Durum wheat genome highlights past domestication signatures and future improvement targets

Marco Maccaferri; Neil S. Harris; Sven O. Twardziok; Raj K. Pasam; Heidrun Gundlach; Manuel Spannagl; Danara Ormanbekova; Thomas Lux; Verena M. Prade; Sara G. Milner; Axel Himmelbach; Martin Mascher; Paolo Bagnaresi; Primetta Faccioli; Paolo Cozzi; Massimiliano Lauria; Barbara Lazzari; Alessandra Stella; Andrea Manconi; Matteo Gnocchi; Marco Moscatelli; Raz Avni; Jasline Deek; Sezgi Biyiklioglu; Elisabetta Frascaroli; Simona Corneti; Silvio Salvi; Gabriella Sonnante; Francesca Desiderio; Caterina Marè; Cristina Crosatti; Erica Mica; Hakan Özkan; Benjamin Kilian; Pasquale De Vita; Daniela Marone; Reem Joukhadar; Elisabetta Mazzucotelli; Domenica Nigro; Agata Gadaleta; Shiaoman Chao; Justin D. Faris; Arthur T.O. Melo; Mike Pumphrey; Nicola Pecchioni; Luciano Milanesi; Krystalee Wiebe; Jennifer Ens; Ron P. MacLachlan; John M. Clarke; Andrew G. Sharpe; Chu Shin Koh; Kevin Y.H. Liang; Gregory J. Taylor; Ron Knox; Hikmet Budak; Anna M. Mastrangelo; Steven S. Xu; Nils Stein; Iago Hale; Assaf Distelfeld; Matthew J. Hayden; Roberto Tuberosa; Sean Walkowiak; Klaus F.X. Mayer; Aldo Ceriotti; Curtis J. Pozniak; Luigi Cattivelli

doi:10.1038/s41588-019-0381-3

Durum wheat genome highlights past domestication signatures and future improvement targets

Marco Maccaferri, Neil S. Harris, Sven O. Twardziok, Raj K. Pasam, Heidrun Gundlach, Manuel Spannagl, Danara Ormanbekova, Thomas Lux, Verena M. Prade, Sara G. Milner, Axel Himmelbach, Martin Mascher, Paolo Bagnaresi, Primetta Faccioli, Paolo Cozzi, Massimiliano Lauria, Barbara Lazzari, Alessandra Stella, Andrea Manconi, Matteo GnocchiMarco Moscatelli, Raz Avni, Jasline Deek, Sezgi Biyiklioglu, Elisabetta Frascaroli, Simona Corneti, Silvio Salvi, Gabriella Sonnante, Francesca Desiderio, Caterina Marè, Cristina Crosatti, Erica Mica, Hakan Özkan, Benjamin Kilian, Pasquale De Vita, Daniela Marone, Reem Joukhadar, Elisabetta Mazzucotelli, Domenica Nigro, Agata Gadaleta, Shiaoman Chao, Justin D. Faris, Arthur T.O. Melo, Mike Pumphrey, Nicola Pecchioni, Luciano Milanesi, Krystalee Wiebe, Jennifer Ens, Ron P. MacLachlan, John M. Clarke, Andrew G. Sharpe, Chu Shin Koh, Kevin Y.H. Liang, Gregory J. Taylor, Ron Knox, Hikmet Budak, Anna M. Mastrangelo, Steven S. Xu, Nils Stein, Iago Hale, Assaf Distelfeld, Matthew J. Hayden, Roberto Tuberosa, Sean Walkowiak, Klaus F.X. Mayer, Aldo Ceriotti, Curtis J. Pozniak, Luigi Cattivelli

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

Abstract

The domestication of wild emmer wheat led to the selection of modern durum wheat, grown mainly for pasta production. We describe the 10.45 gigabase (Gb) assembly of the genome of durum wheat cultivar Svevo. The assembly enabled genome-wide genetic diversity analyses revealing the changes imposed by thousands of years of empirical selection and breeding. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the genome with several major diversity losses in the pericentromeric regions. A locus on chromosome 5B carries a gene encoding a metal transporter (TdHMA3-B1) with a non-functional variant causing high accumulation of cadmium in grain. The high-cadmium allele, widespread among durum cultivars but undetected in wild emmer accessions, increased in frequency from domesticated emmer to modern durum wheat. The rapid cloning of TdHMA3-B1 rescues a wild beneficial allele and demonstrates the practical use of the Svevo genome for wheat improvement.

Original language	English
Pages (from-to)	885-895
Number of pages	11
Journal	Nature Genetics
Volume	51
Issue number	5
DOIs	https://doi.org/10.1038/s41588-019-0381-3
State	Published - 1 May 2019
Externally published	Yes

Bibliographical note

Funding Information:
We acknowledge the funding support of: the Italian Ministry of Education and Research with projects CNR Flagship InterOmics PB05 (L.M., A.C., G.S.), PON ELIXIR CNR-BiOmics PIR01_00017 (L.M., M.G., M.Mo.) and PON ISCOCEM (P.D.); CREA project Interomics (L.C.); Fondazione in rete per la ricerca agroalimentare AGER project From Seed to Pasta (R.T.); FP7-KBBE Project DROPS ID244347 (R.T.); Genome Canada (A.G.S., C.P.); the Western Grain Research Foundation (A.G.S., C.P.); the Manitoba Wheat and Barley Commission (A.G.S., C.P.); the Saskatchewan Wheat Development Commission (A.G.S., C.P.); the Alberta Wheat Development Commission (A.G.S., C.P.); the Saskatchewan Ministry of Agriculture (A.G.S., C.P.); the administrative support of Genome Prairie (A.G.S., C.P.); Canadian Triticum Applied Genomics -CTAG2-(A.G.S., C.P.); Binational Science Foundation grant no. 2015409 (I.H., A.D.); Israel Science Foundation grant no. 1137/17 (A.D.); USDA-Agricultural Research Service Current Research Information System project 3060-21000-038-00-D (J.D.F., S.S.X.); German Federal Ministry of Food and Agriculture grant no. 2819103915 (N.S., K.F.X.M.); German Ministry of Education and Research grant no. 031A536 (K.F.X.M.); and Natural Sciences and Engineering Council of Canada grant nos. SPG 336119-06 and RGPIN 92787 (G.J.T., C.P.). The authors are grateful to E. Elias (North Dakota State University) for providing nine DW cultivars, included in the Global Tetraploid Wheat Collection and E. Scarpella (University of Alberta, Edmonton, Canada) for assistance with confocal microscopy.

Publisher Copyright:
© 2019, The Author(s), under exclusive licence to Springer Nature America, Inc.

ASJC Scopus subject areas

Genetics

Access to Document

10.1038/s41588-019-0381-3

Cite this

Maccaferri, M., Harris, N. S., Twardziok, S. O., Pasam, R. K., Gundlach, H., Spannagl, M., Ormanbekova, D., Lux, T., Prade, V. M., Milner, S. G., Himmelbach, A., Mascher, M., Bagnaresi, P., Faccioli, P., Cozzi, P., Lauria, M., Lazzari, B., Stella, A., Manconi, A., ... Cattivelli, L. (2019). Durum wheat genome highlights past domestication signatures and future improvement targets. Nature Genetics, 51(5), 885-895. https://doi.org/10.1038/s41588-019-0381-3

@article{4e026c78e01548c5baa7c5375f8009e8,

title = "Durum wheat genome highlights past domestication signatures and future improvement targets",

abstract = "The domestication of wild emmer wheat led to the selection of modern durum wheat, grown mainly for pasta production. We describe the 10.45 gigabase (Gb) assembly of the genome of durum wheat cultivar Svevo. The assembly enabled genome-wide genetic diversity analyses revealing the changes imposed by thousands of years of empirical selection and breeding. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the genome with several major diversity losses in the pericentromeric regions. A locus on chromosome 5B carries a gene encoding a metal transporter (TdHMA3-B1) with a non-functional variant causing high accumulation of cadmium in grain. The high-cadmium allele, widespread among durum cultivars but undetected in wild emmer accessions, increased in frequency from domesticated emmer to modern durum wheat. The rapid cloning of TdHMA3-B1 rescues a wild beneficial allele and demonstrates the practical use of the Svevo genome for wheat improvement.",

author = "Marco Maccaferri and Harris, {Neil S.} and Twardziok, {Sven O.} and Pasam, {Raj K.} and Heidrun Gundlach and Manuel Spannagl and Danara Ormanbekova and Thomas Lux and Prade, {Verena M.} and Milner, {Sara G.} and Axel Himmelbach and Martin Mascher and Paolo Bagnaresi and Primetta Faccioli and Paolo Cozzi and Massimiliano Lauria and Barbara Lazzari and Alessandra Stella and Andrea Manconi and Matteo Gnocchi and Marco Moscatelli and Raz Avni and Jasline Deek and Sezgi Biyiklioglu and Elisabetta Frascaroli and Simona Corneti and Silvio Salvi and Gabriella Sonnante and Francesca Desiderio and Caterina Mar{\`e} and Cristina Crosatti and Erica Mica and Hakan {\"O}zkan and Benjamin Kilian and {De Vita}, Pasquale and Daniela Marone and Reem Joukhadar and Elisabetta Mazzucotelli and Domenica Nigro and Agata Gadaleta and Shiaoman Chao and Faris, {Justin D.} and Melo, {Arthur T.O.} and Mike Pumphrey and Nicola Pecchioni and Luciano Milanesi and Krystalee Wiebe and Jennifer Ens and MacLachlan, {Ron P.} and Clarke, {John M.} and Sharpe, {Andrew G.} and Koh, {Chu Shin} and Liang, {Kevin Y.H.} and Taylor, {Gregory J.} and Ron Knox and Hikmet Budak and Mastrangelo, {Anna M.} and Xu, {Steven S.} and Nils Stein and Iago Hale and Assaf Distelfeld and Hayden, {Matthew J.} and Roberto Tuberosa and Sean Walkowiak and Mayer, {Klaus F.X.} and Aldo Ceriotti and Pozniak, {Curtis J.} and Luigi Cattivelli",

note = "Funding Information: We acknowledge the funding support of: the Italian Ministry of Education and Research with projects CNR Flagship InterOmics PB05 (L.M., A.C., G.S.), PON ELIXIR CNR-BiOmics PIR01_00017 (L.M., M.G., M.Mo.) and PON ISCOCEM (P.D.); CREA project Interomics (L.C.); Fondazione in rete per la ricerca agroalimentare AGER project From Seed to Pasta (R.T.); FP7-KBBE Project DROPS ID244347 (R.T.); Genome Canada (A.G.S., C.P.); the Western Grain Research Foundation (A.G.S., C.P.); the Manitoba Wheat and Barley Commission (A.G.S., C.P.); the Saskatchewan Wheat Development Commission (A.G.S., C.P.); the Alberta Wheat Development Commission (A.G.S., C.P.); the Saskatchewan Ministry of Agriculture (A.G.S., C.P.); the administrative support of Genome Prairie (A.G.S., C.P.); Canadian Triticum Applied Genomics -CTAG2-(A.G.S., C.P.); Binational Science Foundation grant no. 2015409 (I.H., A.D.); Israel Science Foundation grant no. 1137/17 (A.D.); USDA-Agricultural Research Service Current Research Information System project 3060-21000-038-00-D (J.D.F., S.S.X.); German Federal Ministry of Food and Agriculture grant no. 2819103915 (N.S., K.F.X.M.); German Ministry of Education and Research grant no. 031A536 (K.F.X.M.); and Natural Sciences and Engineering Council of Canada grant nos. SPG 336119-06 and RGPIN 92787 (G.J.T., C.P.). The authors are grateful to E. Elias (North Dakota State University) for providing nine DW cultivars, included in the Global Tetraploid Wheat Collection and E. Scarpella (University of Alberta, Edmonton, Canada) for assistance with confocal microscopy. Publisher Copyright: {\textcopyright} 2019, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2019",

month = may,

day = "1",

doi = "10.1038/s41588-019-0381-3",

language = "English",

volume = "51",

pages = "885--895",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "5",

}

Maccaferri, M, Harris, NS, Twardziok, SO, Pasam, RK, Gundlach, H, Spannagl, M, Ormanbekova, D, Lux, T, Prade, VM, Milner, SG, Himmelbach, A, Mascher, M, Bagnaresi, P, Faccioli, P, Cozzi, P, Lauria, M, Lazzari, B, Stella, A, Manconi, A, Gnocchi, M, Moscatelli, M, Avni, R, Deek, J, Biyiklioglu, S, Frascaroli, E, Corneti, S, Salvi, S, Sonnante, G, Desiderio, F, Marè, C, Crosatti, C, Mica, E, Özkan, H, Kilian, B, De Vita, P, Marone, D, Joukhadar, R, Mazzucotelli, E, Nigro, D, Gadaleta, A, Chao, S, Faris, JD, Melo, ATO, Pumphrey, M, Pecchioni, N, Milanesi, L, Wiebe, K, Ens, J, MacLachlan, RP, Clarke, JM, Sharpe, AG, Koh, CS, Liang, KYH, Taylor, GJ, Knox, R, Budak, H, Mastrangelo, AM, Xu, SS, Stein, N, Hale, I, Distelfeld, A, Hayden, MJ, Tuberosa, R, Walkowiak, S, Mayer, KFX, Ceriotti, A, Pozniak, CJ & Cattivelli, L 2019, 'Durum wheat genome highlights past domestication signatures and future improvement targets', Nature Genetics, vol. 51, no. 5, pp. 885-895. https://doi.org/10.1038/s41588-019-0381-3

TY - JOUR

T1 - Durum wheat genome highlights past domestication signatures and future improvement targets

AU - Maccaferri, Marco

AU - Harris, Neil S.

AU - Twardziok, Sven O.

AU - Pasam, Raj K.

AU - Gundlach, Heidrun

AU - Spannagl, Manuel

AU - Ormanbekova, Danara

AU - Lux, Thomas

AU - Prade, Verena M.

AU - Milner, Sara G.

AU - Himmelbach, Axel

AU - Mascher, Martin

AU - Bagnaresi, Paolo

AU - Faccioli, Primetta

AU - Cozzi, Paolo

AU - Lauria, Massimiliano

AU - Lazzari, Barbara

AU - Stella, Alessandra

AU - Manconi, Andrea

AU - Gnocchi, Matteo

AU - Moscatelli, Marco

AU - Avni, Raz

AU - Deek, Jasline

AU - Biyiklioglu, Sezgi

AU - Frascaroli, Elisabetta

AU - Corneti, Simona

AU - Salvi, Silvio

AU - Sonnante, Gabriella

AU - Desiderio, Francesca

AU - Marè, Caterina

AU - Crosatti, Cristina

AU - Mica, Erica

AU - Özkan, Hakan

AU - Kilian, Benjamin

AU - De Vita, Pasquale

AU - Marone, Daniela

AU - Joukhadar, Reem

AU - Mazzucotelli, Elisabetta

AU - Nigro, Domenica

AU - Gadaleta, Agata

AU - Chao, Shiaoman

AU - Faris, Justin D.

AU - Melo, Arthur T.O.

AU - Pumphrey, Mike

AU - Pecchioni, Nicola

AU - Milanesi, Luciano

AU - Wiebe, Krystalee

AU - Ens, Jennifer

AU - MacLachlan, Ron P.

AU - Clarke, John M.

AU - Sharpe, Andrew G.

AU - Koh, Chu Shin

AU - Liang, Kevin Y.H.

AU - Taylor, Gregory J.

AU - Knox, Ron

AU - Budak, Hikmet

AU - Mastrangelo, Anna M.

AU - Xu, Steven S.

AU - Stein, Nils

AU - Hale, Iago

AU - Distelfeld, Assaf

AU - Hayden, Matthew J.

AU - Tuberosa, Roberto

AU - Walkowiak, Sean

AU - Mayer, Klaus F.X.

AU - Ceriotti, Aldo

AU - Pozniak, Curtis J.

AU - Cattivelli, Luigi

N1 - Funding Information: We acknowledge the funding support of: the Italian Ministry of Education and Research with projects CNR Flagship InterOmics PB05 (L.M., A.C., G.S.), PON ELIXIR CNR-BiOmics PIR01_00017 (L.M., M.G., M.Mo.) and PON ISCOCEM (P.D.); CREA project Interomics (L.C.); Fondazione in rete per la ricerca agroalimentare AGER project From Seed to Pasta (R.T.); FP7-KBBE Project DROPS ID244347 (R.T.); Genome Canada (A.G.S., C.P.); the Western Grain Research Foundation (A.G.S., C.P.); the Manitoba Wheat and Barley Commission (A.G.S., C.P.); the Saskatchewan Wheat Development Commission (A.G.S., C.P.); the Alberta Wheat Development Commission (A.G.S., C.P.); the Saskatchewan Ministry of Agriculture (A.G.S., C.P.); the administrative support of Genome Prairie (A.G.S., C.P.); Canadian Triticum Applied Genomics -CTAG2-(A.G.S., C.P.); Binational Science Foundation grant no. 2015409 (I.H., A.D.); Israel Science Foundation grant no. 1137/17 (A.D.); USDA-Agricultural Research Service Current Research Information System project 3060-21000-038-00-D (J.D.F., S.S.X.); German Federal Ministry of Food and Agriculture grant no. 2819103915 (N.S., K.F.X.M.); German Ministry of Education and Research grant no. 031A536 (K.F.X.M.); and Natural Sciences and Engineering Council of Canada grant nos. SPG 336119-06 and RGPIN 92787 (G.J.T., C.P.). The authors are grateful to E. Elias (North Dakota State University) for providing nine DW cultivars, included in the Global Tetraploid Wheat Collection and E. Scarpella (University of Alberta, Edmonton, Canada) for assistance with confocal microscopy. Publisher Copyright: © 2019, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2019/5/1

Y1 - 2019/5/1

N2 - The domestication of wild emmer wheat led to the selection of modern durum wheat, grown mainly for pasta production. We describe the 10.45 gigabase (Gb) assembly of the genome of durum wheat cultivar Svevo. The assembly enabled genome-wide genetic diversity analyses revealing the changes imposed by thousands of years of empirical selection and breeding. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the genome with several major diversity losses in the pericentromeric regions. A locus on chromosome 5B carries a gene encoding a metal transporter (TdHMA3-B1) with a non-functional variant causing high accumulation of cadmium in grain. The high-cadmium allele, widespread among durum cultivars but undetected in wild emmer accessions, increased in frequency from domesticated emmer to modern durum wheat. The rapid cloning of TdHMA3-B1 rescues a wild beneficial allele and demonstrates the practical use of the Svevo genome for wheat improvement.

AB - The domestication of wild emmer wheat led to the selection of modern durum wheat, grown mainly for pasta production. We describe the 10.45 gigabase (Gb) assembly of the genome of durum wheat cultivar Svevo. The assembly enabled genome-wide genetic diversity analyses revealing the changes imposed by thousands of years of empirical selection and breeding. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the genome with several major diversity losses in the pericentromeric regions. A locus on chromosome 5B carries a gene encoding a metal transporter (TdHMA3-B1) with a non-functional variant causing high accumulation of cadmium in grain. The high-cadmium allele, widespread among durum cultivars but undetected in wild emmer accessions, increased in frequency from domesticated emmer to modern durum wheat. The rapid cloning of TdHMA3-B1 rescues a wild beneficial allele and demonstrates the practical use of the Svevo genome for wheat improvement.

UR - http://www.scopus.com/inward/record.url?scp=85064088613&partnerID=8YFLogxK

U2 - 10.1038/s41588-019-0381-3

DO - 10.1038/s41588-019-0381-3

M3 - Article

C2 - 30962619

AN - SCOPUS:85064088613

VL - 51

SP - 885

EP - 895

JO - Nature Genetics

JF - Nature Genetics

SN - 1061-4036

IS - 5

ER -

Durum wheat genome highlights past domestication signatures and future improvement targets

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this