Sustainable Solutions for Food Security pp 91-109 | Cite as
Using Genomics to Adapt Crops to Climate Change
Abstract
Rising food demand from a growing global population, combined with a changing climate, endangers global food security. Thus, there is a need to breed new varieties and increase the efficiency and environmental resilience of crops. Past intensification of crop production has primarily been achieved using fertilisers, herbicides and insecticides as well as improved agronomic methods. However, these practices often rely on finite resources and lack sustainability, making them impractical to increase production in the long term. The ongoing revolution in genomics offers an unprecedented potential to aid crops in adapting to changing environments and increase yield, while also facilitating the diversification of crop production with minor and newly established crop species. Identifying the genomic basis of climate-related agronomic traits for introgression into crop germplasm is a major challenge, requiring the integration of sequencing technologies and breeding expertise. Here we review state of the art genomic tools and their application for accelerating crop improvement in the face of climate change.
Keywords
Breeding Climate change Crop improvement Food security Genomics Genome editingNotes
Acknowledgements
Armin Scheben was supported by an IPRS awarded by the Australian government. Yuxuan Yuan was supported by a SIRF funded by the China Scholarship Council and the University of Western Australia. David Edwards acknowledges support from the Australian Research Council LP140100537, LP130100061, LP130100925 and LP110100200.
References
- Abberton, M., Batley, J., Bentley, A., Bryant, J., Cai, H., Cockram, J., Costa de Oliveira, A., Cseke, L. J., Dempewolf, H., De Pace, C., Edwards, D., Gepts, P., Greenland, A., Hall, A. E., Henry, R., Hori, K., Howe, G. T., Hughes, S., Humphreys, M., Lightfoot, D., Marshall, A., Mayes, S., Nguyen, H. T., Ogbonnaya, F. C., Ortiz, R., Paterson, A. H., Tuberosa, R., Valliyodan, B., Varshney, R. K., & Yano, M. (2015). Global agricultural intensification during climate change: A role for genomics. Plant Biotechnology Journal, 14, 1095–1098.CrossRefGoogle Scholar
- Andrews, K. R., Good, J. M., Miller, M. R., Luikart, G., & Hohenlohe, P. A. (2016). Harnessing the power of RADseq for ecological and evolutionary genomics. Nature Reviews. Genetics, 17, 81–92.CrossRefGoogle Scholar
- Arruda, M. P., Brown, P., Brown-Guedira, G., Krill, A. M., Thurber, C., Merrill, K. R., Foresman, B. J., et al. (2016). Genome-wide association mapping of Fusarium head blight resistance in wheat using genotyping-by-sequencing. Plant Genome, 9.Google Scholar
- Bailey-Serres, J., Lee, S. C., & Brinton, E. (2012). Waterproofing crops: Effective flooding survival strategies. Plant Physiology, 160, 1698–1709.CrossRefGoogle Scholar
- Baltes, N. J., Hummel, A. W., Konecna, E., Cegan, R., Bruns, A. N., Bisaro, D. M., & Voytas, D. F. (2015). Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nature Plants, 1, 15145.CrossRefGoogle Scholar
- Batley, J., & Edwards, D. (2016). The application of genomics and bioinformatics to accelerate crop improvement in a changing climate. Current Opinion in Plant Biology, 30, 78–81.CrossRefGoogle Scholar
- Batzoglou, S., Jaffe, D. B., Stanley, K., Butler, J., Gnerre, S., Mauceli, E., Berger, B., et al. (2002). ARACHNE: A whole-genome shotgun assembler. Genome Research, 12, 177–189.CrossRefGoogle Scholar
- Bayer, P. E., Ruperao, P., Mason, A. S., Stiller, J., Chan, C.-K. K., Hayashi, S., Long, Y., et al. (2015). High-resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus. Theoretical and Applied Genetics, 128, 1039–1047.CrossRefGoogle Scholar
- Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N. J., & Nekrasov, V. (2015). Editing plant genomes with CRISPR/Cas9. Current Opinion in Biotechnology, 32, 76–84.CrossRefGoogle Scholar
- Berlin, K., Koren, S., Chin, C. S., Drake, J. P., Landolin, J. M., & Phillippy, A. M. (2015). Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nature Biotechnology, 33, 623–630.CrossRefGoogle Scholar
- Bortesi, L., & Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnology Advances, 33, 41–52.CrossRefGoogle Scholar
- Boyer, J. S., Byrne, P., Cassman, K. G., Cooper, M., Delmer, D., Greene, T., Gruis, F., et al. (2013). The US drought of 2012 in perspective: A call to action. Global Food Security-Agriculture Policy Economics and Environment, 2, 139–143.CrossRefGoogle Scholar
- Brooks, C., Nekrasov, V., Lippman, Z. B., & Van Eck, J. (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-Associated9 System. Plant Physiology, 166, 1292–1297.CrossRefGoogle Scholar
- Cao, L. Y., Zhuang, J. Y., Yuan, S. J., Zhan, X. D., Zheng, K. L., & Cheng, S. H. (2003). Hybrid rice resistant to bacterial leaf blight developed by marker assisted selection. Rice Science, 11, 68–70.Google Scholar
- Carneiro, M. O., Russ, C., Ross, M. G., Gabriel, S. B., Nusbaum, C., & DePristo, M. A. (2012). Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics, 13, 375.CrossRefGoogle Scholar
- Cermak, T., Baltes, N. J., Cegan, R., Zhang, Y., & Voytas, D. F. (2015). High-frequency, precise modification of the tomato genome. Genome Biology, 16, 232.CrossRefGoogle Scholar
- Chalhoub, B., Denoeud, F., Liu, S., Parkin, I. A. P., Tang, H., Wang, X., Chiquet, J., et al. (2014). Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950–953.CrossRefGoogle Scholar
- Chaney, L., Sharp, A. R., Evans, C. R., & Udall, J. A. (2016). Genome mapping in plant comparative genomics. Trends in Plant Science, 21, 770–780.CrossRefGoogle Scholar
- Chin, C. S., Alexander, D. H., Marks, P., Klammer, A. A., Drake, J., Heiner, C., Clum, A., et al. (2013). Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods, 10, 563–569.CrossRefGoogle Scholar
- Clarke, S. (2016). Is genotyping by sequencing a viable alternative to existing methods for genomic selection and GWAS? In Plant and Animal Genome XXIV Conference. San Diego, CA.Google Scholar
- Cooper, M., Gho, C., Leafgren, R., Tang, T., & Messina, C. (2014). Breeding drought-tolerant maize hybrids for the US corn-belt: Discovery to product. Journal of Experimental Botany, 65, 6191–6204.CrossRefGoogle Scholar
- Crossa, J., Beyene, Y., Kassa, S., Perez, P., Hickey, J. M., Chen, C., de los Campos, G., et al. (2013). Genomic prediction in maize breeding populations with genotyping-by-sequencing. G3 (Bethesda), 3, 1903–1926.CrossRefGoogle Scholar
- de Toledo Thomazella, D. P., Brail, Q., Dahlbeck, D., & Staskawicz, B. J. (2016). CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. bioRxiv, 064824.Google Scholar
- Davey, J. W., Hohenlohe, P. A., Etter, P. D., Boone, J. Q., Catchen, J. M., & Blaxter, M. L. (2011). Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews. Genetics, 12, 499–510.CrossRefGoogle Scholar
- Deschamps, S., Llaca, V., & May, G. D. (2012). Genotyping-by-sequencing in plants. Biology (Basel), 1, 460–483.Google Scholar
- Dhanapal, A. P., Ray, J. D., Singh, S. K., Hoyos-Villegas, V., Smith, J. R., Purcell, L. C., King, C. A., et al. (2015). Genome-wide association study (GWAS) of carbon isotope ratio (delta C-13) in diverse soybean [Glycine max (L.) Merr.] genotypes. Theoretical and Applied Genetics, 128, 73–91.CrossRefGoogle Scholar
- Duran, C., Eales, D., Marshall, D., Imelfort, M., Stiller, J., Berkman, P. J., Clark, T., McKenzie, M., Appleby, N., Batley, J., Basford, K., & Edwards, D. (2010). Future tools for association mapping in crop plants. Genome, 53, 1017–1023.CrossRefGoogle Scholar
- Edwards, D. (2016). The impact of genomics technology on adapting plants to climate change. In D. Edwards & J. Batley (Eds.), Plant genomics and climate change (pp. 173–178). New York, NY: Springer.CrossRefGoogle Scholar
- Edwards, D., & Batley, J. (2010). Plant genome sequencing: Applications for crop improvement. Plant Biotechnology Journal, 8, 2–9.CrossRefGoogle Scholar
- Eisenstein, M. (2015). Startups use short-read data to expand long-read sequencing market. Nature Biotechnology, 33, 433–435.CrossRefGoogle Scholar
- Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D.-L., Wang, Z., et al. (2014). Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 111, 4632–4637.CrossRefGoogle Scholar
- Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L., Reyon, D., Joung, J. K., & Sander, J. D. (2013). High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotechnology, 31, 822–826.CrossRefGoogle Scholar
- Fu, L. X., Cai, C. C., Cui, Y. N., Wu, J., Liang, J. L., Cheng, F., & Wang, X. W. (2016). Pooled mapping: An efficient method of calling variations for population samples with low-depth resequencing data. Molecular Breeding, 36, 48–48.CrossRefGoogle Scholar
- Gacek, K., Bayer, P. E., Bartkowiak-Broda, I., Szala, L., Bocianowski, J., Edwards, D., & Batley, J. (2017). Genome-wide association study of genetic control of seed fatty acid biosynthesis in Brassica napus. Frontiers in Plant Science, 7, 2062.CrossRefGoogle Scholar
- Gaffney, J., Schussler, J., Loffler, C., Cai, W. G., Paszkiewicz, S., Messina, C., Groeteke, J., et al. (2015). Industry-scale evaluation of maize hybrids selected for increased yield in drought-stress conditions of the US Corn Belt. Crop Science, 55, 1608–1618.CrossRefGoogle Scholar
- Gao, J. P., Wang, G. H., Ma, S. Y., Xie, X. D., Wu, X. W., Zhang, X. T., Wu, Y. Q., et al. (2015). CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Molecular Biology, 87, 99–110.CrossRefGoogle Scholar
- Gasiunas, G., Barrangou, R., Horvath, P., & Siksnys, V. (2012). Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 109, E2579–E2586.CrossRefGoogle Scholar
- Gnerre, S., Maccallum, I., Przybylski, D., Ribeiro, F. J., Burton, J. N., Walker, B. J., Sharpe, T., et al. (2011). High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proceedings of the National Academy of Sciences of the United States of America, 108, 1513–1518.CrossRefGoogle Scholar
- Godfray, H. C. J., Beddington, J. R., Crute, I. R., Haddad, L., Lawrence, D., Muir, J. F., Pretty, J., et al. (2010). Food security: The challenge of feeding 9 billion people. Science, 327, 812–818.CrossRefGoogle Scholar
- Golicz, A. A., Bayer, P. E., & Edwards, D. (2015). Skim-based genotyping by sequencing. Methods in Molecular Biology, 1245, 257–270.CrossRefGoogle Scholar
- Golicz, A. A., Batley, J., & Edwards, D. (2016a). Towards plant pangenomics. Plant Biotechnology Journal, 14, 1099–1105.CrossRefGoogle Scholar
- Golicz, A. A., Bayer, P. E., Barker, G. C., Edger, P. P., Kim, H., Martinez, P. A., Chan, C. K., et al. (2016b). The pangenome of an agronomically important crop plant Brassica oleracea. Nature Communications, 7, 13390.CrossRefGoogle Scholar
- Goodwin, S., Gurtowski, J., Ethe-Sayers, S., Deshpande, P., Schatz, M. C., & McCombie, W. R. (2015). Oxford Nanopore sequencing, hybrid error correction, and de novo assembly of a eukaryotic genome. Genome Research, 25, 1750–1756.CrossRefGoogle Scholar
- Goodwin, S., McPherson, J. D., & McCombie, W. R. (2016). Coming of age: Ten years of next-generation sequencing technologies. Nature Reviews. Genetics, 17, 333–351.CrossRefGoogle Scholar
- Gorjanc, G., Jenko, J., Hearne, S. J., & Hickey, J. M. (2016). Initiating maize pre-breeding programs using genomic selection to harness polygenic variation from landrace populations. BMC Genomics, 17, 30.CrossRefGoogle Scholar
- He, J., Zhao, X., Laroche, A., Lu, Z. X., Liu, H., & Li, Z. (2014). Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Frontiers in Plant Science, 5, 484.CrossRefGoogle Scholar
- Heffelfinger, C., Fragoso, C. A., Moreno, M. A., Overton, J. D., Mottinger, J. P., Zhao, H., Tohme, J., et al. (2014). Flexible and scalable genotyping-by-sequencing strategies for population studies. BMC Genomics, 15, 979–979.CrossRefGoogle Scholar
- Heffner, E. L., Lorenz, A. J., Jannink, J. L., & Sorrells, M. E. (2010). Plant breeding with genomic selection: Gain per unit time and cost. Crop Science, 50, 1681–1690.CrossRefGoogle Scholar
- Hirsch, C. N., Foerster, J. M., Johnson, J. M., Sekhon, R. S., Muttoni, G., Vaillancourt, B., Penagaricano, F., et al. (2014). Insights into the maize pan-genome and pan-transcriptome. Plant Cell, 26, 121–135.CrossRefGoogle Scholar
- Hwang, E. Y., Song, Q., Jia, G., Specht, J. E., Hyten, D. L., Costa, J., & Cregan, P. B. (2014). A genome-wide association study of seed protein and oil content in soybean. BMC Genomics, 15, 1.CrossRefGoogle Scholar
- Ingvordsen, C. H., Backes, G., Lyngkjaer, M. F., Peltonen-Sainio, P., Jahoor, A., Mikkelsen, T. N., & Jorgensen, R. B. (2015). Genome-wide association study of production and stability traits in barley cultivated under future climate scenarios. Molecular Breeding, 35, 84.CrossRefGoogle Scholar
- Ismail, A. M., Singh, U. S., Singh, S., Dar, M. H., & Mackill, D. J. (2013). The contribution of submergence-tolerant (Sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. Field Crops Research, 152, 83–93.CrossRefGoogle Scholar
- Jaganathan, D., Thudi, M., Kale, S., Azam, S., Roorkiwal, M., Gaur, P. M., Kishor, P. B. K., et al. (2015). Genotyping-by-sequencing based intra-specific genetic map refines a “QTL-hotspot” region for drought tolerance in chickpea. Molecular Genetics and Genomics, 290, 559–571.CrossRefGoogle Scholar
- Jain, M., Fiddes, I. T., Miga, K. H., Olsen, H. E., Paten, B., & Akeson, M. (2015). Improved data analysis for the MinION nanopore sequencer. Nature Methods, 12, 351–356.CrossRefGoogle Scholar
- Ji, X., Zhang, H. W., Zhang, Y., Wang, Y. P., & Gao, C. X. (2015). Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat. Plants, 1, 15144.CrossRefGoogle Scholar
- Jia, H. G., & Wang, N. (2014). Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One, 9, e93806.CrossRefGoogle Scholar
- Jiang, W. Z., Zhou, H. B., Bi, H. H., Fromm, M., Yang, B., & Weeks, D. P. (2013). Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research, 41, e188.CrossRefGoogle Scholar
- Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816–821.CrossRefGoogle Scholar
- Koren, S., Schatz, M. C., Walenz, B. P., Martin, J., Howard, J. T., Ganapathy, G., Wang, Z., et al. (2012). Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nature Biotechnology, 30, 693–700.CrossRefGoogle Scholar
- Kumar, V., Singh, A., Mithra, S. V., Krishnamurthy, S. L., Parida, S. K., Jain, S., Tiwari, K. K., et al. (2015). Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Research, 22, 133–145.CrossRefGoogle Scholar
- Lambert, B., Denolf, P., Engelen, S., Golds, T., Haesendonckx, B., Ruiter, R., Robbens, S., et al. (2015). Omics-directed reverse genetics enables the creation of new productivity traits for the vegetable oil crop canola. Procedia Environmental Sciences, 29, 77–78.CrossRefGoogle Scholar
- Larkan, N. J., Raman, H., Lydiate, D. J., Robinson, S. J., Yu, F., Barbulescu, D. M., Raman, R., et al. (2016). Multi-environment QTL studies suggest a role for cysteine-rich protein kinase genes in quantitative resistance to blackleg disease in Brassica napus. BMC Plant Biology, 16, 183.CrossRefGoogle Scholar
- Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., et al. (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20, 265–272.CrossRefGoogle Scholar
- Li, H., Peng, Z., Yang, X., Wang, W., Fu, J., Wang, J., Han, Y., et al. (2013). Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nature Genetics, 45, 43–50.CrossRefGoogle Scholar
- Li, Y. H., Zhou, G., Ma, J., Jiang, W., Jin, L. G., Zhang, Z., Guo, Y., et al. (2014). De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nature Biotechnology, 32, 1045–1052.CrossRefGoogle Scholar
- Li, R., Hsieh, C. L., Young, A., Zhang, Z., Ren, X., & Zhao, Z. (2015). Illumina synthetic long read sequencing allows recovery of missing sequences even in the “finished” C. elegans Genome. Scientific Reports, 5, 10814.CrossRefGoogle Scholar
- Li, J., Meng, X., Zong, Y., Chen, K., Zhang, H., Liu, J., Li, J., et al. (2016). Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat. Plants, 2, 16139.CrossRefGoogle Scholar
- Lin, K., Zhang, N., Severing, E. I., Nijveen, H., Cheng, F., Visser, R. G., Wang, X., et al. (2014). Beyond genomic variation--Comparison and functional annotation of three Brassica rapa genomes: A turnip, a rapid cycling and a Chinese cabbage. BMC Genomics, 15, 250.CrossRefGoogle Scholar
- Lin, Z., Cogan, N. O. I., Pembleton, L. W., Spangenberg, G. C., Forster, J. W., Hayes, B. J., & Daetwyler, H. D. (2016). Genetic gain and inbreeding from genomic selection in a simulated commercial breeding program for perennial ryegrass. Plant Genome, 9.CrossRefGoogle Scholar
- Liu, L., & Fan, X. D. (2014). CRISPR-Cas system: A powerful tool for genome engineering. Plant Molecular Biology, 85, 209–218.CrossRefGoogle Scholar
- Loman, N. J., Quick, J., & Simpson, J. T. (2015). A complete bacterial genome assembled de novo using only nanopore sequencing data. Nature Methods, 12, 733–735.CrossRefGoogle Scholar
- Lu, F., Romay, M. C., Glaubitz, J. C., Bradbury, P. J., Elshire, R. J., Wang, T., Li, Y., Li, Y., Semagn, K., Zhang, X., Hernandez, A. G., Mikel, M. A., Soifer, I., Barad, O., & Buckler, E. S. (2015). High-resolution genetic mapping of maize pan-genome sequence anchors. Nature Communications, 6, 6914.CrossRefGoogle Scholar
- Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.CrossRefGoogle Scholar
- Meuwissen, T. H. E., Hayes, B. J., & Goddard, M. E. (2001). Prediction of total genetic value using genome-wide dense marker maps. Genetics, 157, 1819–1829.Google Scholar
- Mikami, M., Toki, S., & Endo, M. (2016). Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant & Cell Physiology, 57, 1058–1068.CrossRefGoogle Scholar
- Miller, J. R., Koren, S., & Sutton, G. (2010). Assembly algorithms for next-generation sequencing data. Genomics, 95, 315–327.CrossRefGoogle Scholar
- Montenegro, J. D., Golicz, A. A., Bayer, P. E., Hurgobin, B., Lee, H., Chan, C. K., Visendi, P., Lai, K., Dolezel, J., Batley, J., & Edwards, D. (2017). The pangenome of hexaploid bread wheat. The Plant Journal, 90, 1007. https://doi.org/10.1111/tpj.13515.CrossRefGoogle Scholar
- Mueller, N. D., Gerber, J. S., Johnston, M., Ray, D. K., Ramankutty, N., & Foley, J. A. (2012). Closing yield gaps through nutrient and water management. Nature, 490, 254–257.CrossRefGoogle Scholar
- Munns, R., James, R. A., Xu, B., Athman, A., Conn, S. J., Jordans, C., Byrt, C. S., et al. (2012). Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology, 30, 360–364.CrossRefGoogle Scholar
- Myers, E. W., Sutton, G. G., Delcher, A. L., Dew, I. M., Fasulo, D. P., Flanigan, M. J., Kravitz, S. A., et al. (2000). A whole-genome assembly of Drosophila. Science, 287, 2196–2204.CrossRefGoogle Scholar
- Oerke, E. C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144, 31–43.CrossRefGoogle Scholar
- Paliwal, R., Roder, M. S., Kumar, U., Srivastava, J. P., & Joshi, A. K. (2012). QTL mapping of terminal heat tolerance in hexaploid wheat (T. aestivum L.). Theoretical and Applied Genetics, 125, 561–575.CrossRefGoogle Scholar
- Pattanayak, V., Lin, S., Guilinger, J. P., Ma, E. B., Doudna, J. A., & Liu, D. R. (2013). High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nature Biotechnology, 31, 839–843.CrossRefGoogle Scholar
- Pennisi, E. (2013). The CRISPR craze. Science, 341, 833–836.CrossRefGoogle Scholar
- Pevzner, P. A., & Tang, H. X. (2001). Fragment assembly with double-barreled data. Bioinformatics, 17, Suppl. 1, 225–Suppl. 1, 233.CrossRefGoogle Scholar
- Pevzner, P. A., Tang, H. X., & Waterman, M. S. (2001). An Eulerian path approach to DNA fragment assembly. Proceedings of the National Academy of Sciences of the United States of America, 98, 9748–9753.CrossRefGoogle Scholar
- Poland, J. A., & Rife, T. W. (2012). Genotyping-by-sequencing for plant breeding and genetics. Plant Genome, 5, 92–102.CrossRefGoogle Scholar
- Poland, J., Endelman, J., Dawson, J., Rutkoski, J., Wu, S. Y., Manes, Y., Dreisigacker, S., et al. (2012a). Genomic selection in wheat breeding using genotyping-by-sequencing. Plant Genome, 5, 103–113.CrossRefGoogle Scholar
- Poland, J. A., Brown, P. J., Sorrells, M. E., & Jannink, J. L. (2012b). Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One, 7, e32253.CrossRefGoogle Scholar
- Rabbi, I. Y., Hamblin, M. T., Kumar, P. L., Gedil, M. A., Ikpan, A. S., Jannink, J. L., & Kulakow, P. A. (2014). High-resolution mapping of resistance to cassava mosaic geminiviruses in cassava using genotyping-by-sequencing and its implications for breeding. Virus Research, 186, 87–96.CrossRefGoogle Scholar
- Ran, F. A., Hsu, P. D., Lin, C. Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., et al. (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380–1389.CrossRefGoogle Scholar
- Rhoads, A., & Au, K. F. (2015). PacBio sequencing and its applications. Genomics, Proteomics & Bioinformatics, 13, 278–289.CrossRefGoogle Scholar
- Ronald, P. C. (2014). Lab to farm: Applying research on plant genetics and genomics to crop improvement. PLoS Biology, 12, e1001878.CrossRefGoogle Scholar
- Rutkoski, J. E., Poland, J. A., Singh, R. P., Huerta-Espino, J., Bhavani, S., Barbier, H., Rouse, M. N., et al. (2014). Genomic selection for quantitative adult plant stem rust resistance in wheat. Plant Genome, 7, 1–10.CrossRefGoogle Scholar
- Saxena, R. K., Edwards, D., & Varshney, R. K. (2014). Structural variations in plant genomes. Briefings in Functional Genomics, 13, 296–307.CrossRefGoogle Scholar
- Schatz, M. C., Maron, L. G., Stein, J. C., Hernandez Wences, A., Gurtowski, J., Biggers, E., Lee, H., et al. (2014). Whole genome de novo assemblies of three divergent strains of rice, Oryza sativa, document novel gene space of aus and indica. Genome Biology, 15, 506.Google Scholar
- Scheben, A., & Edwards, D. (2017). Genome editors take on crops. Science, 355, 1122–1123.CrossRefGoogle Scholar
- Scheben, A., Yuan, Y., & Edwards, D. (2016). Advances in genomics for adapting crops to climate change. Current Plant Biology, 6, 2–10.CrossRefGoogle Scholar
- Scheben, A., Batley, J., & Edwards, D. (2017). Genotyping-by-sequencing approaches to characterize crop genomes: Choosing the right tool for the right application. Plant Biotechnology Journal, 15, 149–161.CrossRefGoogle Scholar
- Septiningsih, E. M., Pamplona, A. M., Sanchez, D. L., Neeraja, C. N., Vergara, G. V., Heuer, S., Ismail, A. M., et al. (2009). Development of submergence-tolerant rice cultivars: The Sub1 locus and beyond. Annals of Botany, 103, 151–160.CrossRefGoogle Scholar
- Shen, B., Zhang, W. S., Zhang, J., Zhou, J. K., Wang, J. Y., Chen, L., Wang, L., et al. (2014). Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nature Methods, 11, 399–402.CrossRefGoogle Scholar
- Shi, J., Gao, H., Wang, H., Lafitte, H. R., Archibald, R. L., Yang, M., Hakimi, S. M., et al. (2017). ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnology Journal, 15, 207.CrossRefGoogle Scholar
- Simpson, J. T., Wong, K., Jackman, S. D., Schein, J. E., Jones, S. J., & Birol, I. (2009). ABySS: A parallel assembler for short read sequence data. Genome Research, 19, 1117–1123.CrossRefGoogle Scholar
- Skinner, J., Szucs, P., von Zitzewitz, J., Marquez-Cedillo, L., Filichkin, T., Stockinger, E. J., Thomashow, M. F., et al. (2006). Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theoretical and Applied Genetics, 112, 832–842.CrossRefGoogle Scholar
- Soyk, S., Muller, N. A., Park, S. J., Schmalenbach, I., Jiang, K., Hayama, R., Zhang, L., et al. (2017). Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nature Genetics, 49, 162–168.CrossRefGoogle Scholar
- Spindel, J. E., & McCouch, S. R. (2016). When more is better: How data sharing would accelerate genomic selection of crop plants. The New Phytologist, 212, 814–826.CrossRefGoogle Scholar
- Stankova, H., Hastie, A. R., Chan, S., Vrana, J., Tulpova, Z., Kubalakova, M., Visendi, P., et al. (2016). BioNano genome mapping of individual chromosomes supports physical mapping and sequence assembly in complex plant genomes. Plant Biotechnology Journal, 14, 1523–1531.CrossRefGoogle Scholar
- Sun, Y., Zhang, X., Wu, C., He, Y., Ma, Y., Hou, H., Guo, X., et al. (2016). Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Molecular Plant, 9, 628–631.CrossRefGoogle Scholar
- Svitashev, S., Young, J. K., Schwartz, C., Gao, H. R., Falco, S. C., & Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiology, 169, 931–945.CrossRefGoogle Scholar
- Svitashev, S., Schwartz, C., Lenderts, B., Young, J. K., & Mark Cigan, A. (2016). Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nature Communications, 7, 13274.CrossRefGoogle Scholar
- Szalay, T., & Golovchenko, J. A. (2015). De novo sequencing and variant calling with nanopores using PoreSeq. Nature Biotechnology, 33, 1087–1091.CrossRefGoogle Scholar
- Tester, M., & Langridge, P. (2010). Breeding technologies to increase crop production in a changing world. Science, 327, 818–822.CrossRefGoogle Scholar
- Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., et al. (2005). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial “pan-genome”. Proceedings of the National Academy of Sciences of the United States of America, 102, 13950–13955.CrossRefGoogle Scholar
- Tollenaere, R., Hayward, A., Dalton-Morgan, J., Campbell, E., Lee, J. R. M., Lorenc, M. T., Manoli, S., et al. (2012). Identification and characterization of candidate Rlm4 blackleg resistance genes in Brassica napus using next-generation sequencing. Plant Biotechnology Journal, 10, 709–715.CrossRefGoogle Scholar
- Trethowan, R. M., Reynolds, M., Sayre, K., & Ortiz-Monasterio, I. (2005). Adapting wheat cultivars to resource conserving farming practices and human nutritional needs. The Annals of Applied Biology, 146, 405–413.CrossRefGoogle Scholar
- United Nations. (2015). World population prospects: The 2015 revision. New York, NY: Population Division of the Department of Economic and Social Affairs.CrossRefGoogle Scholar
- Valluru, R., Reynolds, M. P., Davies, W. J., & Sukumaran, S. (2017). Phenotypic and genome-wide association analysis of spike ethylene in diverse wheat genotypes under heat stress. The New Phytologist, 214, 271.CrossRefGoogle Scholar
- Waltz, E. (2016). CRISPR-edited crops free to enter market, skip regulation. Nature Biotechnology, 34, 582.CrossRefGoogle Scholar
- Wang, W., Vinocur, B., & Altman, A. (2003). Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta, 218, 1–14.CrossRefGoogle Scholar
- Wang, Y. P., Cheng, X., Shan, Q. W., Zhang, Y., Liu, J. X., Gao, C. X., & Qiu, J. L. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology, 32, 947–951.CrossRefGoogle Scholar
- Wang, S. H., Zhang, S. B., Wang, W. X., Xiong, X. Y., Meng, F. R., & Cui, X. (2015). Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Reports, 34, 1473–1476.CrossRefGoogle Scholar
- Wang, F. J., Wang, C. L., Liu, P. Q., Lei, C. L., Hao, W., Gao, Y., Liu, Y. G., et al. (2016). Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One, 11, e0154027.CrossRefGoogle Scholar
- Winfield, M. O., Allen, A. M., Burridge, A. J., Barker, G. L. A., Benbow, H. R., Wilkinson, P. A., Coghill, J., et al. (2016). High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnology Journal, 14, 1195–1206.CrossRefGoogle Scholar
- Xu, Y. B., & Crouch, J. H. (2008). Marker-assisted selection in plant breeding: From publications to practice. Crop Science, 48, 391–407.CrossRefGoogle Scholar
- Yang, J., Liu, D., Wang, X., Ji, C., Cheng, F., Liu, B., Hu, Z., et al. (2016). The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nature Genetics, 48, 1225–1232.CrossRefGoogle Scholar
- Yuan, Y., Bayer, P. E., Batley, J., & Edwards, D. (2017). Improvements in genomic technologies: Application to crop genomics. Trends in Biotechnology, 35, 547–558.CrossRefGoogle Scholar
- Zerbino, D. R., & Birney, E. (2008). Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research, 18, 821–829.CrossRefGoogle Scholar
- Zhang, H., Zhang, J., Wei, P., Zhang, B., Gou, F., Feng, Z., Mao, Y., et al. (2014). The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnology Journal, 12, 797–807.CrossRefGoogle Scholar
- Zhang, X., Perez-Rodriguez, P., Semagn, K., Beyene, Y., Babu, R., Lopez-Cruz, M. A., Vicente, F. S., et al. (2015). Genomic prediction in biparental tropical maize populations in water-stressed and well-watered environments using low-density and GBS SNPs. Heredity, 114, 291–299.CrossRefGoogle Scholar
- Zhang, J., Ratanasirintrawoot, S., Chandrasekaran, S., Wu, Z., Ficarro, S. B., Yu, C., Ross, C. A., et al. (2016). LIN28 regulates stem cell metabolism and conversion to primed pluripotency. Cell Stem Cell, 19, 66–80.CrossRefGoogle Scholar
- Zhao, K., Tung, C. W., Eizenga, G. C., Wright, M. H., Ali, M. L., Price, A. H., Norton, G. J., et al. (2011). Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Communications, 2, 467.CrossRefGoogle Scholar
- Zhou, S., Bechner, M. C., Place, M., Churas, C. P., Pape, L., Leong, S. A., Runnheim, R., et al. (2007). Validation of rice genome sequence by optical mapping. BMC Genomics, 8, 278.CrossRefGoogle Scholar
- Zhou, S., Wei, F., Nguyen, J., Bechner, M., Potamousis, K., Goldstein, S., Pape, L., et al. (2009). A single molecule scaffold for the maize genome. PLoS Genetics, 5, e1000711.CrossRefGoogle Scholar
- Zimin, A. V., Marcais, G., Puiu, D., Roberts, M., Salzberg, S. L., & Yorke, J. A. (2013). The MaSuRCA genome assembler. Bioinformatics, 29, 2669–2677.CrossRefGoogle Scholar