Harnessing landrace diversity empowers wheat breeding

Shifeng Cheng; Cong Feng; Luzie U Wingen; Hong Cheng; Andrew B Riche; Mei Jiang; Michelle Leverington-Waite; Zejian Huang; Sarah Collier; Simon Orford; Xiaoming Wang; Rajani Awal; Gary Barker; Tom O'Hara; Clare Lister; Ajay Siluveru; Jesús Quiroz-Chávez; Ricardo H Ramírez-González; Ruth Bryant; Simon Berry; Urmil Bansal; Harbans S Bariana; Malcolm J Bennett; Breno Bicego; Lorelei Bilham; James K M Brown; Amanda Burridge; Chris Burt; Milika Buurman; March Castle; Laetitia Chartrain; Baizhi Chen; Worku Denbel; Ahmed F Elkot; Paul Fenwick; David Feuerhelm; John Foulkes; Oorbessy Gaju; Adam Gauley; Kumar Gaurav; Amber N Hafeez; Ruirui Han; Richard Horler; Junliang Hou; Muhammad S Iqbal; Matthew Kerton; Ankica Kondic-Spica; Ania Kowalski; Jacob Lage; Xiaolong Li; Hongbing Liu; Shiyan Liu; Alison Lovegrove; Lingling Ma; Cathy Mumford; Saroj Parmar; Charlie Philp; Darryl Playford; Alexandra M Przewieslik-Allen; Zareen Sarfraz; David Schafer; Peter R Shewry; Yan Shi; Gustavo Slafer; Baoxing Song; Bo Song; David Steele; Burkhard Steuernagel; Phillip Tailby; Simon Tyrrell; Abdul Waheed; Mercy N Wamalwa; Xingwei Wang; Yanping Wei; Mark Winfield; Shishi Wu; Yubing Wu; Brande B H Wulff; Wenfei Xian; Yawen Xu; Yunfeng Xu; Quan Yuan; Keith J Edwards; Laura Dixon; Paul Nicholson; Noam Chayut; Malcolm J Hawkesford; Cristobal Uauy; Dale Sanders; Sanwen Huang; Simon Griffiths

doi:10.1038/s41586-024-07682-9

Harnessing landrace diversity empowers wheat breeding

Shifeng Cheng^*, Cong Feng, Luzie U Wingen, Hong Cheng, Andrew B Riche, Mei Jiang, Michelle Leverington-Waite, Zejian Huang, Sarah Collier, Simon Orford, Xiaoming Wang, Rajani Awal, Gary Barker, Tom O'Hara, Clare Lister, Ajay Siluveru, Jesús Quiroz-Chávez, Ricardo H Ramírez-González, Ruth Bryant, Simon BerryUrmil Bansal, Harbans S Bariana, Malcolm J Bennett, Breno Bicego, Lorelei Bilham, James K M Brown, Amanda Burridge, Chris Burt, Milika Buurman, March Castle, Laetitia Chartrain, Baizhi Chen, Worku Denbel, Ahmed F Elkot, Paul Fenwick, David Feuerhelm, John Foulkes, Oorbessy Gaju, Adam Gauley, Kumar Gaurav, Amber N Hafeez, Ruirui Han, Richard Horler, Junliang Hou, Muhammad S Iqbal, Matthew Kerton, Ankica Kondic-Spica, Ania Kowalski, Jacob Lage, Xiaolong Li, Hongbing Liu, Shiyan Liu, Alison Lovegrove, Lingling Ma, Cathy Mumford, Saroj Parmar, Charlie Philp, Darryl Playford, Alexandra M Przewieslik-Allen, Zareen Sarfraz, David Schafer, Peter R Shewry, Yan Shi, Gustavo Slafer, Baoxing Song, Bo Song, David Steele, Burkhard Steuernagel, Phillip Tailby, Simon Tyrrell, Abdul Waheed, Mercy N Wamalwa, Xingwei Wang, Yanping Wei, Mark Winfield, Shishi Wu, Yubing Wu, Brande B H Wulff, Wenfei Xian, Yawen Xu, Yunfeng Xu, Quan Yuan, Keith J Edwards, Laura Dixon, Paul Nicholson, Noam Chayut, Malcolm J Hawkesford, Cristobal Uauy, Dale Sanders, Sanwen Huang, Simon Griffiths^*

^*Corresponding author for this work

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Abstract

Harnessing genetic diversity in major staple crops through the development of new breeding capabilities is essential to ensure food security1. Here we examined the genetic and phenotypic diversity of the A.E. Watkins landrace collection2 of bread wheat (Triticum aestivum), a major global cereal, through whole-genome re-sequencing (827 Watkins landraces and 208 modern cultivars) and in-depth field evaluation spanning a decade. We discovered that modern cultivars are derived from just two of the seven ancestral groups of wheat and maintain very long-range haplotype integrity. The remaining five groups represent untapped genetic sources, providing access to landrace-specific alleles and haplotypes for breeding. Linkage disequilibrium (LD) based haplotypes and association genetics analyses link Watkins genomes to the thousands of high-resolution quantitative trait loci (QTL), and significant marker-trait associations identified. Using these structured germplasm, genotyping and informatics resources, we revealed many Watkins-unique beneficial haplotypes that can confer superior traits in modern wheat. Furthermore, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritised QTL in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilising genetic diversity in crop improvement to achieve sustainable food security.

Original language	English
Pages (from-to)	823-831
Number of pages	9
Journal	Nature
Volume	632
Issue number	8026
Early online date	17 Jun 2024
DOIs	https://doi.org/10.1038/s41586-024-07682-9
Publication status	E-pub ahead of print - 17 Jun 2024

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© The Author(s) 2024.

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Cheng, S., Feng, C., Wingen, L. U., Cheng, H., Riche, A. B., Jiang, M., Leverington-Waite, M., Huang, Z., Collier, S., Orford, S., Wang, X., Awal, R., Barker, G., O'Hara, T., Lister, C., Siluveru, A., Quiroz-Chávez, J., Ramírez-González, R. H., Bryant, R., ... Griffiths, S. (2024). Harnessing landrace diversity empowers wheat breeding. Nature, 632(8026), 823-831. Advance online publication. https://doi.org/10.1038/s41586-024-07682-9

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title = "Harnessing landrace diversity empowers wheat breeding",

abstract = "Harnessing genetic diversity in major staple crops through the development of new breeding capabilities is essential to ensure food security1. Here we examined the genetic and phenotypic diversity of the A.E. Watkins landrace collection2 of bread wheat (Triticum aestivum), a major global cereal, through whole-genome re-sequencing (827 Watkins landraces and 208 modern cultivars) and in-depth field evaluation spanning a decade. We discovered that modern cultivars are derived from just two of the seven ancestral groups of wheat and maintain very long-range haplotype integrity. The remaining five groups represent untapped genetic sources, providing access to landrace-specific alleles and haplotypes for breeding. Linkage disequilibrium (LD) based haplotypes and association genetics analyses link Watkins genomes to the thousands of high-resolution quantitative trait loci (QTL), and significant marker-trait associations identified. Using these structured germplasm, genotyping and informatics resources, we revealed many Watkins-unique beneficial haplotypes that can confer superior traits in modern wheat. Furthermore, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritised QTL in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilising genetic diversity in crop improvement to achieve sustainable food security.",

author = "Shifeng Cheng and Cong Feng and Wingen, {Luzie U} and Hong Cheng and Riche, {Andrew B} and Mei Jiang and Michelle Leverington-Waite and Zejian Huang and Sarah Collier and Simon Orford and Xiaoming Wang and Rajani Awal and Gary Barker and Tom O'Hara and Clare Lister and Ajay Siluveru and Jes{\'u}s Quiroz-Ch{\'a}vez and Ram{\'i}rez-Gonz{\'a}lez, {Ricardo H} and Ruth Bryant and Simon Berry and Urmil Bansal and Bariana, {Harbans S} and Bennett, {Malcolm J} and Breno Bicego and Lorelei Bilham and Brown, {James K M} and Amanda Burridge and Chris Burt and Milika Buurman and March Castle and Laetitia Chartrain and Baizhi Chen and Worku Denbel and Elkot, {Ahmed F} and Paul Fenwick and David Feuerhelm and John Foulkes and Oorbessy Gaju and Adam Gauley and Kumar Gaurav and Hafeez, {Amber N} and Ruirui Han and Richard Horler and Junliang Hou and Iqbal, {Muhammad S} and Matthew Kerton and Ankica Kondic-Spica and Ania Kowalski and Jacob Lage and Xiaolong Li and Hongbing Liu and Shiyan Liu and Alison Lovegrove and Lingling Ma and Cathy Mumford and Saroj Parmar and Charlie Philp and Darryl Playford and Przewieslik-Allen, {Alexandra M} and Zareen Sarfraz and David Schafer and Shewry, {Peter R} and Yan Shi and Gustavo Slafer and Baoxing Song and Bo Song and David Steele and Burkhard Steuernagel and Phillip Tailby and Simon Tyrrell and Abdul Waheed and Wamalwa, {Mercy N} and Xingwei Wang and Yanping Wei and Mark Winfield and Shishi Wu and Yubing Wu and Wulff, {Brande B H} and Wenfei Xian and Yawen Xu and Yunfeng Xu and Quan Yuan and Edwards, {Keith J} and Laura Dixon and Paul Nicholson and Noam Chayut and Hawkesford, {Malcolm J} and Cristobal Uauy and Dale Sanders and Sanwen Huang and Simon Griffiths",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

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doi = "10.1038/s41586-024-07682-9",

language = "English",

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Cheng, S, Feng, C, Wingen, LU, Cheng, H, Riche, AB, Jiang, M, Leverington-Waite, M, Huang, Z, Collier, S, Orford, S, Wang, X, Awal, R, Barker, G, O'Hara, T, Lister, C, Siluveru, A, Quiroz-Chávez, J, Ramírez-González, RH, Bryant, R, Berry, S, Bansal, U, Bariana, HS, Bennett, MJ, Bicego, B, Bilham, L, Brown, JKM, Burridge, A, Burt, C, Buurman, M, Castle, M, Chartrain, L, Chen, B, Denbel, W, Elkot, AF, Fenwick, P, Feuerhelm, D, Foulkes, J, Gaju, O, Gauley, A, Gaurav, K, Hafeez, AN, Han, R, Horler, R, Hou, J, Iqbal, MS, Kerton, M, Kondic-Spica, A, Kowalski, A, Lage, J, Li, X, Liu, H, Liu, S, Lovegrove, A, Ma, L, Mumford, C, Parmar, S, Philp, C, Playford, D, Przewieslik-Allen, AM, Sarfraz, Z, Schafer, D, Shewry, PR, Shi, Y, Slafer, G, Song, B, Song, B, Steele, D, Steuernagel, B, Tailby, P, Tyrrell, S, Waheed, A, Wamalwa, MN, Wang, X, Wei, Y, Winfield, M, Wu, S, Wu, Y, Wulff, BBH, Xian, W, Xu, Y, Xu, Y, Yuan, Q, Edwards, KJ, Dixon, L, Nicholson, P, Chayut, N, Hawkesford, MJ, Uauy, C, Sanders, D, Huang, S & Griffiths, S 2024, 'Harnessing landrace diversity empowers wheat breeding', Nature, vol. 632, no. 8026, pp. 823-831. https://doi.org/10.1038/s41586-024-07682-9

TY - JOUR

T1 - Harnessing landrace diversity empowers wheat breeding

AU - Cheng, Shifeng

AU - Feng, Cong

AU - Wingen, Luzie U

AU - Cheng, Hong

AU - Riche, Andrew B

AU - Jiang, Mei

AU - Leverington-Waite, Michelle

AU - Huang, Zejian

AU - Collier, Sarah

AU - Orford, Simon

AU - Wang, Xiaoming

AU - Awal, Rajani

AU - Barker, Gary

AU - O'Hara, Tom

AU - Lister, Clare

AU - Siluveru, Ajay

AU - Quiroz-Chávez, Jesús

AU - Ramírez-González, Ricardo H

AU - Bryant, Ruth

AU - Berry, Simon

AU - Bansal, Urmil

AU - Bariana, Harbans S

AU - Bennett, Malcolm J

AU - Bicego, Breno

AU - Bilham, Lorelei

AU - Brown, James K M

AU - Burridge, Amanda

AU - Burt, Chris

AU - Buurman, Milika

AU - Castle, March

AU - Chartrain, Laetitia

AU - Chen, Baizhi

AU - Denbel, Worku

AU - Elkot, Ahmed F

AU - Fenwick, Paul

AU - Feuerhelm, David

AU - Foulkes, John

AU - Gaju, Oorbessy

AU - Gauley, Adam

AU - Gaurav, Kumar

AU - Hafeez, Amber N

AU - Han, Ruirui

AU - Horler, Richard

AU - Hou, Junliang

AU - Iqbal, Muhammad S

AU - Kerton, Matthew

AU - Kondic-Spica, Ankica

AU - Kowalski, Ania

AU - Lage, Jacob

AU - Li, Xiaolong

AU - Liu, Hongbing

AU - Liu, Shiyan

AU - Lovegrove, Alison

AU - Ma, Lingling

AU - Mumford, Cathy

AU - Parmar, Saroj

AU - Philp, Charlie

AU - Playford, Darryl

AU - Przewieslik-Allen, Alexandra M

AU - Sarfraz, Zareen

AU - Schafer, David

AU - Shewry, Peter R

AU - Shi, Yan

AU - Slafer, Gustavo

AU - Song, Baoxing

AU - Song, Bo

AU - Steele, David

AU - Steuernagel, Burkhard

AU - Tailby, Phillip

AU - Tyrrell, Simon

AU - Waheed, Abdul

AU - Wamalwa, Mercy N

AU - Wang, Xingwei

AU - Wei, Yanping

AU - Winfield, Mark

AU - Wu, Shishi

AU - Wu, Yubing

AU - Wulff, Brande B H

AU - Xian, Wenfei

AU - Xu, Yawen

AU - Xu, Yunfeng

AU - Yuan, Quan

AU - Edwards, Keith J

AU - Dixon, Laura

AU - Nicholson, Paul

AU - Chayut, Noam

AU - Hawkesford, Malcolm J

AU - Uauy, Cristobal

AU - Sanders, Dale

AU - Huang, Sanwen

AU - Griffiths, Simon

PY - 2024/6/17

Y1 - 2024/6/17

N2 - Harnessing genetic diversity in major staple crops through the development of new breeding capabilities is essential to ensure food security1. Here we examined the genetic and phenotypic diversity of the A.E. Watkins landrace collection2 of bread wheat (Triticum aestivum), a major global cereal, through whole-genome re-sequencing (827 Watkins landraces and 208 modern cultivars) and in-depth field evaluation spanning a decade. We discovered that modern cultivars are derived from just two of the seven ancestral groups of wheat and maintain very long-range haplotype integrity. The remaining five groups represent untapped genetic sources, providing access to landrace-specific alleles and haplotypes for breeding. Linkage disequilibrium (LD) based haplotypes and association genetics analyses link Watkins genomes to the thousands of high-resolution quantitative trait loci (QTL), and significant marker-trait associations identified. Using these structured germplasm, genotyping and informatics resources, we revealed many Watkins-unique beneficial haplotypes that can confer superior traits in modern wheat. Furthermore, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritised QTL in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilising genetic diversity in crop improvement to achieve sustainable food security.

AB - Harnessing genetic diversity in major staple crops through the development of new breeding capabilities is essential to ensure food security1. Here we examined the genetic and phenotypic diversity of the A.E. Watkins landrace collection2 of bread wheat (Triticum aestivum), a major global cereal, through whole-genome re-sequencing (827 Watkins landraces and 208 modern cultivars) and in-depth field evaluation spanning a decade. We discovered that modern cultivars are derived from just two of the seven ancestral groups of wheat and maintain very long-range haplotype integrity. The remaining five groups represent untapped genetic sources, providing access to landrace-specific alleles and haplotypes for breeding. Linkage disequilibrium (LD) based haplotypes and association genetics analyses link Watkins genomes to the thousands of high-resolution quantitative trait loci (QTL), and significant marker-trait associations identified. Using these structured germplasm, genotyping and informatics resources, we revealed many Watkins-unique beneficial haplotypes that can confer superior traits in modern wheat. Furthermore, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritised QTL in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilising genetic diversity in crop improvement to achieve sustainable food security.

U2 - 10.1038/s41586-024-07682-9

DO - 10.1038/s41586-024-07682-9

M3 - Article (Academic Journal)

C2 - 38885696

SN - 0028-0836

VL - 632

SP - 823

EP - 831

JO - Nature

JF - Nature

IS - 8026

ER -

Harnessing landrace diversity empowers wheat breeding

Abstract

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