Ancient hybridizations among the ancestral genomes of bread wheat

Thomas Marcussen; Simen R. Sandve; Lise Heier; Manuel Spannagl; Matthias Pfeifer; Kjetill S. Jakobsen; Brande Wulff; Burkhard Steuernagel; Klaus F.X. Mayer; Odd Arne Olsen; Jane Rogers; Jaroslav Doležel; Curtis Pozniak; Kellye Eversole; Catherine Feuillet; Bikram Gill; Bernd Friebe; Adam J. Lukaszewski; Pierre Sourdille; Takashi R. Endo; Marie Kubaláková; Jarmila Šíhalíková; Zdeňka Dubská; Jan Vrána; Romana Šperková; Hana Šimková; Melanie Febrer; Leah Clissold; Kirsten McLay; Kuldeep Singh; Parveen Chhuneja; Nagendra K. Singh; Jitendra Khurana; Eduard Akhunov; Frédéric Choulet; Adriana Alberti; Valérie Barbe; Patrick Wincker; Hiroyuki Kanamori; Fuminori Kobayashi; Takeshi Itoh; Takashi Matsumoto; Hiroaki Sakai; Tsuyoshi Tanaka; Jianzhong Wu; Yasunari Ogihara; Hirokazu Handa; P. Ron Maclachlan; Andrew Sharpe; Darrin Klassen; David Edwards; Jacqueline Batley; Simen Rød Sandve; Sigbjørn Lien; Mario Caccamo; Sarah Ayling; Ricardo H. Ramirez-Gonzalez; Bernardo J. Clavijo; Jonathan Wright; Mihaela M. Martis; Martin Mascher; Jarrod Chapman; Jesse A. Poland; Uwe Scholz; Kerrie Barry; Robbie Waugh; Daniel S. Rokhsar; Gary J. Muehlbauer; Nils Stein; Heidrun Gundlach; Matthias Zytnicki; Véronique Jamilloux; Hadi Quesneville; Thomas Wicker; Primetta Faccioli; Moreno Colaiacovo; Antonio Michele Stanca; Hikmet Budak; Luigi Cattivelli; Natasha Glover; Lise Pingault; Etienne Paux; Sapna Sharma; Rudi Appels; Matthew Bellgard; Brett Chapman; Thomas Nussbaumer; Kai Christian Bader; Hélène Rimbert; Shichen Wang; Ron Knox; Andrzej Kilian; Michael Alaux; Françoise Alfama; Loïc Couderc; Nicolas Guilhot; Claire Viseux; Mikaël Loaec; Beat Keller; Sebastien Praud

doi:10.1126/science.1250092

Ancient hybridizations among the ancestral genomes of bread wheat

Thomas Marcussen, Simen R. Sandve, Lise Heier, Manuel Spannagl, Matthias Pfeifer, Kjetill S. Jakobsen, Brande Wulff, Burkhard Steuernagel, Klaus F.X. Mayer, Odd Arne Olsen, Jane Rogers, Jaroslav Doležel, Curtis Pozniak, Kellye Eversole, Catherine Feuillet, Bikram Gill, Bernd Friebe, Adam J. Lukaszewski, Pierre Sourdille, Takashi R. EndoMarie Kubaláková, Jarmila Šíhalíková, Zdeňka Dubská, Jan Vrána, Romana Šperková, Hana Šimková, Melanie Febrer, Leah Clissold, Kirsten McLay, Kuldeep Singh, Parveen Chhuneja, Nagendra K. Singh, Jitendra Khurana, Eduard Akhunov, Frédéric Choulet, Adriana Alberti, Valérie Barbe, Patrick Wincker, Hiroyuki Kanamori, Fuminori Kobayashi, Takeshi Itoh, Takashi Matsumoto, Hiroaki Sakai, Tsuyoshi Tanaka, Jianzhong Wu, Yasunari Ogihara, Hirokazu Handa, P. Ron Maclachlan, Andrew Sharpe, Darrin Klassen, David Edwards, Jacqueline Batley, Simen Rød Sandve, Sigbjørn Lien, Mario Caccamo, Sarah Ayling, Ricardo H. Ramirez-Gonzalez, Bernardo J. Clavijo, Jonathan Wright, Mihaela M. Martis, Martin Mascher, Jarrod Chapman, Jesse A. Poland, Uwe Scholz, Kerrie Barry, Robbie Waugh, Daniel S. Rokhsar, Gary J. Muehlbauer, Nils Stein, Heidrun Gundlach, Matthias Zytnicki, Véronique Jamilloux, Hadi Quesneville, Thomas Wicker, Primetta Faccioli, Moreno Colaiacovo, Antonio Michele Stanca, Hikmet Budak, Luigi Cattivelli, Natasha Glover, Lise Pingault, Etienne Paux, Sapna Sharma, Rudi Appels, Matthew Bellgard, Brett Chapman, Thomas Nussbaumer, Kai Christian Bader, Hélène Rimbert, Shichen Wang, Ron Knox, Andrzej Kilian, Michael Alaux, Françoise Alfama, Loïc Couderc, Nicolas Guilhot, Claire Viseux, Mikaël Loaec, Beat Keller, Sebastien Praud

Research output: Contribution to journal › Article › peer-review

531 Scopus citations

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.

Original language	English (US)
Journal	Science
Volume	345
Issue number	6194
DOIs	https://doi.org/10.1126/science.1250092
State	Published - Jan 1 2014
Externally published	Yes

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10.1126/science.1250092

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Marcussen, T., Sandve, S. R., Heier, L., Spannagl, M., Pfeifer, M., Jakobsen, K. S., Wulff, B., Steuernagel, B., Mayer, K. F. X., Olsen, O. A., Rogers, J., Doležel, J., Pozniak, C., Eversole, K., Feuillet, C., Gill, B., Friebe, B., Lukaszewski, A. J., Sourdille, P., ... Praud, S. (2014). Ancient hybridizations among the ancestral genomes of bread wheat. Science, 345(6194). https://doi.org/10.1126/science.1250092

@article{96f37d57463e472f95c2cfdfc860f232,

title = "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.",

author = "Thomas Marcussen and Sandve, {Simen R.} and Lise Heier and Manuel Spannagl and Matthias Pfeifer and Jakobsen, {Kjetill S.} and Brande Wulff and Burkhard Steuernagel and Mayer, {Klaus F.X.} and Olsen, {Odd Arne} and Jane Rogers and Jaroslav Dole{\v z}el and Curtis Pozniak and Kellye Eversole and Catherine Feuillet and Bikram Gill and Bernd Friebe and Lukaszewski, {Adam J.} and Pierre Sourdille and Endo, {Takashi R.} and Marie Kubal{\'a}kov{\'a} and Jarmila {\v S}{\'i}hal{\'i}kov{\'a} and Zde{\v n}ka Dubsk{\'a} and Jan Vr{\'a}na and Romana {\v S}perkov{\'a} and Hana {\v S}imkov{\'a} and Melanie Febrer and Leah Clissold and Kirsten McLay and Kuldeep Singh and Parveen Chhuneja and Singh, {Nagendra K.} and Jitendra Khurana and Eduard Akhunov and Fr{\'e}d{\'e}ric Choulet and Adriana Alberti and Val{\'e}rie Barbe and Patrick Wincker and Hiroyuki Kanamori and Fuminori Kobayashi and Takeshi Itoh and Takashi Matsumoto and Hiroaki Sakai and Tsuyoshi Tanaka and Jianzhong Wu and Yasunari Ogihara and Hirokazu Handa and Maclachlan, {P. Ron} and Andrew Sharpe and Darrin Klassen and David Edwards and Jacqueline Batley and Sandve, {Simen R{\o}d} and Sigbj{\o}rn Lien and Mario Caccamo and Sarah Ayling and Ramirez-Gonzalez, {Ricardo H.} and Clavijo, {Bernardo J.} and Jonathan Wright and Martis, {Mihaela M.} and Martin Mascher and Jarrod Chapman and Poland, {Jesse A.} and Uwe Scholz and Kerrie Barry and Robbie Waugh and Rokhsar, {Daniel S.} and Muehlbauer, {Gary J.} and Nils Stein and Heidrun Gundlach and Matthias Zytnicki and V{\'e}ronique Jamilloux and Hadi Quesneville and Thomas Wicker and Primetta Faccioli and Moreno Colaiacovo and Stanca, {Antonio Michele} and Hikmet Budak and Luigi Cattivelli and Natasha Glover and Lise Pingault and Etienne Paux and Sapna Sharma and Rudi Appels and Matthew Bellgard and Brett Chapman and Thomas Nussbaumer and Bader, {Kai Christian} and H{\'e}l{\`e}ne Rimbert and Shichen Wang and Ron Knox and Andrzej Kilian and Michael Alaux and Fran{\c c}oise Alfama and Lo{\"i}c Couderc and Nicolas Guilhot and Claire Viseux and Mika{\"e}l Loaec and Beat Keller and Sebastien Praud",

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year = "2014",

month = jan,

day = "1",

doi = "10.1126/science.1250092",

language = "English (US)",

volume = "345",

journal = "Science",

issn = "1095-9203",

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Marcussen, T, Sandve, SR, Heier, L, Spannagl, M, Pfeifer, M, Jakobsen, KS, Wulff, B, Steuernagel, B, Mayer, KFX, Olsen, OA, Rogers, J, Doležel, J, Pozniak, C, Eversole, K, Feuillet, C, Gill, B, Friebe, B, Lukaszewski, AJ, Sourdille, P, Endo, TR, Kubaláková, M, Šíhalíková, J, Dubská, Z, Vrána, J, Šperková, R, Šimková, H, Febrer, M, Clissold, L, McLay, K, Singh, K, Chhuneja, P, Singh, NK, Khurana, J, Akhunov, E, Choulet, F, Alberti, A, Barbe, V, Wincker, P, Kanamori, H, Kobayashi, F, Itoh, T, Matsumoto, T, Sakai, H, Tanaka, T, Wu, J, Ogihara, Y, Handa, H, Maclachlan, PR, Sharpe, A, Klassen, D, Edwards, D, Batley, J, Sandve, SR, Lien, S, Caccamo, M, Ayling, S, Ramirez-Gonzalez, RH, Clavijo, BJ, Wright, J, Martis, MM, Mascher, M, Chapman, J, Poland, JA, Scholz, U, Barry, K, Waugh, R, Rokhsar, DS, Muehlbauer, GJ, Stein, N, Gundlach, H, Zytnicki, M, Jamilloux, V, Quesneville, H, Wicker, T, Faccioli, P, Colaiacovo, M, Stanca, AM, Budak, H, Cattivelli, L, Glover, N, Pingault, L, Paux, E, Sharma, S, Appels, R, Bellgard, M, Chapman, B, Nussbaumer, T, Bader, KC, Rimbert, H, Wang, S, Knox, R, Kilian, A, Alaux, M, Alfama, F, Couderc, L, Guilhot, N, Viseux, C, Loaec, M, Keller, B & Praud, S 2014, 'Ancient hybridizations among the ancestral genomes of bread wheat', Science, vol. 345, no. 6194. https://doi.org/10.1126/science.1250092

TY - JOUR

T1 - Ancient hybridizations among the ancestral genomes of bread wheat

AU - Marcussen, Thomas

AU - Sandve, Simen R.

AU - Heier, Lise

AU - Spannagl, Manuel

AU - Pfeifer, Matthias

AU - Jakobsen, Kjetill S.

AU - Wulff, Brande

AU - Steuernagel, Burkhard

AU - Mayer, Klaus F.X.

AU - Olsen, Odd Arne

AU - Rogers, Jane

AU - Doležel, Jaroslav

AU - Pozniak, Curtis

AU - Eversole, Kellye

AU - Feuillet, Catherine

AU - Gill, Bikram

AU - Friebe, Bernd

AU - Lukaszewski, Adam J.

AU - Sourdille, Pierre

AU - Endo, Takashi R.

AU - Kubaláková, Marie

AU - Šíhalíková, Jarmila

AU - Dubská, Zdeňka

AU - Vrána, Jan

AU - Šperková, Romana

AU - Šimková, Hana

AU - Febrer, Melanie

AU - Clissold, Leah

AU - McLay, Kirsten

AU - Singh, Kuldeep

AU - Chhuneja, Parveen

AU - Singh, Nagendra K.

AU - Khurana, Jitendra

AU - Akhunov, Eduard

AU - Choulet, Frédéric

AU - Alberti, Adriana

AU - Barbe, Valérie

AU - Wincker, Patrick

AU - Kanamori, Hiroyuki

AU - Kobayashi, Fuminori

AU - Itoh, Takeshi

AU - Matsumoto, Takashi

AU - Sakai, Hiroaki

AU - Tanaka, Tsuyoshi

AU - Wu, Jianzhong

AU - Ogihara, Yasunari

AU - Handa, Hirokazu

AU - Maclachlan, P. Ron

AU - Sharpe, Andrew

AU - Klassen, Darrin

AU - Edwards, David

AU - Batley, Jacqueline

AU - Sandve, Simen Rød

AU - Lien, Sigbjørn

AU - Caccamo, Mario

AU - Ayling, Sarah

AU - Ramirez-Gonzalez, Ricardo H.

AU - Clavijo, Bernardo J.

AU - Wright, Jonathan

AU - Martis, Mihaela M.

AU - Mascher, Martin

AU - Chapman, Jarrod

AU - Poland, Jesse A.

AU - Scholz, Uwe

AU - Barry, Kerrie

AU - Waugh, Robbie

AU - Rokhsar, Daniel S.

AU - Muehlbauer, Gary J.

AU - Stein, Nils

AU - Gundlach, Heidrun

AU - Zytnicki, Matthias

AU - Jamilloux, Véronique

AU - Quesneville, Hadi

AU - Wicker, Thomas

AU - Faccioli, Primetta

AU - Colaiacovo, Moreno

AU - Stanca, Antonio Michele

AU - Budak, Hikmet

AU - Cattivelli, Luigi

AU - Glover, Natasha

AU - Pingault, Lise

AU - Paux, Etienne

AU - Sharma, Sapna

AU - Appels, Rudi

AU - Bellgard, Matthew

AU - Chapman, Brett

AU - Nussbaumer, Thomas

AU - Bader, Kai Christian

AU - Rimbert, Hélène

AU - Wang, Shichen

AU - Knox, Ron

AU - Kilian, Andrzej

AU - Alaux, Michael

AU - Alfama, Françoise

AU - Couderc, Loïc

AU - Guilhot, Nicolas

AU - Viseux, Claire

AU - Loaec, Mikaël

AU - Keller, Beat

AU - Praud, Sebastien

N1 - Generated from Scopus record by KAUST IRTS on 2022-09-13

PY - 2014/1/1

Y1 - 2014/1/1

N2 - 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.

AB - 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.

UR - https://www.science.org/doi/10.1126/science.1250092

UR - http://www.scopus.com/inward/record.url?scp=84904402814&partnerID=8YFLogxK

U2 - 10.1126/science.1250092

DO - 10.1126/science.1250092

M3 - Article

SN - 1095-9203

VL - 345

JO - Science

JF - Science

IS - 6194

ER -

Ancient hybridizations among the ancestral genomes of bread wheat

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