Ancient hybridizations among the ancestral genomes of bread wheat
Abstract
The allohexaploid bread wheat genome consists of three closely related subgenomes (A, B, and D), but a clear understanding of their phylogenetic history has been lacking. We used genome assemblies of bread wheat and five diploid relatives to analyze genome-wide samples of gene trees, as well as to estimate evolutionary relatedness and divergence times. We show that the A and B genomes diverged from a common ancestor ~7 million years ago and that these genomes gave rise to the D genome through homoploid hybrid speciation 1 to 2 million years later. Our findings imply that the present-day bread wheat genome is a product of multiple rounds of hybrid speciation (homoploid and polyploid) and lay the foundation for a new framework for understanding the wheat genome as a multilevel phylogenetic mosaic.
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References and Notes
1
Heun M., et al., Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278, 1312–1314 (1997).
2
Lev-Yadun S., Gopher A., Abbo S., The cradle of agriculture. Science 288, 1602–1603 (2000).
3
Riehl S., Zeidi M., Conard N. J., Emergence of agriculture in the foothills of the Zagros Mountains of Iran. Science 341, 65–67 (2013).
4
Salamini F., Özkan H., Brandolini A., Schäfer-Pregl R., Martin W., Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3, 429–441 (2002).
5
McFadden E. S., Sears E. R., The origin of Triticum spelta and its free-threshing hexaploid relatives. J. Hered. 37, 81–107, 107 (1946).
6
Dubcovsky J., Dvorak J., Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316, 1862–1866 (2007).
7
International Wheat Genome Sequencing Consortium, A chromosome-based draft sequence of the hexaploid bread wheat genome. Science 345, 1251788 (2014).
8
Petersen G., Seberg O., Yde M., Berthelsen K., Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol. Phylogenet. Evol. 39, 70–82 (2006) and references therein.
9
Huang S., Sirikhachornkit A., Su X., Faris J., Gill B., Haselkorn R., Gornicki P., Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc. Natl. Acad. Sci. U.S.A. 99, 8133–8138 (2002).
10
Akhunov E. D., Akhunova A. R., Dvorák J., BAC libraries of Triticum urartu, Aegilops speltoides and Ae. tauschii, the diploid ancestors of polyploid wheat. Theor. Appl. Genet. 111, 1617–1622 (2005) and references therein.
11
Chalupska D., Lee H. Y., Faris J. D., Evrard A., Chalhoub B., Haselkorn R., Gornicki P., Acc homoeoloci and the evolution of wheat genomes. Proc. Natl. Acad. Sci. U.S.A. 105, 9691–9696 (2008).
12
Dvorak J., Akhunov E. D., Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploid evolution in the Aegilops-Triticum alliance. Genetics 171, 323–332 (2005).
13
Fan X., Sha L.-N., Yu S.-B., Wu D.-D., Chen X.-H., Zhuo X.-F., Zhang H.-Q., Kang H.-Y., Wang Y., Zheng Y.-L., Zhou Y.-H., Phylogenetic reconstruction and diversification of the Triticeae (Poaceae) based on single-copy nuclear Acc1 and Pgk1 gene data. Biochem. Syst. Ecol. 50, 346–360 (2013).
14
Strömberg C. A. E., Evolution of grasses and grassland ecosystems. Annu. Rev. Earth Planet. Sci. 39, 517–544 (2011).
15
Escobar J. S., Scornavacca C., Cenci A., Guilhaumon C., Santoni S., Douzery E. J., Ranwez V., Glémin S., David J., Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae). BMC Evol. Biol. 11, 181–198 (2011).
16
Lobell D. B., Schlenker W., Costa-Roberts J., Climate trends and global crop production since 1980. Science 333, 616–620 (2011).
17
Ling H. Q., Zhao S., Liu D., Wang J., Sun H., Zhang C., Fan H., Li D., Dong L., Tao Y., Gao C., Wu H., Li Y., Cui Y., Guo X., Zheng S., Wang B., Yu K., Liang Q., Yang W., Lou X., Chen J., Feng M., Jian J., Zhang X., Luo G., Jiang Y., Liu J., Wang Z., Sha Y., Zhang B., Wu H., Tang D., Shen Q., Xue P., Zou S., Wang X., Liu X., Wang F., Yang Y., An X., Dong Z., Zhang K., Zhang X., Luo M. C., Dvorak J., Tong Y., Wang J., Yang H., Li Z., Wang D., Zhang A., Wang J., Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496, 87–90 (2013).
18
Jia J., Zhao S., Kong X., Li Y., Zhao G., He W., Appels R., Pfeifer M., Tao Y., Zhang X., Jing R., Zhang C., Ma Y., Gao L., Gao C., Spannagl M., Mayer K. F., Li D., Pan S., Zheng F., Hu Q., Xia X., Li J., Liang Q., Chen J., Wicker T., Gou C., Kuang H., He G., Luo Y., Keller B., Xia Q., Lu P., Wang J., Zou H., Zhang R., Xu J., Gao J., Middleton C., Quan Z., Liu G., Wang J., Yang H., Liu X., He Z., Mao L., Wang J.International Wheat Genome Sequencing Consortium, Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496, 91–95 (2013).
19
Vigeland M. D., Spannagl M., Asp T., Paina C., Rudi H., Rognli O.-A., Fjellheim S., Sandve S. R., Evidence for adaptive evolution of low-temperature stress response genes in a Pooideae grass ancestor. New Phytol. 199, 1060–1068 (2013).
20
Drummond A. J., Suchard M. A., Xie D., Rambaut A., Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).
21
Degnan J. H., Rosenberg N. A., Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332–340 (2009).
22
Pfeifer M., Kugler K. G., Sandve S. R., Zhan B., Rudi H., Hvidsten T. R.International Wheat Genome Sequencing Consortium, Mayer K. F. X., Olsen O.-A., Genome interplay in the grain transcriptome of hexploid bread wheat. Science 345, 1250091 (2014).
23
J. P. Lotsy, Evolution by Means of Hybridization (Martinus Nijhoff, The Hague, Netherlands, 1916).
24
Abbott R., Albach D., Ansell S., Arntzen J. W., Baird S. J., Bierne N., Boughman J., Brelsford A., Buerkle C. A., Buggs R., Butlin R. K., Dieckmann U., Eroukhmanoff F., Grill A., Cahan S. H., Hermansen J. S., Hewitt G., Hudson A. G., Jiggins C., Jones J., Keller B., Marczewski T., Mallet J., Martinez-Rodriguez P., Möst M., Mullen S., Nichols R., Nolte A. W., Parisod C., Pfennig K., Rice A. M., Ritchie M. G., Seifert B., Smadja C. M., Stelkens R., Szymura J. M., Väinölä R., Wolf J. B., Zinner D., Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).
25
Eroukhmanoff F., Bailey R. I., Sætre G.-P., Hybridization and genome evolution I: The role of contingency during hybrid speciation. Curr. Zool. 59, 667–674 (2013).
26
Mallet J., Hybrid speciation. Nature 446, 279–283 (2007).
27
Doyle J. J., Egan A. N., Dating the origins of polyploidy events. New Phytol. 186, 73–85 (2010).
28
Li L., Stoeckert C. J., Roos D. S., OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189 (2003).
29
Katoh K., Asimenos G., Toh H., Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537, 39–64 (2009).
30
Penn O., Privman E., Landan G., Graur D., Pupko T., An alignment confidence score capturing robustness to guide tree uncertainty. Mol. Biol. Evol. 27, 1759–1767 (2010).
31
Schliep K. P., phangorn: Phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).
32
Paradis E., Claude J., Strimmer K., APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20, 289–290 (2004).
33
Yu Y., Barnett R. M., Nakhleh L., Parsimonious inference of hybridization in the presence of incomplete lineage sorting. Syst. Biol. 62, 738–751 (2013).
34
Than C., Ruths D., Nakhleh L., PhyloNet: A software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9, 322 (2008).
35
Sturtz S., Ligges U., Gelman A., R2WinBUGS: A package for running WinBUGS from R. J. Stat. Softw. 12, 1–16 (2005).
36
Heath L., van der Walt E., Varsani A., Martin D. P., Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J. Virol. 80, 11827–11832 (2006).
37Juchniewicz K., Flora kopalna Turowa koło Bogatyni w świetle analizy nabłonkowej. Prace Muzeum Ziemi 24, 65–132 (1975).
38Worobiec G., Kasiński J., Dispersed cuticles from the Neogene Ruja lignite deposit near Legnica, Lower Silesia, Poland. Acta Palaeobotanica 49, 135–191 (2009).
39
Thomasson J. R., Berriochloa gabeli and Berriochloa huletti (Gramineae: Stipeae), two new grass species from the late Miocene Ash Hollow Formation of Nebraska and Kansas. J. Paleontol. 79, 185–199 (2005).
40
Thomasson J. R., Epidermal patterns of the lemma in some fossil and living grasses and their phylogenetic significance. Science 199, 975–977 (1978).
41
S. R. Manchester, in Fossil Flora and Stratigraphy of the Florissant Formation, Colorado, E. Evanoff, K. M. Gregory-Wodzicki, K. R. Johnson, Eds. (Proceedings of the Denver Museum of Nature and Science Series, Denver, 2001), pp. 137–161.
42
Prasad V., Strömberg C. A. E., Leaché A. D., Samant B., Patnaik R., Tang L., Mohabey D. M., Ge S., Sahni A., Late Cretaceous origin of the rice tribe provides evidence for early diversification in Poaceae. Nat. Commun. 2, 480 (2011).
43
Bouckaert R. R., DensiTree: Making sense of sets of phylogenetic trees. Bioinformatics 26, 1372–1373 (2010).
44
Lunn D. J., Thomas A., Best N., Spiegelhalter D., WinBUGS - A Bayesian modelling framework: Concepts, structure, and extensibility. Stat. Comput. 10, 325–337 (2000).
45
Huson D. H., SplitsTree: Analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73 (1998).
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Published In
Science
Volume 345 | Issue 6194
18 July 2014
18 July 2014
Copyright
Copyright © 2014, American Association for the Advancement of Science.
Submission history
Received: 23 December 2013
Accepted: 20 May 2014
Published in print: 18 July 2014
Acknowledgments
This work was financed by Norwegian Research Council grant 199387 to Norwegian University of Life Sciences and Graminor AS to O.-A.O. The phylogenetic analyses were run, in part, on the Bioportal supercomputing facility at the University of Oslo. We thank C.-P. Antoine and two anonymous reviewers for valuable comments on the manuscript and S. Sæbø for help on implementation of the OpenBUGS analyses in R. Ortholog alignments, gene trees, and the OpenBUGS model used for multispecies coalescent modeling can be downloaded from Dryad (data available from the Dryad Digital Repository: http://doi.org/10.5061/dryad.f6c34).
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