Allohexaploids in the Genus Brassica

Critical Reviews in Plant Sciences

Volumn 37, Issue 5, 2018, Pages 422-437

  Gaebelein, Roman ^a   Mason, Annaliese S ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Brassica; interspecific hybridization; meiotic stability; polyploidy

Indexed keywords

EID: 85055676648     PISSN: 07352689     EISSN: 15497836     Source Type: Journal    
DOI: 10.1080/07352689.2018.1517143     Document Type: Article

References (84)

1. Arumugam, N., Mukhopadhyay, A., Gupta, V., Pental, D., and Pradhan, A. K. 1996. Synthesis of hexaploid (AABBCC) somatic hybrids: a bridging material for transfer of ‘tour’ cytoplasmic male sterility to different Brassica species. Theor. Appl. Genet. 92: 762–768
2. Bansal, P., Banga, S., and Banga, S. S. 2012. Heterosis as investigated in terms of polyploidy and genetic diversity using designed Brassica juncea amphiploid and its progenitor diploid species. PLoS One 7: 1–15
3. Bhullar, R., Nagarajan, R., Bennypaul, H., Sidhu, G. K., Sidhu, G., Rustgi, S., Wettstein, D. Von, and Gill, K. S. 2014. Silencing of a metaphase I-specific gene results in a phenotype similar to that of the pairing homeologous 1 (Ph1) gene mutations. Proc. Natl. Acad. Sci. U.S.A. 111: 14187–14192
4. Blary, A., Gonzalo, A., Eber, F., Berard, A., Berges, H., Bessoltane, N., Charif, D., Charpentier, C., Cromer, L., Fourment, J., Genevriez, C., Le Paslier, M. C., Lode, M., Lucas, M. O., Nesi, N., Lloyd, A., Chevre, A. M., and Jenczewski, E. 2018. FANCM limits meiotic crossovers in Brassica crops. Frontiers in Plant Science 9: 368
5. Bouttier, C., and Morgan, D. G. 1992. Ovule development and determination of seed number per pod in oilsed rape (Brassica napus L.). J. Exp. Bot. 43: 709–714
6. Busso, C., Attia, T., and Röbbelen, G. 1987. Trigenomic combinations for the analysis of meiotic control in the cultivated Brassica species. Genome 29: 331–333
7. B.Chalhoub, F.Denoeud, S.Liu, I.A.P.Parkin, H.Tang, X.Wang, J.Chiquet, H.Belcram, C.Tong, B.Samans, M.Correa, Da C.Silva, J.Just, C.Falentin, C.Koh, S., Le I.Clainche, M.Bernard, P.Bento, B.Noel, K.Labadie, A.Alberti, M.Charles, D.Arnaud, H.Guo, C.Daviaud, S.Alamery, K.Jabbari, M.Zhao, P.P.Edger, H.Chelaifa, D.Tack, G.Lassalle, I.Mestiri, N.Schnel, Le M.C.Paslier, G.Fan, V.Renault, P.E.Bayer, A.A.Golicz, S.Manoli, T.H.Lee, V.H.D.Thi, S.Chalabi, Q.Hu, C.Fan, R.Tollenaere, Y.Lu, C.Battail, J.Shen, C.H.D.Sidebottom, A.Canaguier, A.Chauveau, A.Berard, G.Deniot, M.Guan, Z.Liu, F.Sun, Y.P.Lim, E.Lyons, C.D.Town, I.Bancroft, J.Meng, J.Ma, J.C.Pires, G.J.King, D.Brunel, R.Delourme, M.Renard, J.M.Aury, K.L.Adams, J.Batley, R.J.Snowdon, J.Tost, D.Edwards, Y.Zhou, W.Hua, A.G.Sharpe, A.H.Paterson, C.Guan, and Wincker, P. 2014. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345: 950–953
8. Chen, J., Ge, X., Yao, X., Feng, Y., and Li, Z. 2011a. Synthesis and characterization of interspecific trigenomic hybrids and allohexaploids between three cultivated Brassica allotetraploids and wild species. African J. Biotechnol. 10: 12171–12176
9. Chen, L. P., Ge, Y. M., and Zhu, X. Y. 2006. Artificial synthesis of interspecific chimeras between tuber mustard (Brassica juncea) and cabbage (Brassica oleracea) and cytological analysis. Plant Cell Rep. 25: 907–913
10. Chen, L.-P., Zhang, M.-F., Li, C.-S., and Hirata, Y. 2005. Production of interspecific somatic hybrids between tuber mustard (Brassica juncea) and red cabbage (Brassica oleracea). Plant Cell. Tissue Organ Cult. 80: 305–311
11. Chen, S., Nelson, M. N., Chèvre, A.-M., Jenczewski, E., Li, Z., Mason, A. S., Meng, J., Plummer, J. A., Pradhan, A., Siddique, K. H. M. 2011b. Trigenomic bridges for Brassica improvement. Crit. Rev. Plant Sci. 30: 524–547
12. Chèvre, A., Barret, P., Eber, F., Dupuy, P., Brun, H., Tanguy, X., and Renard, M. 1997. Selection of stable Brassica napus-B. juncea recombinant lines resistant to blackleg (Leptosphaeria maculans). 1. Identification of molecular markers, chromosomal and genomic origin of the introgression. Theor. Appl. Genet. 95: 1104–1111
13. Chevre, A., Eber, F., This, P., Barret, P., Tanguy, X., Brun, H., Delseny, M., and Renard, M. 1996. Characterization of Brassica nigra chromosomes and of blackleg resistance in B. napus-B. nigra addition lines. Plant Breed. 115: 113–118
14. M.Cifuentes, L.Grandont, G.Moore, ChèA.M.vre, and Jenczewski, E. 2010. Genetic regulation of meiosis in polyploidy species: new insights into an old question. New Phytologist 186: 29–36
15. Cui, C., Ge, X., Gautam, M., Kang, L., and Li, Z. 2012. Cytoplasmic and genomic effects on meiotic pairing in Brassica hybrids and allotetraploids from pair crosses of three cultivated diploids. Genetics 191: 725–738
16. De Storme, N., and Mason, A. 2014. Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Curr. Plant Biol. 1: 10–33
17. Dixelius, C., and Wahlberg, S. 1999. Resistance to Leptosphaeria maculans is conserved in a specific region of the Brassica B genome. Theor. Appl. Genet. 99: 368–372
18. Eenink, A. H. 1974. Matromorphy in Brassica oleracea L. I. terminology, parthenogenesis in Cruciferae and the formation and usability of matromorphic plants. Euphytica 23: 429–433
19. Fitzjohn, R. G., Armstrong, T. T., Newstrom-Lloyd, L. E., Wilton, A. D., and Cochrane, M. 2007. Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape. Euphytica 158: 209–230
20. Ge, X. H., and Li, Z. Y. 2006. Extra divisions and nuclei fusions in microspores from Brassica allohexaploid (AABBCC) × Orychophragmus violaceus hybrids. Plant Cell Rep. 25: 1075–1080
21. Ge, X. H., and Li, Z. Y. 2007. Intra- and intergenomic homology of B-genome chromosomes in trigenomic combinations of the cultivated Brassica species revealed by GISH analysis. Chromosom. Res. 15: 849–861
22. X.H.Ge, J.Wang, and Z.Li, Y. 2009. Different genome-specific chromosome stabilities in synthetic Brassica allohexaploids revealed by wide crosses with Orychophragmus. Annals of Botany 104: 19–31
23. Gehringer, A., Snowdon, R., Spiller, T., Basunanda, P., and Friedt, W. 2007. New oilseed rape (Brassica napus) hybrids with high levels of heterosis for seed yield under nutrient-poor conditions. Breed. Sci. 57: 315–320
24. Gerdemann-Knöck, M., Sacristan, M. D., Braatz, C., and Schieder, O. 1994. Utilization of asymmetric somatic hybridization for the transfer of disease resistance from Brassica nigra to Brassica napus. Plant Breed. 113: 106–113
25. Greer, E., Martin, A. C., Pendle, A., Colas, I., Jones, A. M. E., Moore, G., and Shaw, P. 2012. The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24: 152–162
26. Griffiths, S., Sharp, R., Foote, T. N., Bertin, I., Wanous, M., Reader, S., Colas, I., and Moore, G. 2006. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439: 749–752
27. Gupta, M., Atri, C., Agarwal, N., and Banga, S. S. 2016. Development and molecular-genetic characterization of a stable Brassica allohexaploid. Theor. Appl. Genet. 129: 2085–2100
28. Heyn, F. J. W. 1977. Analysis of unreduced gametes in Brassiceae by crosses between species and ploidy levels. Zeitschrift Für Pflanzenzüchtung 78: 13–30
29. Howard, H. W. 1942. The effect of polyploidy and hybridity on seed size in crosses between Brassica chinensis, B. carinata, amphidiploid B. chinensis-carinata and auto-tetraploid B. chinensis. J. Genet. 43: 105–119
30. Iwasa, S. 1964. Cytogenetic studies on the artificially raised trigenomic hexaploid hybrid forms in the genus Brassica. J. Fac. Agric. Kyushu Univ. 13: 309–352
31. Jahier, J., Chevre, A. M., Tanguy, A. M., and Eber, F. 1989. Extraction of disomic addition lines of Brassica napus–Brassica nigra. Genome 32: 408–413
32. Jenczewski, E., Eber, F., Grimaud, A., Huet, S., Lucas, M. O., Monod, H., and Chèvre, A. M. 2003. PrBn, a major gene controlling homeologous pairing in oilseed rape (Brassica napus) haploids. Genetics 164: 645–653
33. Jiang, Y., Tian, E., Li, R., Chen, L., and Meng, J. 2007. Genetic diversity of Brassica carinata with emphasis on the interspecific crossability with B. rapa. Plant Breed. 126: 487–491
34. Kumari, P., Bisht, D. S., and Bhat, S. R. 2017. Stable, fertile somatic hybrids between Sinapis alba and Brassica juncea show resistance to Alternaria brassicae and heat stress. Plant Cell. Tissue Organ Cult. 133: 77–86
35. Leitch, A. R., and Leitch, I. J. 2008. Genomic plasticity and the diversity of polyploid plants. Science. 320: 481–484
36. Li, J., Rao, L., Meng, Q., Ghani, M. A., and Chen, L. 2015. Production of Brassica tri-genomic vegetable germplasm by hybridisation between tuber mustard (Brassica juncea) and red cabbage (B. oleracea). Euphytica 204: 323–333
37. Li, Q., Xiong, Z., Mei, J., Song, H., and Qian, W. 2017. Genetics and Epigenetic Alterations of Hexaploid Early Generation Derived from Hybrid Between Brassica napus and B. oleracea. BioRxiv
38. Lian, Y.-J., Lin, G.-Z., Zhao, X.-M., and Lim, H.-T. 2011. Production and genetic characterization of somatic hybrids between leaf mustard (Brassica juncea) and broccoli (Brassica oleracea). Vitr. Cell. Dev. Biol.–Plant 47: 289–296
39. Lloyd, A., and Bomblies, K. 2016. Meiosis in autopolyploid and allopolyploid Arabidopsis. Curr. Opin. Plant Biol. 30: 116–122
40. L.N.Lukens, J.C.Pires, E.Leon, R.Vogelzang, L.Oslach, and Osborn, T. 2006. Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiology 140: 336–348
41. Martín, A. C., Rey, M. D., Shaw, P., and Moore, G. 2017. Dual effect of the wheat Ph1 locus on chromosome synapsis and crossover. Chromosoma 126: 669–680
42. Mason, A. S., and Batley, J. 2015. Creating new interspecific hybrid and polyploid crops. Trends Biotechnol. 33: 436–441
43. Mason, A. S., Huteau, V., Eber, F., Coriton, O., Yan, G., Nelson, M. N., Cowling, W. A., and Chèvre, A. M. 2010. Genome structure affects the rate of autosyndesis and allosyndesis in AABC, BBAC and CCAB Brassica interspecific hybrids. Chromosom. Res. 18: 655–666
44. Mason, A. S., Nelson, M. N., Takahira, J., Cowling, W. A., Alves, G. M., Chaudhuri, A., Chen, N., Ragu, M. E., Dalton-Morgan, J., and Coriton, O. 2014. The fate of chromosomes and alleles in an allohexaploid Brassica population. Genetics 197: 273–283
45. Mason, A. S., Nelson, M. N., Yan, G., and Cowling, W. A. 2011. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol. 11: 103
46. Mason, A. S., and Pires, J. C. 2015. Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet. 31: 5–10
47. Mason, A., Takahira, J., Atri, C., Samans, B., Hayward, A., Cowling, W., Batley, J., and Nelson, M. 2015. Microspore culture reveals complex meiotic behaviour in a trigenomic Brassica hybrid. BMC Plant Biol. 15: 173
48. Mason, A. S., Rousseau-Gueutin, M., Morice, J., Bayer, P. E., Besharat, N., Cousin, A., Pradhan, A., Parkin, I. A. P., Chèvre, A. M., and Batley, J. 2016. Centromere locations in Brassica A and C genomes revealed through half-tetrad analysis. Genetics 202: 513–523
49. Mason, A. S., Yan, G., Cowling, W. A., and Nelson, M. N. 2012. A new method for producing allohexaploid Brassica through unreduced gametes. Euphytica 186: 277–287
50. Meng, J., Shi, S., Gan, L., Li, Z., and Qu, X. 1998. The production of yellow-seeded Brassica napus (AACC) through crossing interspecific hybrids of B. campestris (AA) and B. carinata (BBCC) with B. napus. Euphytica 103: 329–333
51. Mizushima, U. 1950. On several artificial allopolyploids obtained in the tribe Brassicaceae of Cruciferae. Tohoku J. Agric. Res. 1: 15–27
52. 1 hybrids of B. juncea and B. nigra. Cytologia (Tokyo). 6: 62–67
53. Mwathi, M. W., Gupta, M., Atri, C., Banga, S. S., Batley, J., and Mason, A. S. 2017. Segregation for fertility and meiotic stability in novel Brassica allohexaploids. Theor. Appl. Genet. 130: 767–776
54. Nicolas, S. D., Leflon, M., Monod, H., Eber, F., Coriton, O., Huteau, V., Chèvre, A.-M., and Jenczewski, E. 2009. Genetic regulation of meiotic cross-overs between related genomes in Brassica napus haploids and hybrids. Plant Cell 21: 373–385
55. Parkin, I. A. P., Sharpe, A. G., and Lydiate, D. J. 2003. Patterns of genome duplication within the Brassica napus genome. NRC Res. Press. 46: 291–303
56. Plieske, J., Struss, D., and Röbbelen, G. 1998. Inheritance of resistance derived from the B-genome of Brassica against Phoma lingam in rapeseed and the development of molecular markers. Theor. Appl. Genet. 97: 929–936
57. Pradhan, A., Plummer, J. A., Nelson, M. N., Cowling, W. A., and Yan, G. 2010. Trigenomic hybrids from interspecifi crosses between Brassica napus and B. nigra. Crop Pasture Sci. 61: 464–474
58. Purty, R. S., Kumar, G., Singla-Pareek, S. L., and Pareek, A. 2008. Towards salinity tolerance in Brassica: An overview. Physiol. Mol. Biol. Plants 14: 39–49
59. Rahman, M. H. 2001. Production of yellow-seeded Brassica napus through interspecific crosses. Plant Breed. 120: 463–472
60. Ramsey, J., and Schemske, D. W. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29: 467–501
61. Ramsey, J., and Schemske, D. W. 2002. Neopolyploidy in Flowering Plants. Annu. Rev. Ecol. Syst. 33: 589–639
62. Sacristán, M. D., Gerdemann-Knörck, M., and Schieder, O. 1989. Incorporation of hygromycin resistance in Brassica nigra and its transfer to B. napus through asymmetric protoplast fusion. Theor. Appl. Genet. 78: 194–200
63. Samans, B., Chalhoub, B., and Snowdon, R. J. 2017. Surviving a genome collision: genomic signatures of allopolyploidization in the recent crop species Brassica napus. Plant Genome 10: 1–15
64. Santos, J. L., Alfaro, D., Sanchez-Moran, E., Armstrong, S. J., Franklin, F. C. H., and Jones, G. H. 2003. Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165: 1533–1540
65. Sjödin, C., and Glimelius, K. 1989. Brassica naponigra, a somatic hybrid resistant to Phoma lingam. Theor. Appl. Genet. 77: 651–656
66. Soltis, P. S., and Soltis, D. E. 2016. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 30: 159–165
67. Spoelhof, J. P., Soltis, P. S., and Soltis, D. E. 2017. Pure polyploidy: closing the gaps in autopolyploid research. J. Syst. Evol. 55: 340–352
68. Sprague, S. J., Balesdent, M. H., Brun, H., Hayden, H. L., Marcroft, S. J., Pinochet, X., Rouxel, T., and Howlett, B. J. 2006. Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur. J. Plant Pathol. 114: 33–40
69. Struss, D., Bellin, U., and Röbbelen, G. 1991. Development of B-genome chromosome addition lines of B. napus using different interspecific Brassica hybrids. Plant Breed. 106: 209–214
70. Szadkowski, E., Eber, F., Huteau, V., Lodé, M., Huneau, C., Belcram, H., Coriton, O., Manzanares-Dauleux, M. J., Delourme, R., and King, G. J. 2010. The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol. 186: 102–112
71. Takeda, T., and Takahata, Y. 1996. Production of alloplasmic Chinese cabbage using synthesized trigenomic hexaploid (AABBCC) in Brassica. Acta Horticulturae. 407: 151–154
72. Tian, E., Jiang, Y., Chen, L., Zou, J., Liu, F., and Meng, J. 2010. Synthesis of a Brassica trigenomic allohexaploid (B. carinata × B. rapa) de novo and its stability in subsequent generations. Theor. Appl. Genet. 121: 1431–1440
73. Tonguç, M., and Griffiths, P. D. 2004. Development of black rot resistant interspecific hybrids between Brassica oleracea L. cultivars and Brassica accession A 19182, using embryo rescue. Euphytica 136: 313–318
74. U, Nagaharu. 1935. Genome-analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese J. Bot. 7: 389–452
75. Weerakoon, S. R. 2011. Producing inter-specific hybrids between Brassica juncea and B. oleracea to synthesize trigenomic Brassica. J. Sci. Univ. Kelaniya 6: 13–34
76. S.R.Weerakoon, P.Si, W.Zili, J.Meng, G.Yan, A.Sciences, and A.Sciences,. 2009. Production and confirmation of hybrids through interspecific crossing between tetraploid B. juncea and diploid B. oleracea towards a hexaploid Brassica population. Presented at 16th Australian Research Assembly on Brassicas, Victoria, Australia, September 14–16
77. Z.Wei, M.Wang, S.Chang, C.Wu, P.Liu, J.Meng, and J.Zou,. 2016. Introgressing subgenome components from Brassica rapa and B. carinata to B. juncea for broadening its genetic base and exploring intersubgenomic heterosis. Front. Plant Sci. 7: 1677
78. Wen, J., Zhu, L., Qi, L., Ke, H., Yi, B., Shen, J., Tu, J., Ma, C., and Fu, T. D. 2012. Characterization of interploid hybrids from crosses between Brassica juncea and B. oleracea and the production of yellow-seeded B. napus. Theor. Appl. Genet. 125: 19–32
79. Wittkop, B., Snowdon, R. J., and Friedt, W. 2009. Status and perspectives of breeding for enhanced yield and quality of oilseed crops for Europe. Euphytica 170: 131–140
80. Xiong, Z., Gaeta, R. T., and Pires, J. C. 2011. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc. Natl. Acad. Sci. U. S. A. 108: 7908–7913
81. Yamagishi, H., Hirai, M., Yoshikawa, H., and Yui, S. 1989. Production of somatic hybrid between black mustard (Brassica nigra Koch.; BB) and Hakuran (B. napus L.;AACC). Japanese J. Breed. 39: 369–375
82. Yang, S., Chen, S., Geng, X. X., Yan, G., Li, Z. Y., Meng, J. L., Cowling, W. A., and Zhou, W. J. 2016. The first genetic map of a synthesized allohexaploid Brassica with A, B and C genomes based on simple sequence repeat markers. Theor. Appl. Genet. 129: 689–701
83. Zhou, J., Chen, T., Cheng, C., Xianhong, G., and Zaiyun, L. 2016. Distinct subgenome stabilities in synthesized Brassica allohexaploids. Theor. Appl. Genet. 129: 1257–1271
84. Zou, J., Zhu, J., Huang, S., Tian, E., Xiao, Y., Fu, D., Tu, J., Fu, T., and Meng, J. 2010. Broadening the avenue of intersubgenomic heterosis in oilseed Brassica. Theor. Appl. Genet. 120: 283–290