Shifting the limits in wheat research and breeding using a fully annotated reference genome
Insights from the annotated wheat genome
Wheat is one of the major sources of food for much of the world. However, because bread wheat's genome is a large hybrid mix of three separate subgenomes, it has been difficult to produce a high-quality reference sequence. Using recent advances in sequencing, the International Wheat Genome Sequencing Consortium presents an annotated reference genome with a detailed analysis of gene content among subgenomes and the structural organization for all the chromosomes. Examples of quantitative trait mapping and CRISPR-based genome modification show the potential for using this genome in agricultural research and breeding. Ramírez-González et al. exploited the fruits of this endeavor to identify tissue-specific biased gene expression and coexpression networks during development and exposure to stress. These resources will accelerate our understanding of the genetic basis of bread wheat.
Structured Abstract
INTRODUCTION
Wheat (Triticum aestivum L.) is the most widely cultivated crop on Earth, contributing about a fifth of the total calories consumed by humans. Consequently, wheat yields and production affect the global economy, and failed harvests can lead to social unrest. Breeders continuously strive to develop improved varieties by fine-tuning genetically complex yield and end-use quality parameters while maintaining stable yields and adapting the crop to regionally specific biotic and abiotic stresses.
RATIONALE
Breeding efforts are limited by insufficient knowledge and understanding of wheat biology and the molecular basis of central agronomic traits. To meet the demands of human population growth, there is an urgent need for wheat research and breeding to accelerate genetic gain as well as to increase and protect wheat yield and quality traits. In other plant and animal species, access to a fully annotated and ordered genome sequence, including regulatory sequences and genome-diversity information, has promoted the development of systematic and more time-efficient approaches for the selection and understanding of important traits. Wheat has lagged behind, primarily owing to the challenges of assembling a genome that is more than five times as large as the human genome, polyploid, and complex, containing more than 85% repetitive DNA. To provide a foundation for improvement through molecular breeding, in 2005, the International Wheat Genome Sequencing Consortium set out to deliver a high-quality annotated reference genome sequence of bread wheat.
RESULTS
An annotated reference sequence representing the hexaploid bread wheat genome in the form of 21 chromosome-like sequence assemblies has now been delivered, giving access to 107,891 high-confidence genes, including their genomic context of regulatory sequences. This assembly enabled the discovery of tissue- and developmental stage–related gene coexpression networks using a transcriptome atlas representing all stages of wheat development. The dynamics of change in complex gene families involved in environmental adaptation and end-use quality were revealed at subgenome resolution and contextualized to known agronomic single-gene or quantitative trait loci. Aspects of the future value of the annotated assembly for molecular breeding and research were exemplarily illustrated by resolving the genetic basis of a quantitative trait locus conferring resistance to abiotic stress and insect damage as well as by serving as the basis for genome editing of the flowering-time trait.
CONCLUSION
This annotated reference sequence of wheat is a resource that can now drive disruptive innovation in wheat improvement, as this community resource establishes the foundation for accelerating wheat research and application through improved understanding of wheat biology and genomics-assisted breeding. Importantly, the bioinformatics capacity developed for model-organism genomes will facilitate a better understanding of the wheat genome as a result of the high-quality chromosome-based genome assembly. By necessity, breeders work with the genome at the whole chromosome level, as each new cross involves the modification of genome-wide gene networks that control the expression of complex traits such as yield. With the annotated and ordered reference genome sequence in place, researchers and breeders can now easily access sequence-level information to precisely define the necessary changes in the genomes for breeding programs. This will be realized through the implementation of new DNA marker platforms and targeted breeding technologies, including genome editing.
Wheat genome deciphered, assembled, and ordered.
Seeds, or grains, are what counts with respect to wheat yields (left panel), but all parts of the plant contribute to crop performance. With complete access to the ordered sequence of all 21 wheat chromosomes, the context of regulatory sequences, and the interaction network of expressed genes—all shown here as a circular plot (right panel) with concentric tracks for diverse aspects of wheat genome composition—breeders and researchers now have the ability to rewrite the story of wheat crop improvement. Details on value ranges underlying the concentric heatmaps of the right panel are provided in the full article online.
Abstract
An annotated reference sequence representing the hexaploid bread wheat genome in 21 pseudomolecules has been analyzed to identify the distribution and genomic context of coding and noncoding elements across the A, B, and D subgenomes. With an estimated coverage of 94% of the genome and containing 107,891 high-confidence gene models, this assembly enabled the discovery of tissue- and developmental stage–related coexpression networks by providing a transcriptome atlas representing major stages of wheat development. Dynamics of complex gene families involved in environmental adaptation and end-use quality were revealed at subgenome resolution and contextualized to known agronomic single-gene or quantitative trait loci. This community resource establishes the foundation for accelerating wheat research and application through improved understanding of wheat biology and genomics-assisted breeding.
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Supplementary Material
Summary
Materials and Methods
Figs. S1 to S59
Tables S1 to S43
Databases S1 to S5
Resources
References and Notes
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Volume 361 | Issue 6403
17 August 2018
17 August 2018
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Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Submission history
Received: 13 December 2017
Accepted: 11 July 2018
Published in print: 17 August 2018
Acknowledgments
The IWGSC would like to thank the following individuals: M. Burrell and C. Bridson (Norwich Biosciences Institute) for computational support of RNA-seq data; I. Christie (Graminor AS) and H. Rudi (Norwegian University of Life Sciences) for assistance with chromosome 7B; R. P. Davey (Earlham Institute) for assistance with RNA-seq data; J. Deek (Tel Aviv University) for growing the source plants and DNA extraction used for whole-genome sequencing; Z. Dubská, E. Jahnová, M. Seifertová, R. Šperková, R. Tušková, and J. Weiserová (Institute of Experimental Botany, Olomouc) for assistance with flow cytometric chromosome sorting, BAC library construction, and estimation of genome size; S. Durand, V. Jamilloux, M. Lainé, and C. Michotey (URGI, INRA) for assistance with and access to the IWGSC sequence repository; A. Fiebig of the Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) for submitting the Hi-C data; T. Florio for the design of the wheat schematic for the expression atlas and SSt1 figure (www.flozbox.com/Science_Illustrated); C. Karunakaran and T. Bond of the Canadian Light Source for performing CT imaging; J. Kawai, N. Kondo, H. Sano, N. Suzuki, M. Tagami, and H. Tarui of RIKEN for assistance with deep sequencing of chromosome 6B; H. Fujisawa, Y. Katayose, K. Kurita, S. Mori, Y. Mukai, and H. Sasaki of the Institute of Crop Science, NARO for assistance with deep sequencing of chromosome 6B; T. Matsumoto of Tokyo University of Agriculture for assistance with deep sequencing of chromosome 6B; P. Lenoble and C. Orvain of Genoscope for assistance in the sequencing of chromosome 1B; A. J. Lukaszewski of the University of California, Riverside, and B. Friebe and J. Raupp of Kansas State University for providing seeds of wheat telosomic lines for chromosome sorting; C. Maulis (https://polytypo.design; https://propepper.net) for design and graphics of the prolamin superfamily chromosome map; M. Seifertová and H. Tvardíková of the Institute of Experimental Botany for assistance with BAC DNA extraction and sequencing for chromosomes 3DS, 4A, and 7DS; and I. Willick and K. Tanino of the University of Saskatchewan for their assistance in sample preparation and the use of lab facilities. Funding: The authors would like to thank the following for their financial support of research that enabled the completion of the IWGSC RefSeq v1.0 Project: Agence Nationale pour la Recherche (ANR), ANR-11-BSV5-0015–Ploid-Ploid Wheat–Unravelling bases of polyploidy success in wheat and ANR-16-TERC-0026-01–3DWHEAT; Agriculture and Agri-Food Canada National Wheat Improvement Program and the AgriFlex Program; Alberta Wheat Development Commission through the Canadian Applied Tricticum Genomics (CTAG2); Australian Government, Department of Industry, Innovation, Climate Change, Science, Research, and Tertiary Education, Australia China Science and Research Fund Group Mission (Funding Agreement ACSRF00542); Australian Research Council Centre of Excellence in Plant Energy Biology (CE140100008); Australian Research Council Laureate Fellowship (FL140100179); Bayer CropScience; Biotechnology and Biological Sciences Research Council (BBSRC) 20:20 Wheat (project number BB/J00426X/1), Institute Strategic Programme grant (BB/J004669/1), Designing Future Wheat (DFW) Institute Strategic Programme (BB/P016855/1), the Wheat Genomics for Sustainable Agriculture (BB/J003557/1), and the Anniversary Future Leader Fellowship (BB/M014045/1); Canada First Research Excellence Fund through the Designing Crops for Global Food Security initiative at the University of Saskatchewan; Council for Agricultural Research and Economics, Italy, through CREA-Interomics; Department of Biotechnology, Ministry of Science and Technology, Government of India File No. F grant no. BT/IWGSC/03/TF/2008; DFG (SFB924) for support of KFXM; European Commission through the TriticeaeGenome (FP7-212019); France Génomique (ANR-10-INBS-09) Genome Canada through the CTAG2 project; Genome Prairie through the CTAG2 project; German Academic Exchange Service (DAAD) PPP Australien 1j16; German Federal Ministry of Food and Agriculture grant 2819103915 WHEATSEQ; German Ministry of Education and Research grant 031A536 de.NBI; Global Institute for Food Security Genomics and Bioinformatics fund; Gordon and Betty Moore Foundation grant GBMF4725 to Two Blades Foundation; Grain Research Development Corporation (GRDC) Australia; Graminor AS NFR project 199387, Expanding the technology base for Norwegian wheat breeding; Sequencing wheat chromosome 7B; illumina; INRA, French National Institute for Agricultural Research; International Wheat Genome Sequencing Consortium and its sponsors; Israel Science Foundation grants 999/12, 1137/17, and 1824/12; Junta de Andalucía, Spain, project P12-AGR-0482; MINECO (Spanish Ministry of Economy, Industry, and Competitiveness) project BIO2011-15237-E; Ministry of Agriculture, Forestry, and Fisheries of Japan through Genomics for Agricultural Innovation, KGS-1003 and through Genomics-based Technology for Agricultural Improvement, NGB-1003; Ministry of Education and Science of Russian Federation project RFMEFI60414X0106 and project RFMEFI60414 X0107; Ministry of Education, Youth, and Sport of the Czech Republic award no. LO1204 (National Program of Sustainability I); Nisshin Flour Milling, Inc.; National Research Council of Canada Wheat Flagship program; Norwegian University of Life Sciences (NMBU) NFR project 199387, Expanding the technology base for Norwegian wheat breeding, Sequencing wheat chromosome 7B; National Science Foundation, United States, award (FAIN) 1339389, GPF-PG: Genome Structure and Diversity of Wheat and Its Wild Relatives, award DBI-0701916, and award IIP-1338897; Russian Science Foundation project 14-14-00161; Saskatchewan Ministry of Agriculture through the CTAG2 project; Saskatchewan Wheat Development Commission through the CTAG2 project; The Czech Science Foundation award no. 521/06/1723 (Construction of BAC library and physical mapping of the wheat chromosome 3D), award no. 521-08-1629 (Construction of BAC DNA libraries specific for chromosome 4AL and positional cloning of gene for adult plant resistance to powdery mildew in wheat), award no. P501/10/1740 (Physical map of the wheat chromosome 4AL and positional cloning of a gene for yield), award no. P501/12/2554 (Physical map of wheat chromosome arm 7DS and its use to clone a Russian wheat aphid-resistance gene), award no. P501/12/G090 (Evolution and function of complex plant genomes), award no. 14-07164S (Cloning and molecular characterization of wheat QPm-tut-4A gene conferring seedling and adult plant race-nonspecific powdery-mildew resistance), and award no. 13-08786S (Chromosome arm 3DS of bread wheat: Its sequence and function in allopolyploid genome); The Research Council of Norway (NFR) project 199387, Expanding the technology base for Norwegian wheat breeding; Sequencing wheat chromosome 7B; U.S. Department of Agriculture NIFA 2008-35300-04588, the University of Zurich; Western Grains Research Foundation through the CTAG2 project; Western Grains Research Foundation National Wheat Improvement Program; and the Winifred-Asbjornson Plant Science Endowment Fund. The research leading to these results has also received funding from the French Government managed by the ANR under the Investment for the Future program (BreedWheat project ANR-10-BTBR-03), from FranceAgriMer (2011-0971 and 2013-0544), French Funds to support Plant Breeding (FSOV), and INRA. Axiom genotyping was conducted on the genotyping platform GENTYANE at INRA Clermont-Ferrand (gentyane.clermont.inra.fr). This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the HPC cluster. Author contributions: See below, where authors are arranged by working group and contributions; leaders, co-leaders, and major contributors are listed alphabetically first and then other contributors follow alphabetically. Competing interests: The authors declare no competing interests. Bayer CropScience holds a patent application (WO2015000914A1) that covers the modulation of flowering time in monocots using the FLC gene. Data and materials availability: The IWGSC RefSeq v1.0 assembly and annotation data, physical maps for all chromosomes and chromosome arms, and all data related to this study are available in the IWGSC Data Repository hosted at URGI: https://wheat-urgi.versailles.inra.fr/Seq-Repository, Assembly and annotation data are also available at ENSEMBL-Plants: https://plants.ensembl.org/Triticum_aestivum/Info/Index. The BAC libraries for all chromosomes and chromosomes arms are available at the CNRGV-INRA: https://cnrgv.toulouse.inra.fr/en/Library/Wheat. Details on gene-family expansion and contraction in the genome of bread wheat cultivar Chinese Spring are provided in database S6 at http://dx.doi.org/10.5447/IPK/2018/5 (52). The raw sequencing data used for de novo whole-genome assembly are available from the Sequence Read Archive under accession number SRP114784. RNA-seq data are available at SRA under accession numbers PRJEB25639, PRJEB23056, PRJNA436817, PRJEB25640, SRP133837, and PRJEB25593. Hi-C sequence data are available under accession number PRJEB25248. ChIP-seq data are available under SRA study PRJNA420988 (SRP1262229). CS bisulfite sequencing data are available under project number SRP133674 (SRR6792673 to SRR6792689). Organellar DNA sequences were deposited at NCBI GenBank (MH051715 and MH051716). Further details on data accessibility are outlined in the supplementary materials and methods.
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