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Rapid gene cloning in cereals

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Abstract

Key message

The large and complex genomes of many cereals hindered cloning efforts in the past. Advances in genomics now allow the rapid cloning of genes from humanity’s most valuable crops.

Abstract

The past two decades were characterized by a genomics revolution that entailed profound changes to crop research, plant breeding, and agriculture. Today, high-quality reference sequences are available for all major cereal crop species. Large resequencing and pan-genome projects start to reveal a more comprehensive picture of the genetic makeup and the diversity among domesticated cereals and their wild relatives. These technological advancements will have a dramatic effect on dissecting genotype–phenotype associations and on gene cloning. In this review, we will highlight the status of the genomic resources available for various cereal crops and we will discuss their implications for gene cloning. A particular focus will be given to the cereal species barley and wheat, which are characterized by very large and complex genomes that have been inaccessible to rapid gene cloning until recently. With the advancements in genomics and the development of several rapid gene-cloning methods, it has now become feasible to tackle the cloning of most agriculturally important genes, even in wheat and barley.

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References

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178

    Article  CAS  PubMed  Google Scholar 

  • An G, Lee S, Kim SH, Kim SR (2005) Molecular genetics using T-DNA in rice. Plant Cell Physiol 46:14–22

    Article  CAS  PubMed  Google Scholar 

  • Arora S, Steuernagel B, Chandramohan S, Long Y, Matny O, Johnson R, Enk J, Periyannan S, Hatta MAM, Athiyannan N, Cheema J, Yu G, Kangara N, Ghosh S, Szabo LJ, Poland J, Bariana H, Jones JDG, Bentley AR, Ayliffe M, Olson E, Xu SS, Steffenson BJ, Lagudah E, Wulff BBH (2018) Resistance gene discovery and cloning by sequence capture and association genetics. bioRxiv. https://doi.org/10.1101/248146

  • Bazakos C, Hanemian M, Trontin C, Jiménez-Gómez JM, Loudet O (2017) New strategies and tools in quantitative genetics: how to go from the phenotype to the genotype. Annu Rev Plant Biol 68:435–455

    Article  CAS  PubMed  Google Scholar 

  • Bevan MW, Uauy C, Wulff BB, Zhou J, Krasileva K, Clark MD (2017) Genomic innovation for crop improvement. Nature 543:346–354

    Article  CAS  PubMed  Google Scholar 

  • Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Villeda HS, Sofia da Silva H, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718

    Article  CAS  PubMed  Google Scholar 

  • Chia JM, Song C, Bradbury PJ, Costich D, de Leon N, Doebley J, Elshire RJ, Gaut B, Geller L, Glaubitz JC, Gore M, Guill KE, Holland J, Hufford MB, Lai J, Li M, Liu X, Lu Y, McCombie R, Nelson R, Poland J, Prasanna BM, Pyhäjärvi T, Rong T, Sekhon RS, Sun Q, Tenaillon MI, Tian F, Wang J, Xu X, Zhang Z, Kaeppler SM, Ross-Ibarra J, McMullen MD, Buckler ES, Zhang G, Xu Y, Ware D (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44:803–807

    Article  CAS  PubMed  Google Scholar 

  • Clark RT, Famoso AN, Zhao K, Shaff JE, Craft EJ, Bustamante CD, McCouch SR, Aneshansley DJ, Kochian LV (2013) High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development. Plant Cell Environ 36:454–466

    Article  CAS  PubMed  Google Scholar 

  • Crain JL, Wei Y, Barker J, Thompson SM, Alderman PD, Reynolds M, Zhang N, Poland J (2016) Development and deployment of a portable field phenotyping platform. Crop Sci 56:965–975

    Article  Google Scholar 

  • Czedik-Eysenberg A, Seitner S, Güldener U, Koemeda S, Jez J, Colombini M, Djamei A (2018) The ‘PhenoBox’, a flexible, automated, open-source plant phenotyping solution. New Phytol 219:808–823

    Article  PubMed  PubMed Central  Google Scholar 

  • Desta ZA, Ortiz R (2014) Genomic selection: genome-wide prediction in plant improvement. Trends Plant Sci 19:592–601

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff NV, Furtek DB, Nelson OE (1984) Cloning of the bronze locus in maize by a simple and generalizable procedure using the transposable controlling element Activator (Ac). Proc Natl Acad Sci USA 81:3825–3829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fekih R, Takagi H, Tamiru M, Abe A, Natsume S, Yaegashi H, Sharma S, Sharma S, Kanzaki H, Matsumura H, Saitoh H, Mitsuoka C, Utsushi H, Uemura A, Kanzaki E, Kosugi S, Yoshida K, Cano L, Kamoun S, Terauchi R (2013) MutMap +: genetic mapping and mutant identification without crossing in rice. PLoS ONE 8:e68529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  CAS  PubMed  Google Scholar 

  • Gottwald S, Bauer P, Komatsuda T, Lundqvist U, Stein N (2009) TILLING in the two-rowed barley cultivar ‘Barke’ reveals preferred sites of functional diversity in the gene HvHox1. BMC Res Notes 2:258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haghighattalab A, González Pérez L, Mondal S, Singh D, Schinstock D, Rutkoski J, Ortiz-Monasterio I, Singh RP, Goodin D, Poland J (2016) Application of unmanned aerial systems for high throughput phenotyping of large wheat breeding nurseries. Plant Methods 12:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hake S, Vollbrecht E, Freeling M (1989) Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J 8:15–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann A, Czauderna T, Hoffmann R, Stein N, Schreiber F (2011) HTPheno: an image analysis pipeline for high-throughput plant phenotyping. BMC Bioinform 12:148

    Article  Google Scholar 

  • Henry IM, Nagalakshmi U, Lieberman MC, Ngo KJ, Krasileva KV, Vasquez-Gross H, Akhunova A, Akhunov E, Dubcovsky J, Tai TH, Comai L (2014) Efficient genome-wide detection and cataloging of EMS-induced mutations using exome capture and next-generation sequencing. Plant Cell 26:1382–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrera-Foessel SA, Singh RP, Huerta-Espino J, Rosewarne GM, Periyannan SK, Viccars L, Calvo-Salazar V, Lan C, Lagudah ES (2012) Lr68: a new gene conferring slow rusting resistance to leaf rust in wheat. Theor Appl Genet 124:1475–1486

    Article  CAS  PubMed  Google Scholar 

  • Hickey JM, Chiurugwi T, Mackay I, Powell W, Implementing Genomic Selection in CGIAR Breeding Programs Workshop Participants (2017) Genomic prediction unifies animal and plant breeding programs to form platforms for biological discovery. Nat Genet 49:1297–1303

    Article  CAS  PubMed  Google Scholar 

  • Hussain W, Baenziger PS, Belamkar V, Guttieri MJ, Venegas JP, Easterly A, Sallam A, Poland J (2017) Genotyping-by-sequencing derived high-density linkage map and its application to QTL mapping of flag leaf traits in bread wheat. Sci Rep 7:16394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Jiao Y, Burke JJ, Chopra R, Burow G, Chen J, Wang B, Hayes C, Emendack Y, Ware D, Xin Z (2016) A sorghum mutant resource as an efficient platform for gene discovery in grasses. Plant Cell 28:1551–1562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan KW, Wang S, Lun Y, Gardiner L-J, MacLachlan R, Hucl P, Wiebe K, Wong D, Forrest KL, Consortium I, Sharpe AG, Sidebottom CHD, Hall N, Toomajian C, Close T, Dubcovsky J, Akhunova A, Talbert L, Bansal UK, Bariana HS, Hayden MJ, Pozniak C, Jeddeloh JA, Hall A, Akhunov E (2015) A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes. Genome Biol 16:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Jupe F, Witek K, Verweij W, Sliwka J, Pritchard L, Etherington GJ, Maclean D, Cock PJ, Leggett RM, Bryan GJ, Cardle L, Hein I, Jones JD (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J 76:530–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller B, Wicker T, Krattinger SG (2018) Advances in wheat and pathogen genomics: implications for disease control. Annu Rev Phytopathol 56:67–87

    Article  CAS  PubMed  Google Scholar 

  • Khush GS, Mackill DJ, Sidhu GS (1989) Breeding rice for resistance to bacterial blight. In: Proceedings of the international workshop on bacterial blight of rice. International Rice Research Institute, Manila

  • Khush GS, Bacalangco E, Ogawa T (1991) A new gene for resistance to bacterial blight from O. longistaminata. Rice Genet Newslett 7:121–122

    Google Scholar 

  • Kourelis J, van der Hoorn RAL (2018) Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, Simmonds J, Ramirez-Gonzalez RH, Wang X, Borrill P, Fosker C, Ayling S, Phillips AL, Uauy C, Dubcovsky J (2017) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114:E913–E921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krattinger SG, Keller B (2016) Molecular genetics and evolution of disease resistance in cereals. New Phytol 212:320–332

    Article  CAS  PubMed  Google Scholar 

  • Krattinger S, Wicker T, Keller B (2009) Map-based cloning of genes in Triticeae (wheat and barley). In: Muehlbauer G, Feuillet C (eds) Genetics and genomics of the Triticeae. Springer, New York, pp 337–357

    Chapter  Google Scholar 

  • Li G, Jain R, Chern M, Pham NT, Martin JA, Wei T, Schackwitz WS, Lipzen AM, Duong PQ, Jones KC, Jiang L, Ruan D, Bauer D, Peng Y, Barry KW, Schmutz J, Ronald PC (2017a) The sequences of 1504 mutants in the model rice variety Kitaake facilitate rapid functional genomic studies. Plant Cell 29:1218–1231

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, Zhou X, Zhu X, Chen Z, Wang J, Zhao W, Ma B, Qin P, Chen W, Wang Y, Liu J, Wang W, Wu X, Li P, Wang J, Zhu L, Li S, Chen X (2017b) A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170(114–126):e115

    Google Scholar 

  • Liu S, Yeh CT, Tang HM, Nettleton D, Schnable PS (2012) Gene mapping via bulked segregant RNA-Seq (BSR-Seq). PLoS ONE 7:e36406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mago R, Tabe L, Vautrin S, Šimková H, Kubaláková M, Upadhyaya N, Berges H, Kong X, Breen J, Doležel J, Appels R, Ellis JG, Spielmeyer W (2014) Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus. BMC Plant Biol 14:379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Simkova H, Stankova H, Vrana J, Chan S, Munoz-Amatriain M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Dolezel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    Article  CAS  PubMed  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeting induced locallesions in genomes (TILLING) for plant functional genomics. Plant Physiol 123:439–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36:344–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McIntosh R, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Somers D, Appels R, Devos K (2008) Catalogue of gene symbols for wheat. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds) Proceedings of the 11th international wheat genetics symposium. Sydney University Press, Sydney

  • Michael TP, Jupe F, Bemm F, Motley ST, Sandoval JP, Lanz C, Loudet O, Weigel D, Ecker JR (2018) High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat Commun 9:541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How many species are there on earth and in the ocean? PLoS Biol 9:e1001127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson GC, Rosegrant MW, Palazzo A, Gray I, Ingersoll C, Robertson R, Tokgoz S, Zhu T, Sulser TB, Ringler C, Msangi S, You L (2010) Food security, farming, and climate change to 2050: scenarios, results, policy options. International Food Policy Research Institute, Washington, D.C.

    Google Scholar 

  • Ni J, Pujar A, Youens-Clark K, Yap I, Jaiswal P, Tecle I, Tung CW, Ren L, Spooner W, Wei X, Avraham S, Ware D, Stein L, McCouch S (2009) Gramene QTL database: development, content and applications. Database 2009. https://doi.org/10.1093/database/bap005

  • Niu Z, Jiang A, Abu Hammad W, Oladzadabbasabadi A, Xu SS, Mergoum M, Elias EM (2014) Review of doubled haploid production in durum and common wheat through wheat × maize hybridization. Plant Breeding 133:313–320

    Article  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Poland J, Rutkoski J (2016) Advances and challenges in genomic selection for disease resistance. Annu Rev Phytopathol 54:79–98

    Article  CAS  PubMed  Google Scholar 

  • Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216

    Article  CAS  PubMed  Google Scholar 

  • Putnam NH, O’Connell BL, Stites JC, Rice BJ, Blanchette M, Calef R, Troll CJ, Fields A, Hartley PD, Sugnet CW, Haussler D, Rokhsar DS, Green RE (2016) Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res 26:342–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasheed A, Hao Y, Xia X, Khan A, Xu Y, Varshney RK, He Z (2017) Crop breeding chips and genotyping platforms: progress, challenges, and oerspectives. Mol Plant 10:1047–1064

    Article  CAS  PubMed  Google Scholar 

  • Rawat N, Sehgal SK, Joshi A, Rothe N, Wilson DL, McGraw N, Vadlani PV, Li W, Gill BS (2012) A diploid wheat TILLING resource for wheat functional genomics. BMC Plant Biol 12:205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoades MM (1952) The effect of the Bronze locus on anthocyanin formation in maize. Am Nat 86:105–108

    Article  CAS  Google Scholar 

  • Ronald PC, Albano B, Tabien R, Abenes L, Wu KS, McCouch S, Tanksley SD (1992) Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol Gen Genet 236:113–120

    CAS  PubMed  Google Scholar 

  • Saballos A, Sattler SE, Sanchez E, Foster TP, Xin Z, Kang C, Pedersen JF, Vermerris W (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). Plant J 70:818–830

    Article  CAS  PubMed  Google Scholar 

  • Saintenac C, Lee WS, Cambon F, Rudd JJ, King RC, Marande W, Powers SJ, Bergès H, Phillips AL, Uauy C, Hammond-Kosack KE, Langin T, Kanyuka K (2018) Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat Genet 50:368–374

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, Doležel J, Keller B, Wulff BB (2016) Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17:221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanger F, Air GM, Barrell BG, Brown NL, Coulson AR, Fiddes JC, Hutchison CA, Slocombe PM, Smith M (1977) Nucleotide sequence of bacteriophage φX174 DNA. Nature 265:687–695

    Article  CAS  PubMed  Google Scholar 

  • Sattler SE, Funnell-Harris DL, Pedersen JF (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci 178:229–238

    Article  CAS  Google Scholar 

  • Sattler SE, Saballos A, Xin Z, Funnell-Harris DL, Vermerris W, Pedersen JF (2014) Characterization of novel sorghum brown midrib mutants from an EMS-mutagenized population. G3 (Bethesda) 4:2115–2124

    Article  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Schneeberger K (2014) Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet 15:662–676

    Article  CAS  PubMed  Google Scholar 

  • Schön CC, Utz HF, Groh S, Truberg B, Openshaw S, Melchinger AE (2004) Quantitative trait locus mapping based on resampling in a vast maize testcross experiment and its relevance to quantitative genetics for complex traits. Genetics 167:485–498

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva P, Calvo-Salazar V, Condón F, Quincke M, Pritsch C, Gutiérrez L, Castro A, Herrera-Foessel S, von Zitzewitz J, Germán S (2015) Effects and interactions of genes Lr34, Lr68 and Sr2 on wheat leaf rust adult plant resistance in Uruguay. Euphytica 204:599–608

    Article  CAS  Google Scholar 

  • Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D (2005) A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23(1):75–81

    Article  CAS  PubMed  Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  CAS  PubMed  Google Scholar 

  • Stadler LJ (1928) Mutations in barley induced by X-rays and radium. Science 68:186–187

    Article  CAS  PubMed  Google Scholar 

  • Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, Chougule K, Gao D, Iwata A, Goicoechea JL, Wei S, Wang J, Liao Y, Wang M, Jacquemin J, Becker C, Kudrna D, Zhang J, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu CC, Kao SM, Zeng JW, Wei FJ, Zhao Q, Feng Q, El Baidouri M, Carpentier MC, Lasserre E, Cooke R, Rosa Farias DD, da Maia LC, Dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan C, Weigel D, Jena KK, Wicker T, Chen M, Han B, Henry R, Hsing YC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long M, Ware D, Wing RA (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50:285–296

    Article  CAS  PubMed  Google Scholar 

  • Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JD, Lagudah ES, Wulff BB (2016) Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34:652–655

    Article  CAS  PubMed  Google Scholar 

  • Talamè V, Bovina R, Sanguineti MC, Tuberosa R, Lundqvist U, Salvi S (2008) TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnol J 6:477–485

    Article  CAS  PubMed  Google Scholar 

  • The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  CAS  Google Scholar 

  • The International Wheat Genome Sequencing Consortium (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

    Article  CAS  Google Scholar 

  • Thind AK, Wicker T, Šimková H, Fossati D, Moullet O, Brabant C, Vrána J, Doležel J, Krattinger SG (2017) Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. Nat Biotechnol 35:793–796

    Article  CAS  PubMed  Google Scholar 

  • Thomas CA Jr (1971) The genetic organization of chromosomes. Annu Rev Genet 5:237–256

    Article  CAS  PubMed  Google Scholar 

  • Till BJ, Reynolds SH, Weil C, Springer N, Burtner C, Young K, Bowers E, Codomo CA, Enns LC, Odden AR, Greene EA, Comai L, Henikoff S (2004) Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol 4:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Till BJ, Cooper J, Tai TH, Colowit P, Greene EA, Henikoff S, Comai L (2007) Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol 7:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9:115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uauy C, Wulff BBH, Dubcovsky J (2017) Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat. Annu Rev Genet 51:435–454

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Shi C, Thudi M, Mariac C, Wallace J, Qi P, Zhang H, Zhao Y, Wang X, Rathore A, Srivastava RK, Chitikineni A, Fan G, Bajaj P, Punnuri S, Gupta SK, Wang H, Jiang Y, Couderc M, Katta M, Paudel DR, Mungra KD, Chen W, Harris-Shultz KR, Garg V, Desai N, Doddamani D, Kane NA, Conner JA, Ghatak A, Chaturvedi P, Subramaniam S, Yadav OP, Berthouly-Salazar C, Hamidou F, Wang J, Liang X, Clotault J, Upadhyaya HD, Cubry P, Rhoné B, Gueye MC, Sunkar R, Dupuy C, Sparvoli F, Cheng S, Mahala RS, Singh B, Yadav RS, Lyons E, Datta SK, Hash CT, Devos KM, Buckler E, Bennetzen JL, Paterson AH, Ozias-Akins P, Grando S, Wang J, Mohapatra T, Weckwerth W, Reif JC, Liu X, Vigouroux Y, Xu X (2017) Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments. Nat Biotechnol 35:969–976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Virlet N, Sabermanesh K, Sadeghi-Tehran P, Hawkesford MJ (2017) Field Scanalyzer: an automated robotic field phenotyping platform for detailed crop monitoring. Funct Plant Biol 44:143–153

    Article  Google Scholar 

  • Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, Conrad LJ, Kikuchi K, Kubinec TA, Hall BD, Weeks R, Unger-Wallace E, Muszynski M, Brendel VP, Brutnell TP (2010) Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22:1667–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vrána J, Kubaláková M, Simková H, Číhalíkovái J, Lysák MA, Dolezel J (2000) Flow sorting of mitotic chromosomes in common wheat (Triticum aestivum L.). Genetics 156:2033–2041

    PubMed  PubMed Central  Google Scholar 

  • Wang GL, Holsten TE, Song WY, Wang HP, Ronald PC (1995) Construction of a rice bacterial artificial chromosome library and identification of clones linked to the Xa-21 disease resistance locus. Plant J 7:525–533

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Dudareva N, Morgan JA, Chapple C (2015) Genetic manipulation of lignocellulosic biomass for bioenergy. Curr Opin Chem Biol 29:32–39

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu J, Sun C, Fu B, Zhang H, Gao Y, Zhao X, Shen F, Cui X, Yu H, Li Z, Chen M, Detras J, Zhou Y, Zhang X, Zhao Y, Kudrna D, Wang C, Li R, Jia B, Lu J, He X, Dong Z, Xu J, Li Y, Wang M, Shi J, Li J, Zhang D, Lee S, Hu W, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu Y, Yue Z, Naredo MEB, Talag J, Wang X, Li J, Fang X, Yin Y, Glaszmann JC, Zhang J, Li J, Hamilton RS, Wing RA, Ruan J, Zhang G, Wei C, Alexandrov N, McNally KL, Li Z, Leung H (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:43–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, Rey MD, Asyraf Md Hatta M, Hinchliffe A, Steed A, Reynolds D, Adamski NM, Breakspear A, Korolev A, Rayner T, Dixon LE, Riaz A, Martin W, Ryan M, Edwards D, Batley J, Raman H, Carter J, Rogers C, Domoney C, Moore G, Harwood W, Nicholson P, Dieters MJ, DeLacy IH, Zhou J, Uauy C, Boden SA, Park RF, Wulff BBH, Hickey LT (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:23–29

    Article  PubMed  Google Scholar 

  • Witek K, Jupe F, Witek AI, Baker D, Clark MD, Jones JDG (2016) Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nat Biotechnol 34:656–660

    Article  CAS  PubMed  Google Scholar 

  • Xin Z, Wang ML, Barkley NA, Burow G, Franks C, Pederson G, Burke J (2008) Applying genotyping (TILLING) and phenotyping analyses to elucidate gene function in a chemically induced sorghum mutant population. BMC Plant Biol 8:103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Chen LL, Xing F, Kudrna DA, Yao W, Copetti D, Mu T, Li W, Song JM, Xie W, Lee S, Talag J, Shao L, An Y, Zhang CL, Ouyang Y, Sun S, Jiao WB, Lv F, Du B, Luo M, Maldonado CE, Goicoechea JL, Xiong L, Wu C, Xing Y, Zhou DX, Yu S, Zhao Y, Wang G, Yu Y, Luo Y, Zhou ZW, Hurtado BE, Danowitz A, Wing RA, Zhang Q (2016) Extensive sequence divergence between the reference genomes of two elite indica rice varieties Zhenshan 97 and Minghui 63. Proc Natl Acad Sci USA 113:E5163–E5171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, Zhan Q, Lu Y, Zhang L, Huang T, Wang Y, Fan D, Zhao Y, Wang Z, Zhou C, Chen J, Zhu C, Li W, Weng Q, Xu Q, Wang ZX, Wei X, Han B, Huang X (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50:278–284

    Article  CAS  PubMed  Google Scholar 

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  1. Biological and Environmental Science and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900, Saudi Arabia

    Jan Bettgenhaeuser & Simon G. Krattinger

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Bettgenhaeuser, J., Krattinger, S.G. Rapid gene cloning in cereals. Theor Appl Genet 132, 699–711 (2019). https://doi.org/10.1007/s00122-018-3210-7

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