids of Lolium multiflorum with Festuca pratensis. Genome 42:720–726
doi: 10.1139/g98-169