Stable, fertile lines produced by hybridization between allotetraploids Brassica juncea (AABB) and Brassica carinata (BBCC) have merged the A and C genomes.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
05 2021
Historique:
received: 30 06 2020
accepted: 12 01 2021
pubmed: 22 1 2021
medline: 15 5 2021
entrez: 21 1 2021
Statut: ppublish

Résumé

Many flowering plant taxa contain allopolyploids that share one or more genomes in common. In the Brassica genus, crop species Brassica juncea and Brassica carinata share the B genome, with 2n = AABB and 2n = BBCC genome complements, respectively. Hybridization results in 2n = BBAC hybrids, but the fate of these hybrids over generations of self-pollination has never been reported. We produced and characterized B. juncea × B. carinata (2n = BBAC) interspecific hybrids over six generations of self-pollination under selection for high fertility using a combination of genotyping, fertility phenotyping, and cytogenetics techniques. Meiotic pairing behaviour improved from 68% bivalents in the F

Identifiants

pubmed: 33476056
doi: 10.1111/nph.17225
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1242-1257

Informations de copyright

© 2021 The Authors New Phytologist © 2021 New Phytologist Trust.

Références

Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229-246.
Alix K, Joets J, Ryder CD, Moore J, Barker GC, Bailey JP, King GJ, (Pat) Heslop-Harrison JS. 2008. The CACTA transposon Bot1 played a major role in Brassica genome divergence and gene proliferation. The Plant Journal 56: 1030-1044.
Attia T, Röbbelen G. 1986. Cytogenetic studies amphihaploids. Canadian Journal of Genetics and Cytology 28: 330-334.
Badaeva ED, Amosova AV, Muravenko OV, Samatadze TE, Chikida NN, Zelenin AV, Friebe B, Gill BS. 2002. Genome differentiation in Aegilops. 3. Evolution of the D-genome cluster. Plant Systematics and Evolution 231: 163-190.
Badaeva ED, Amosova AV, Samatadze TE, Zoshchuk SA, Shostak NG, Chikida NN, Zelenin AV, Raupp WJ, Friebe B, Gill BS. 2004. Genome differentiation in Aegilops. 4. Evolution of the U-genome cluster. Plant Systematics and Evolution 246: 45-76.
Bayer PE, Hurgobin B, Golicz AA, Chan CKK, Yuan Y, Lee HT, Renton M, Meng J, Li R, Long Y et al. 2017. Assembly and comparison of two closely related Brassica napus genomes. Plant Biotechnology Journal 15: 1602-1610.
Bird KA, VanBuren R, Puzey JR, Edger PP. 2018. The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytologist 220: 87-93.
Brennan AC, Barker D, Hiscock SJ, Abbott RJ. 2012. Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae). Heredity 108: 87-95.
Chalhoub B, Denoeud F, Liu S, Parkin Iap, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B et al. 2014. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345: 950-953.
Chang PL, Dilkes BP, McMahon M, Comai L, Nuzhdin SV. 2010. Homoeolog-specific retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and network partners. Genome Biology 11: R125.
Chen LP, Zhang MF, Li CS, Hirata Y. 2005. Production of interspecific somatic hybrids between tuber mustard (Brassica juncea) and red cabbage (Brassica oleracea). Plant Cell, Tissue and Organ Culture 80: 305-311.
Cheng F, Sun C, Wu J, Schnable J, Woodhouse MR, Liang J, Cai C, Freeling M, Wang X. 2016. Epigenetic regulation of subgenome dominance following whole genome triplication in Brassica rapa. New Phytologist 211: 288-299.
Chester M, Gallagher JP, Symonds VV, Cruz da Silva AV, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE. 2012. Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proceedings of the National Academy of Sciences, USA 109: 1176-1181.
Clarke WE, Higgins EE, Plieske J, Wieseke R, Sidebottom C, Khedikar Y, Batley J, Edwards D, Meng J, Li R et al. 2016. A high-density SNP genotyping array for Brassica napus and its ancestral diploid species based on optimised selection of single-locus markers in the allotetraploid genome. Theoretical and Applied Genetics 129: 1887-1899.
Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846.
Dubovets NI, Sycheva YA. 2017. Microevolutionary differentiation of cereal tetraploid species by the formation of recombinant genomes. Russian Journal of Genetics 7: 327-334.
Emery M, Willis MMS, Hao Y, Barry K, Oakgrove K, Peng Y, Schmutz J, Lyons E, Pires JC, Edger PP et al. 2018. Preferential retention of genes from one parental genome after polyploidy illustrates the nature and scope of the genomic conflicts induced by hybridization. PLoS Genetics 14: e1007267.
Fulton TM, Chunwongse J, Tanksley SD. 1995. Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13: 207-209.
Gaebelein R, Schiessl SV, Samans B, Batley J, Mason AS. 2019. Inherited allelic variants and novel karyotype changes influence fertility and genome stability in Brassica allohexaploids. New Phytologist 223: 965-978.
Garsmeur O, Schnable JC, Almeida A, Jourda C, D’Hont A, Freeling M. 2014. Two evolutionarily distinct classes of paleopolyploidy. Molecular Biology and Evolution 31: 448-454.
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 Research 15: 849-861.
Gou X, Bian Y, Zhang A, Zhang H, Wang B, Lv R, Li J, Zhu B, Gong L, Liu B. 2018. Transgenerationally precipitated meiotic chromosome instability fuels rapid karyotypic evolution and phenotypic diversity in an artificially constructed allotetraploid wheat (AADD). Molecular Biology and Evolution 35: 1078-1091.
Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G. 2006. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439: 749-752.
Grusz AL, Sigel EM, Witherup C. 2017. Homoeologous chromosome pairing across the eukaryote phylogeny. Molecular Phylogenetics and Evolution 117: 83-94.
Harper AL, Trick M, He Z, Clissold L, Fellgett A, Griffiths S, Bancroft I. 2016. Genome distribution of differential homoeologue contributions to leaf gene expression in bread wheat. Plant Biotechnology Journal 14: 1207-1214.
Inaba R, Nishio T. 2002. Phylogenetic analysis of Brassiceae based on the nucleotide sequences of the S-locus related gene, SLR1. Theoretical and Applied Genetics 105: 1159-1165.
Ising G. 1966. Cytogenetic studies in Cyrtanthus: IV. Chromosome morphology in Cyrtanthus luteus Baker (Anoiganthus luteus Baker) and Cyrtanthus breviflorus Harvey (Anoiganthus breviflorus Baker). Hereditas 63: 352-384.
James JK, Abbott RJ. 2005. Recent, allopatric, homoploid hybrid speciation: the origin of Senecio squalidus (Asteraceae) in the British Isles from hybrid zone on Mount Etna, Sicily. Evolution 59: 2533-2547.
Janečka J, Lysak MA. 2016. chromdraw: an R package for visualization of linear and circular karyotypes. Chromosome Research 24: 217-223.
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
Karlin S, Altschul SF. 1990. Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proceedings of the National Academy of Sciences, USA 87: 2264-2268.
Kimber G, Yen Y. 1988. Analysis of pivotal-differential evolutionary patterns. Evolution 85: 9106-9108.
Lagercrantz U, Lydiate DJ. 1996. Comparative genome mapping in Brassica. Genetics 144: 1903-1910.
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. Theoretical and Applied Genetics 113: 1467-1480.
Leflon M, Grandont L, Eber F, Huteau V, Coriton O, Chelysheva L, Jenczewski E, Chevre A-M. 2010. Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell Online 22: 2253-2264.
Leitch AR, Leitch IJ. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483.
Levin DA, Soltis DE. 2018. Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude. Current Opinion in Plant Biology 42: 1-7.
Lipman MJ, Chester M, Soltis PS, Soltis DE. 2013. Natural hybrids between Tragopogon mirus and T. miscellus (Asteraceae): a new perspective on karyotypic changes following hybridization at the polyploid level. American Journal of Botany 100: 2016-2022.
Luo Z, Wang M, Long Y, Huang Y, Shi L, Zhang C, Liu X, Fitt BDL, Xiang J, Mason AS et al. 2017. Incorporating pleiotropic quantitative trait loci in dissection of complex traits: seed yield in rapeseed as an example. Theoretical and Applied Genetics 130: 1569-1585.
Mallet J. 2005. Hybridization as an invasion of the genome. Trends in Ecology & Evolution 20: 229-237.
Mallet J. 2007. Hybrid speciation. Nature 446: 279-283.
Mason AS, Batley J, Bayer PE, Hayward A, Cowling WA, Nelson MN. 2014. High-resolution molecular karyotyping uncovers pairing between ancestrally related Brassica chromosomes. New Phytologist 202: 964-974.
Mason AS, Huteau V, Eber F, Coriton O, Yan G, Nelson MN, Cowling WA, Chèvre A-MM. 2010. Genome structure affects the rate of autosyndesis and allosyndesis in AABC, BBAC and CCAB Brassica interspecific hybrids. Chromosome Research 18: 655-666.
Mason AS, Nelson MN, Castello MC, Yan G, Cowling WA. 2011a. Genotypic effects on the frequency of homoeologous and homologous recombination in Brassica napus × B. carinata hybrids. Theoretical and Applied Genetics 122: 543-553.
Mason AS, Nelson MN, Yan G, Cowling WA. 2011b. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biology 11: e103.
Mason AS, Rousseau-Gueutin M, Morice J, Bayer PE, Besharat N, Cousin A, Pradhan A, Parkin IAP, Chèvre AM, Batley J et al. 2016. Centromere locations in Brassica A and C genomes revealed through half-tetrad analysis. Genetics 202: 513-523.
Mirzaghaderi G, Mason AS. 2017. Revisiting pivotal-differential genome evolution in wheat. Trends in Plant Science 22: 674-684.
Molnár I, Šimková H, Leverington-Waite M, Goram R, Cseh A, Vrána J, Farkas A, Doležel J, Molnár-Láng M, Griffiths S. 2013. Syntenic relationships between the U and M genomes of Aegilops, wheat and the model species Brachypodium and rice as revealed by COS markers. PLoS ONE 8: e70844.
U N. 1935. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese Journal of Botany 7: 389-452.
Navabi Z-K, Huebert T, Sharpe AG, O’Neill CM, Bancroft I, Parkin IAP. 2013. Conserved microstructure of the Brassica B genome of Brassica nigra in relation to homologous regions of Arabidopsis thaliana, B. rapa and B. oleracea. BMC Genomics 14: e250.
Navabi ZK, Parkin IAP, Pires JC, Xiong Z, Thiagarajah MR, Good AG, Rahman MH. 2010. Introgression of B-genome chromosomes in a doubled haploid population of Brassica napus × B. carinata. Genome 53: 619-629.
Nelson MN, Mason AS, Castello MC, Thomson L, Yan G, Cowling WA. 2009. Microspore culture preferentially selects unreduced (2n) gametes from an interspecific hybrid of Brassica napus L. × Brassica carinata Braun. Theoretical and Applied Genetics 119: 497-505.
Nicolas SD, Leflon M, Monod H, Eber F, Coriton O, Huteau V, Chevre A-M, Jenczewski E. 2009. Genetic regulation of meiotic cross-overs between related genomes in Brassica napus haploids and hybrids. Plant Cell Online 21: 373-385.
Novikova PY, Tsuchimatsu T, Simon S, Nizhynska V, Voronin V, Burns R, Fedorenko OM, Holm S, Säll T, Prat E et al. 2017. Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica. Molecular Biology and Evolution 34: 957-968.
Panjabi P, Jagannath A, Bisht NC, Lakshmi KL, Sharma S, Gupta V, Pradhan AK, Pental D. 2008. Comparative mapping of Brassica juncea and Arabidopsis thaliana using intron polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genomics 9: e113.
Pelé A, Rousseau-Gueutin M, Chèvre A-M. 2018. Speciation success of polyploid plants closely relates to the regulation of meiotic recombination. Frontiers in Plant Science 9: e907.
Prakash S. 1999. 2 Origin and domestication. In: Gómez-Campo C ed. Biology of Brassica coenospecies. Developments in plant genetics and breeding. New York, NY, USA: Elsevier, 4: 33-58
Prakash S, Bhat SR, Quiros CF, Kirti PB, Chopra VL. 2009. Brassica and its close allies: cytogenetics and evolution. In: Janick J, ed. Plant breeding reviews, vol. 31. Hoboken, NJ, USA: John Wiley & Sons, 21-187.
Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics. 29: 467-501.
Renny-Byfield S, Gong L, Gallagher JP, Wendel JF. 2015. Persistence of subgenomes in paleopolyploid cotton after 60 My of evolution. Molecular Biology and Evolution 32: 1063-1071.
Rieseberg LH. 1997. Hybrid origins of plant species. Annual Review of Ecology and Systematics 28: 359-389.
Rieseberg LH. 2006. Hybrid speciation in wild sunflowers. Annals of the Missouri Botanical Garden 93: 34-48.
Samans B, Chalhoub B, Snowdon RJ. 2017. Surviving a genome collision: genomic signatures of allopolyploidization in the recent crop species Brassica napus. Plant Genome 10: doi: 10:3835/plantgenome2017.02.0013.
Schelfhout CJ, Wroth JM, Yan G, Cowling WA. 2008. Enhancement of genetic diversity in canola-quality Brassica napus and B. juncea by interspecific hybridisation. Australian Journal of Agricultural Research 59: 918-925.
Schnable JC, Springer NM, Freeling M. 2011. Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proceedings of the National Academy of Sciences, USA 108: 4069-4074.
Snowdon RJ, Köhler W, Friedt W, Köhler A. 1997. Genomic in situ hybridization in Brassica amphidiploids and interspecific hybrids. Theoretical and Applied Genetics 95: 1320-1324.
Soltis DE, Soltis PS. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348-352.
Soltis DE, Soltis PS, Bennett MD, Leitch IJ. 2003. Evolution of genome size in the angiosperms. American Journal of Botany 90: 1596-1603.
Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E. 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biological Journal of the Linnean Society 82: 485-501.
Soltis PS, Soltis DE. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561-588.
Song K, Lu P, Tang K, Osbornt TC. 1995. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proceedings of the National Academy of Sciences, USA 92: 7719-7723.
Szadkowski E, Eber F, Huteau V, Lodé M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux MJ, Delourme R, King GJ et al. 2010. The first meiosis of resynthesized Brassica napus, a genome blender. New Phytologist 186: 102-112.
Thomas BC, Pedersen B, Freeling M. 2006. Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Research 16: 934-946.
Tian E, Jiang Y, Chen L, Zou J, Liu F, Meng J. 2010. Synthesis of a Brassica trigenomic allohexaploid (B. carinata × B. rapa) de novo and its stability in subsequent generations. Theoretical and Applied Genetics 121: 1431-1440.
Ungerer MC, Baird SJ, Pan J, Rieseberg LH. 1998. Rapid hybrid speciation in wild sunflowers. Proceedings of the National Academy of Sciences, USA 95: 11757-11762.
Wang JBO, Wang C, Shi SH, Zhong Y. 2000. Evolution of parental ITS regions of nuclear rDNA in allopolyploid Aegilops (Poaceae) species. Hereditas 133: 1-7.
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F et al. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43: 1035-1040.
Wendel JF, Lisch D, Hu G, Mason AS. 2018. The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Current Opinion in Genetics & Development 49: 1-7.
Wu J, Lin L, Xu M, Chen P, Liu D, Sun Q, Ran L, Wang Y. 2018. Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus. BMC Genomics 19: e586.
Xiong Z, Gaeta RT, Pires JC. 2011. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proceedings of the National Academy of Sciences, USA 108: 7908-7913.
Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F et al. 2013. Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proceedings of the National Academy of Sciences, USA 110: 3447-3452.
Zhang P, Hiebert CW, McIntosh RA, McCallum BD, Thomas JB, Hoxha S, Singh D, Bansal U. 2016. The relationship of leaf rust resistance gene Lr13 and hybrid necrosis gene Ne2m on wheat chromosome 2BS. Theoretical and Applied Genetics 129: 485-493.
Zohary D, Feldman M. 1962. Hybridization between amphiploids and the evolution of polyploids in the wheat (Aegilops-Triticum) group. Evolution 16: 44-61.
Zou J, Hu D, Mason AS, Shen X, Wang X, Wang N, Grandke F, Wang M, Chang S, Snowdon RJ et al. 2018. Genetic changes in a novel breeding population of Brassica napus synthesized from hundreds of crosses between B. rapa and B. carinata. Plant Biotechnology Journal 16: 507-519.

Auteurs

Elvis Katche (E)

Plant Breeding Department, Justus Liebig University, Heinrich-Buff-Ring 26-32, Giessen, 35392, Germany.

Roman Gaebelein (R)

Plant Breeding Department, Justus Liebig University, Heinrich-Buff-Ring 26-32, Giessen, 35392, Germany.

Zurianti Idris (Z)

School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia.

Paula Vasquez-Teuber (P)

Plant Breeding Department, Justus Liebig University, Heinrich-Buff-Ring 26-32, Giessen, 35392, Germany.
School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia.
Department of Plant Production, Faculty of Agronomy, University of Concepción, Av. Vicente Méndez 595, Chillán, Chile.

Yu-Tzu Lo (YT)

School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia.

David Nugent (D)

School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia.

Jacqueline Batley (J)

School of Biological Sciences, The University of Western Australia, 35 Stirling Hwy, Crawley, Perth, WA, 6009, Australia.

Annaliese S Mason (AS)

Plant Breeding Department, Justus Liebig University, Heinrich-Buff-Ring 26-32, Giessen, 35392, Germany.
School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia.
Plant Breeding Department, University of Bonn, Katzenburgweg 5, Bonn, 53115, Germany.

Articles similaires

A scenario for an evolutionary selection of ageing.

Tristan Roget, Claire Macmurray, Pierre Jolivet et al.
1.00
Aging Selection, Genetic Biological Evolution Animals Fertility
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis
Humans Female Ethiopia Adolescent Adult

Classifications MeSH