Unambiguous chromosome identification reveals the factors impacting irregular chromosome behaviors in allotriploid AAC Brassica.

Publisher: Springer Country of Publication: Germany NLM ID: 0145600 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-2242 (Electronic) Linking ISSN: 00405752 NLM ISO Abbreviation: Theor Appl Genet Subsets: MEDLINE

Original Publication: Berlin, New York, Springer

Chromosomes, Plant*/genetics ; Meiosis* ; Chromosome Pairing*; Brassica napus/genetics ; Brassica napus/growth & development ; Chromosome Segregation/genetics ; Triploidy ; Brassica rapa/genetics ; Brassica/genetics ; Brassica/physiology ; Aneuploidy

Key Message: 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.
(© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Armstrong K, Keller W (1982) Chromosome pairing in haploids of Brassica oleracea. Can J Genet Cytol 24:735–739. (PMID: 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. (PMID: 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. (PMID: 2689201210.1007/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. (PMID: 3387442210.1111/j.1469-8137.1995.tb03005.x)
Brock RD, Pryor AJ (1996) An unstable minichromosome generates variegated oil yellow maize seedlings. Chromosoma 104:575–584. (PMID: 866225010.1007/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. (PMID: 369893031008359810.1073/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. (PMID: 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. (PMID: 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. (PMID: 3128045910.1007/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. (PMID: 18024568217489110.1105/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. (PMID: 1214466910.1046/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. (PMID: 1789940810.1007/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. (PMID: 31142748654163710.1038/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. (PMID: 24737673403656410.1105/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. (PMID: 18083907221763710.1105/tpc.107.055905)
Harlan JR, deWet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390. (PMID: 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. (PMID: 1058883510.1002/(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. (PMID: 3024247910.1007/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. (PMID: 1960306010.1038/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. (PMID: 15944363144978010.1534/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. (PMID: 3302094910.1111/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. (PMID: 31105746649809810.3389/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. (PMID: 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. (PMID: 3387372410.1046/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. (PMID: 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. (PMID: 12807785146259110.1093/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. (PMID: 22126410324730410.1186/1471-2148-11-346)
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. (PMID: 1510071110.1038/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. (PMID: 1534290951879310.1073/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. (PMID: 1676319410.1242/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. (PMID: 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. (PMID: 2905434610.1016/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. (PMID: 1687779910.1007/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. (PMID: 2883164110.1007/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. (PMID: 2106306210.1007/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. (PMID: 21693666311961910.1093/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. (PMID: 1698355210.1007/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. (PMID: 20622148292909610.1105/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. (PMID: 2613048210.1007/s10709-015-9853-2)
Loidl J (1995) Meiotic chromosome pairing in triploid and tetraploid Saccharomyces cerevisiae. Genetics 139:1511–1520. (PMID: 7789756120648010.1093/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. (PMID: 10.1270/jsbbs.51.73)
Maguire MP (1987) Meiotic behavior of a tiny fragment chromosome that carries a transposed centromere. Genome 29:744–747. (PMID: 343652310.1139/g87-126)
Mason AS, Pires JC (2015) Unreduced gametes: meiotic mishap or evolutionary mechanism. Trends Genet 31:5–10. (PMID: 2544554910.1016/j.tig.2014.09.011)
McClintock B (1929) A cytological and genetical study of triploid maize. Genetics 14:180–222. (PMID: 17246573120102910.1093/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. (PMID: 2416627610.1007/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. (PMID: 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. (PMID: 19190241266062910.1105/tpc.108.062273)
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437. (PMID: 1109283310.1146/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. (PMID: 16020789145678610.1534/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. (PMID: 1847023610.1139/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. (PMID: 28493942544485110.1371/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. (PMID: 2259452110.1139/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. (PMID: 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. (PMID: 1466741410.1016/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. (PMID: 10.1146/annurev.ecolsys.29.1.467)
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639. (PMID: 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. (PMID: 17246983120910410.1093/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. (PMID: 10.3835/plantgenome2017.02.001329293818)
Sandfaer J (1975) The occurrence of spontaneous triploids in different barley varieties. Hereditas 80:149–153. (PMID: 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. (PMID: 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. (PMID: 1847023510.1139/g95-148)
Sheltzer JM, Amon A (2011) The aneuploidy paradox: costs and benefits of an incorrect karyotype. Trends Genet 27:446–453. (PMID: 21872963319782210.1016/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. (PMID: 2069712110.1534/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. (PMID: 2151787110.1111/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. (PMID: 2014911310.1111/j.1469-8137.2010.03182.x)
Toda E, Okamoto T (2016) Formation of triploid plants via possible polyspermy. Plant Signal Behav 11:e1218107. (PMID: 27617495505846010.1080/15592324.2016.1218107)
Toda E, Okamoto T (2020) Polyspermy in angiosperms: Its contribution to polyploid formation and speciation. Mol Reprod Dev 87:374–379. (PMID: 3173619210.1002/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. (PMID: 15520255144909610.1534/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. (PMID: 28732039552183910.1371/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. (PMID: 3370443110.1093/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. (PMID: 21512129309348110.1073/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. (PMID: 21041557301829910.1534/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. (PMID: 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. (PMID: 3198187610.1016/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. (PMID: 3389398010.1007/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. (PMID: 2874113110.1007/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. (PMID: 10545471146083310.1093/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. (PMID: 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. (PMID: 10.1139/g98-169)

31560302，31871239 National Natural Science Foundation of China; 32260337 National Natural Science Foundation of China; 32260508 National Natural Science Foundation of China; 2020GG0080 Inner Mongolia Key Technology Research Plan; 2020ZD09 Inner Mongolia Natural Science Foundation

Date Created: 20241004 Date Completed: 20241004 Latest Revision: 20241013

20241014

10.1007/s00122-024-04734-6

39365356