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

^*Corresponding author for this work

School of Plant Sciences and Food Security

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

533 Scopus citations

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

Funding

Funders	Funder number
Saskatchewan Wheat Development Commission
Alberta Wheat Development Commission
Genome Prairie
Genome Canada
Western Grains Research Foundation
Haridus- ja Teadusministeerium
Manitoba Wheat and Barley Commission
European Commission
Canadian Triticum Applied Genomics
USDA-Agricultural
Ministry of Agriculture - Saskatchewan
Creative Europe
Bundesministerium für Ernährung und Landwirtschaft	2819103915
Seventh Framework Programme	244374
United States-Israel Binational Science Foundation	2015409
Natural Sciences and Engineering Research Council of Canada	RGPIN 92787, SPG 336119-06
Israel Science Foundation	1137/17
FP7 Food, Agriculture and Fisheries, Biotechnology	DROPS ID244347
Bundesministerium für Bildung und Forschung	031A536
Consiglio Nazionale delle Ricerche	PIR01_00017

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41588-019-0381-3

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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

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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 = "Publisher Copyright: {\textcopyright} 2019, The Author(s), under exclusive licence to Springer Nature America, Inc.",

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

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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

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.

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Durum wheat genome highlights past domestication signatures and future improvement targets

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UN SDGs

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