Molecular Breeding

, 37:14 | Cite as

TILLING by Sequencing (TbyS) for targeted genome mutagenesis in crops

  • Anishkumar P. K. Kumar
  • Peter C. McKeown
  • Adnane Boualem
  • Peter Ryder
  • Galina Brychkova
  • Abdelhafid Bendahmane
  • Abhimanyu Sarkar
  • Manash Chatterjee
  • Charles Spillane
Review

Abstract

TILLING (Targeting Induced Local Lesions in Genomes) by Sequencing (TbyS) refers to the application of high-throughput sequencing technologies to mutagenised TILLING populations as a tool for functional genomics. TbyS can be used to identify and characterise induced variation in genes (controlling traits of interest) within large mutant populations, and is a powerful approach for the study and harnessing of genetic variation in crop breeding programmes. The extension of existing TILLING platforms by TbyS will accelerate crop functional genomics studies, in concert with the rapid increase in genome editing capabilities and the number and quality of sequenced crop plant genomes. In this mini-review, we provide an overview of the growth of TbyS and its potential applications to crop molecular breeding.

Keywords

TILLING by Sequencing Induced variation TbyS Mutagenesis CRISPR/Cas9 Genome editing 

References

  1. Abbott A (2015) Europe’s genetically edited plants stuck in legal limbo. Nature 528:319–320CrossRefPubMedGoogle Scholar
  2. Acevedo-Garcia J, Spencer D, Thieron H, Reinstadler A, Hammond-Kosack K, Phillips AL, Panstruga R (2016) mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnol J. doi:10.1111/pbi.12631 PubMedGoogle Scholar
  3. Alagoz Y, Gurkok T, Zhang B, Unver T (2016) Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci Rep 6:30910. doi:10.1038/srep30910 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Basak J, Nithin C (2015) Targeting non-coding RNAs in plants with the CRISPR-Cas technology is a challenge yet worth accepting. frontiers in plant science 6Google Scholar
  5. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9(1):39CrossRefPubMedPubMedCentralGoogle Scholar
  6. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84. doi:10.1016/j.copbio.2014.11.007 CrossRefPubMedGoogle Scholar
  7. Berbel A, Ferrandiz C, Hecht V, Dalmais M, Lund OS, Sussmilch FC, Taylor SA, Bendahmane A, Ellis TH, Beltran JP, Weller JL, Madueno F (2012) VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nat Commun 3:797. doi:10.1038/ncomms1801 CrossRefPubMedGoogle Scholar
  8. Blomstedt CK, Gleadow RM, O'Donnell N, Naur P, Jensen K, Laursen T, Olsen CE, Stuart P, Hamill JD, Moller BL, Neale AD (2012) A combined biochemical screen and TILLING approach identifies mutations in Sorghum bicolor L. Moench resulting in acyanogenic forage production. Plant Biotechnol J 10(1):54–66. doi:10.1111/j.1467-7652.2011.00646.x CrossRefPubMedGoogle Scholar
  9. Boualem A, Fleurier S, Troadec C, Audigier P, Kumar AP, Chatterjee M, Alsadon AA, Sadder MT, Wahb-Allah MA, Al-Doss AA (2014) Development of a Cucumis sativus TILLinG platform for forward and reverse genetics. PLoS One 9(5):e97963CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brooks C, Nekrasov V, Lippman ZB, 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 Physiol 166(3):1292–1297. doi:10.1104/pp.114.247577 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brozynska M, Furtado A, Henry RJ (2016) Genomics of crop wild relatives: expanding the gene pool for crop improvement. Plant Biotechnol J 14(4):1070–1085. doi:10.1111/pbi.12454 CrossRefPubMedGoogle Scholar
  12. Cermak T, Baltes NJ, Cegan R, Zhang Y, Voytas DF (2015) High-frequency, precise modification of the tomato genome. Genome Biol 16(1):232. doi:10.1186/s13059-015-0796-9 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Molecular plant pathologyGoogle Scholar
  14. Comai L, Young K, Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Henikoff S (2004) Efficient discovery of DNA polymorphisms in natural populations by ecotilling. Plant J 37(5):778–786CrossRefPubMedGoogle Scholar
  15. Cooper HD, Spillane C, Hodgkin T (2001) Broadening the genetic base of crop production. CABIGoogle Scholar
  16. Cooper JL, Henikoff S, Comai L, Till BJ (2013) TILLING and ecotilling for rice. Methods Mol Biol 956:39–56. doi:10.1007/978-1-62703-194-3_4 CrossRefPubMedGoogle Scholar
  17. Dahmani-Mardas F, Troadec C, Boualem A, Leveˆque S, Alsadon AA, Aldoss AA, Dogimont C, Bendahmane A (2010) Engineering melon plants with improved fruit shelf life using the TILLING approach. PLoS One 5(12):e15776CrossRefPubMedPubMedCentralGoogle Scholar
  18. Egelie KJ, Graff GD, Strand SP, Johansen B (2016) The emerging patent landscape of CRISPR-Cas gene editing technology. Nat Biotechnol 34(10):1025–1031CrossRefPubMedGoogle Scholar
  19. Elahi N, Duncan RW, Stasolla C (2015) Decreased seed oil production in FUSCA3 Brassica napus mutant plants. Plant Physiol Biochem 96:222–230. doi:10.1016/j.plaphy.2015.08.002 CrossRefPubMedGoogle Scholar
  20. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific reports 5Google Scholar
  21. Fang Y, Tyler BM (2015) Efficient disruption and replacement of an effector gene in the oomycete Phytophthora sojae using CRISPR/Cas9. Mol Plant Pathol 17:127–139CrossRefPubMedGoogle Scholar
  22. Gauffier C, Lebaron C, Moretti A, Constant C, Moquet F, Bonnet G, Caranta C, Gallois JL (2016) A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy. The Plant journal : for cell and molecular biology 85(6):717–729. doi:10.1111/tpj.13136 CrossRefGoogle Scholar
  23. Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV, Sanchez-Leon S, Baltes NJ, Starker C, Barro F, Gao C, Voytas DF (2016) High efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J. doi:10.1111/tpj.13446 Google Scholar
  24. Godfray HC, Garnett T (2014) Food security and sustainable intensification. Philos Trans R Soc Lond Ser B Biol Sci 369(1639):20120273. doi:10.1098/rstb.2012.0273 CrossRefGoogle Scholar
  25. 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 Research Notes 2(1):258CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gross BL, Olsen KM (2010) Genetic perspectives on crop domestication. Trends Plant Sci 15(9):529–537CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hartung F, Schiemann J (2014) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J 78(5):742–752. doi:10.1111/tpj.12413 CrossRefPubMedGoogle Scholar
  28. Henry IM, Nagalakshmi U, Lieberman MC, Ngo KJ, Krasileva KV, Vasquez-Gross H, Akhunova A, Akhunov E, Dubcovsky J, Tai TH (2014) Efficient genome-wide detection and cataloging of EMS-induced mutations using exome capture and next-generation sequencing. Plant Cell 26(4):1382–1397CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C, Bendahmane A, Ellis N (2009) Tendril-less regulates tendril formation in pea leaves. Plant Cell 21(2):420–428. doi:10.1105/tpc.108.064071 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Huang S, Weigel D, Beachy RN, Li J (2016) A proposed regulatory framework for genome-edited crops. Nat Genet 48(2):109CrossRefPubMedGoogle Scholar
  31. King R, Bird N, Ramirez-Gonzalez R, Coghill JA, Patil A, Hassani-Pak K, Uauy C, Phillips AL (2015) Mutation scanning in wheat by exon capture and next-generation sequencing. PLoS One 10(9):e0137549. doi:10.1371/journal.pone.0137549 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Konzak CF, Nilan RA, Kleinhofs A (1976) Artificial mutagenesis as an aid in overcoming genetic vulnerability of crop plants. Basic Life Sci 8:163–177PubMedGoogle Scholar
  33. Kovach MJ, McCouch SR (2008) Leveraging natural diversity: back through the bottleneck. Curr Opin Plant Biol 11(2):193–200. doi:10.1016/j.pbi.2007.12.006 CrossRefPubMedGoogle Scholar
  34. Kumar AP, Boualem A, Bhattacharya A, Parikh S, Desai N, Zambelli A, Leon A, Chatterjee M, Bendahmane A (2013) SMART—sunflower mutant population and reverse genetic tool for crop improvement. BMC Plant Biol 13:38. doi:10.1186/1471-2229-13-38 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lai KS, Kaothien-Nakayama P, Iwano M, Takayama S (2012) A TILLING resource for functional genomics in Arabidopsis thaliana accession C24. Genes & Genetic Systems 87(5):291–297CrossRefGoogle Scholar
  36. Ledford H (2016) Titanic clash over CRISPR patents turns ugly. Nature 537(7621):460–461CrossRefPubMedGoogle Scholar
  37. Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C (2016) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2:16139. doi:10.1038/nplants.2016.139 CrossRefPubMedGoogle Scholar
  38. Lowder LG, Zhang D, Baltes NJ, Paul JW 3rd, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169(2):971–985. doi:10.1104/pp.15.00636 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mao Y, Zhang Z, Feng Z, Wei P, Zhang H, Botella JR, Zhu JK (2016) Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol J 14(2):519–532CrossRefPubMedGoogle Scholar
  40. McDougall P (2011) The cost and time involved in the discovery, development and authorisation of a new plant biotechnology derived trait. Phillips McDougall, United KingdomGoogle Scholar
  41. McKeown PC, Fort A, Duszynska D, Sulpice R, Spillane C (2013a) Emerging molecular mechanisms for biotechnological harnessing of heterosis in crops. Trends Biotechnol 31:549–551CrossRefPubMedGoogle Scholar
  42. McKeown PC, Keshavaiah C, Fort A, Tuteja R, Chatterjee M, Varshney RK, Spillane C (2013b) Genomics in agriculture and food processing. In: Panesar PS, Marwaha SS (eds) Biotechnology in agriculture and food processing: Opportunities and challenges. Taylor & Francis, CRC PressGoogle Scholar
  43. Meyer RS, Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14(12):840–852CrossRefPubMedGoogle Scholar
  44. Minoia S, Boualem A, Marcel F, Troadec C, Quemener B, Cellini F, Petrozza A, Vigouroux J, Lahaye M, Carriero F, Bendahmane A (2016) Induced mutations in tomato SlExp1 alter cell wall metabolism and delay fruit softening. Plant Sci 242:195–202. doi:10.1016/j.plantsci.2015.07.001 CrossRefPubMedGoogle Scholar
  45. Missirian V, Comai L, Filkov V (2011) Statistical mutation calling from sequenced overlapping DNA pools in TILLING experiments. BMC Bioinformatics 12:287. doi:10.1186/1471-2105-12-287 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147(3):969–977. doi:10.1104/pp.108.118232 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Morineau C, Bellec Y, Tellier F, Gissot L, Kelemen Z, Nogue F, Faure JD (2016) Selective gene dosage by CRISPR-Cas9 genome editing in hexaploid Camelina sativa. Plant Biotechnol J. doi:10.1111/pbi.12671 PubMedGoogle Scholar
  48. Morris SH, Spillane C (2008) GM directive deficiencies in the European Union. EMBO Rep 9(6):500–504. doi:10.1038/embor.2008.94 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Murphy D (2007) Plant breeding and biotechnology. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  50. Nieto C, Piron F, Dalmais M, Marco CF, Moriones E, Gómez-Guillamón ML, Truniger V, Gómez P, Garcia-Mas J, Aranda MA (2007) EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol 7(1):34CrossRefPubMedPubMedCentralGoogle Scholar
  51. Onda Y, Mochida K (2016) Exploring genetic diversity in plants using high-throughput sequencing techniques. Curr Genomics 17(4):358–367. doi:10.2174/1389202917666160331202742 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Parry MA, Madgwick PJ, Bayon C, Tearall K, Hernandez-Lopez A, Baudo M, Rakszegi M, Hamada W, Al-Yassin A, Ouabbou H (2009) Mutation discovery for crop improvement. J Exp Bot 60(10):2817–2825CrossRefPubMedGoogle Scholar
  53. Perry J, Brachmann A, Welham T, Binder A, Charpentier M, Groth M, Haage K, Markmann K, Wang TL, Parniske M (2009) TILLING in Lotus japonicus identified large allelic series for symbiosis genes and revealed a bias in functionally defective ethyl methanesulfonate alleles toward glycine replacements. Plant Physiol 151(3):1281–1291CrossRefPubMedPubMedCentralGoogle Scholar
  54. Puchta H (2016) Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr Opin Plant Biol 36:1–8. doi:10.1016/j.pbi.2016.11.011 CrossRefPubMedGoogle Scholar
  55. Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol 17(8):1276–1288. doi:10.1111/mpp.12417 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Quetier F (2016) The CRISPR-Cas9 technology: closer to the ultimate toolkit for targeted genome editing. Plant Sci 242:65–76. doi:10.1016/j.plantsci.2015.09.003 CrossRefPubMedGoogle Scholar
  57. Reddy TV, Dwivedi S, Sharma NK (2012) Development of TILLING by sequencing platform towards enhanced leaf yield in tobacco. Ind Crop Prod 40:324–335CrossRefGoogle Scholar
  58. Ricroch A, Harwood W, Svobodová Z, Sági L, Hundleby P, Badea EM, Rosca I, Cruz G, Salema Fevereiro MP, Marfà Riera V (2015) Challenges facing European agriculture and possible biotechnological solutions. Crit Rev Biotechnol:1–9Google Scholar
  59. Ricroch AE, Ammann K, Kuntz M (2016a) Editing EU legislation to fit plant genome editing. EMBO reports: e201643099Google Scholar
  60. Ricroch AE, Ammann K, Kuntz M (2016b) Editing EU legislation to fit plant genome editing. EMBO Rep. doi:10.15252/embr.201643099 PubMedGoogle Scholar
  61. Scully ED, Gries T, Funnell-Harris DL, Xin Z, Kovacs FA, Vermerris W, Sattler SE (2015) Characterization of novel Brown midrib 6 mutations affecting lignin biosynthesis in sorghum. J Integr Plant Biol. doi:10.1111/jipb.12375 PubMedGoogle Scholar
  62. Sestili F, Botticella E, Bedo Z, Phillips A, Lafiandra D (2010) Production of novel allelic variation for genes involved in starch biosynthesis through mutagenesis. Mol Breed 25(1):145–154. doi:10.1007/s11032-009-9314-7 CrossRefGoogle Scholar
  63. Seth K, Harish (2016) Current status of potential applications of repurposed Cas9 for structural and functional genomics of plants. Biochem Biophys Res Commun. doi:10.1016/j.bbrc.2016.10.130 Google Scholar
  64. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu J-L (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31(8):686–688CrossRefPubMedGoogle Scholar
  65. Shen L, Wang C, Fu Y, Wang J, Liu Q, Zhang X, Yan C, Qian Q, Wang K (2016) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol. doi:10.1111/jipb.12501 Google Scholar
  66. Sheridan C (2014) First CRISPR-Cas patent opens race to stake out intellectual property. Nat Biotechnol 32(7):599–601. doi:10.1038/nbt0714-599 CrossRefPubMedGoogle Scholar
  67. Sherkow JS (2015) Law, history and lessons in the CRISPR patent conflict. Nat Biotechnol 33(3):256–257. doi:10.1038/nbt.3160 CrossRefPubMedGoogle Scholar
  68. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2016) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J. doi:10.1111/pbi.12603 Google Scholar
  69. 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. doi:10.1038/nbt1043 CrossRefPubMedGoogle Scholar
  70. Slade AJ, Knauf VC (2005) TILLING moves beyond functional genomics into crop improvement. Transgenic Res 14(2):109–115CrossRefPubMedGoogle Scholar
  71. Smyth SJ (2016) Canadian regulatory perspectives on genome engineered crops. GM Crops Food: 0. doi:10.1080/21645698.2016.1257468
  72. Soyk S, Muller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jimenez-Gomez JM, Lippman ZB (2016) Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet. doi:10.1038/ng.3733 PubMedGoogle Scholar
  73. Spillane C, Swanson T (2002) Agricultural biotechnology and developing countries: proprietary knowledge and diffusion of benefits. Biotechnology, agriculture and the developing world: The distributional implications of technological change:67–134Google Scholar
  74. Sprink T, Eriksson D, Schiemann J, Hartung F (2016a) Regulatory hurdles for genome editing: process- vs. product-based approaches in different regulatory contexts. Plant Cell Rep 35(7):1493–1506. doi:10.1007/s00299-016-1990-2 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Sprink T, Eriksson D, Schiemann J, Hartung F (2016b) Regulatory hurdles for genome editing: process-vs. product-based approaches in different regulatory contexts. Plant cell reports: 1–14Google Scholar
  76. Straubeta A, Lahaye T (2013) Zinc fingers, TAL effectors, or Cas9-based DNA binding proteins: what’s best for targeting desired genome loci? Mol Plant 6(5):1384–1387. doi:10.1093/mp/sst075 CrossRefPubMedGoogle Scholar
  77. Sulpice R, McKeown PC (2015) Moving towards a comprehensive map of central plant metabolism. Annual review of plant biology 66 (1)Google Scholar
  78. Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169(2):931–945. doi:10.1104/pp.15.00793 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Tang H, Sezen U, Paterson AH (2010) Domestication and plant genomes. Curr Opin Plant Biol 13(2):160–166. doi:10.1016/j.pbi.2009.10.008 CrossRefPubMedGoogle Scholar
  80. Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Young K, Taylor NE, Henikoff JG, Comai L, Henikoff S (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13(3):524–530. doi:10.1101/gr.977903 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Triques K, Sturbois B, Gallais S, Dalmais M, Chauvin S, Clepet C, Aubourg S, Rameau C, Caboche M, Bendahmane A (2007a) Characterization of Arabidopsis thaliana mismatch specific endonucleases: application to mutation discovery by TILLING in pea. The Plant journal : for cell and molecular biology 51(6):1116–1125. doi:10.1111/j.1365-313X.2007.03201.x CrossRefGoogle Scholar
  82. Triques K, Sturbois B, Gallais S, Dalmais M, Chauvin S, Clepet C, Aubourg S, Rameau C, Caboche M, Bendahmane A (2007b) Characterization of Arabidopsis thaliana mismatch specific endonucleases: application to mutation discovery by TILLING in pea. Plant J 51(6):1116–1125. doi:10.1111/j.1365-313X.2007.03201.x CrossRefPubMedGoogle Scholar
  83. Tsai H, Howell T, Nitcher R, Missirian V, Watson B, Ngo KJ, Lieberman M, Fass J, Uauy C, Tran RK, Khan AA, Filkov V, Tai TH, Dubcovsky J, Comai L (2011) Discovery of rare mutations in populations: TILLING by sequencing. Plant Physiol 156(3):1257–1268. doi:10.1104/pp.110.169748 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Tsai H, Missirian V, Ngo KJ, Tran RK, Chan SR, Sundaresan V, Comai L (2013) Production of a high-efficiency TILLING population through polyploidization. Plant Physiol 161(4):1604–1614. doi:10.1104/pp.112.213256 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Uluisik S, Chapman NH, Smith R, Poole M, Adams G, Gillis RB, Besong TM, Sheldon J, Stiegelmeyer S, Perez L, Samsulrizal N, Wang D, Fisk ID, Yang N, Baxter C, Rickett D, Fray R, Blanco-Ulate B, Powell AL, Harding SE, Craigon J, Rose JK, Fich EA, Sun L, Domozych DS, Fraser PD, Tucker GA, Grierson D, Seymour GB (2016) Corrigendum: genetic improvement of tomato by targeted control of fruit softening. Nat Biotechnol 34(10):1072. doi:10.1038/nbt1016-1072d CrossRefPubMedGoogle Scholar
  86. Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3: Genes| Genomes| Genetics 3(12):2233–2238CrossRefPubMedPubMedCentralGoogle Scholar
  87. van de Wiel C, Lotz L, de Bakker H, Smulders M (2016) Intellectual property rights and native traits in plant breeding. UR Plant Breeding, WageningenCrossRefGoogle Scholar
  88. Van Hintum TJL, Brown AHD, Spillane C, Hodgkin T Core collections of Plant Genetic Resources. 2000 In: IPGRI technical bulletin, IPGRI, Rome. pp 1–48Google Scholar
  89. van Nimwegen KJ, van Soest RA, Veltman JA, Nelen MR, van der Wilt GJ, Vissers LE, Grutters JP (2016) Is the $1000 genome as near as we think? A cost analysis of next-generation sequencing. Clin Chem. doi:10.1373/clinchem.2016.258632 PubMedGoogle Scholar
  90. Vicente-Dolera N, Troadec C, Moya M, del Rio-Celestino M, Pomares-Viciana T, Bendahmane A, Pico B, Roman B, Gomez P (2014) First TILLING platform in Cucurbita pepo: a new mutant resource for gene function and crop improvement. PLoS One 9(11):e112743. doi:10.1371/journal.pone.0112743 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Visendi P, Batley J, Edwards D (2013) Next generation characterisation of cereal genomes for marker discovery. Biology 2(4):1357–1377CrossRefPubMedPubMedCentralGoogle Scholar
  92. Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12(6):e1001877CrossRefPubMedPubMedCentralGoogle Scholar
  93. Waltz E (2016) Gene-edited CRISPR mushroom escapes US regulation. Nature 532(7599):293. doi:10.1038/nature.2016.19754 CrossRefPubMedGoogle Scholar
  94. Wang L, Wang L, Tan Q, Fan Q, Zhu H, Hong Z, Zhang Z, Duanmu D (2016) Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus Japonicus using CRISPR-Cas9. Front Plant Sci 7:1333. doi:10.3389/fpls.2016.01333 PubMedPubMedCentralGoogle Scholar
  95. Wang T, Uauy C, Till B, Liu CM (2010) TILLING and associated technologies. J Integr Plant Biol 52(11):1027–1030CrossRefPubMedGoogle Scholar
  96. Wang TL, Uauy C, Robson F, Till B (2012) TILLING in extremis. Plant Biotechnol J 10(7):761–772. doi:10.1111/j.1467-7652.2012.00708.x CrossRefPubMedGoogle Scholar
  97. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J-L (2014a) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotech 32(9):947–951. doi:10.1038/nbt.2969 http://www.nature.com/nbt/journal/v32/n9/abs/nbt.2969.html-supplementary-information CrossRefGoogle Scholar
  98. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014b) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32(9):947–951. doi:10.1038/nbt.2969 CrossRefPubMedGoogle Scholar
  99. Wang Z-P, Xing H-L, Dong L, Zhang H-Y, Han C-Y, Wang X-C, Chen Q-J (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol 16(1):1CrossRefGoogle Scholar
  100. Warschefsky E, Penmetsa RV, Cook DR, von Wettberg EJ (2014) Back to the wilds: tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am J Bot 101(10):1791–1800. doi:10.3732/ajb.1400116 CrossRefPubMedGoogle Scholar
  101. Weil CF (2009) TILLING in grass species. Plant Physiol 149(1):158–164. doi:10.1104/pp.108.128785 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Wolt JD, Wang K, Yang B (2015) The regulatory status of genome-edited crops. Plant Biotechnol J. doi:10.1111/pbi.12444 PubMedPubMedCentralGoogle Scholar
  103. Zhou H, He M, Li J, Chen L, Huang Z, Zheng S, Zhu L, Ni E, Jiang D, Zhao B, Zhuang C (2016) Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep 6:37395. doi:10.1038/srep37395 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Zhu C, Bortesi L, Baysal C, Twyman RM, Fischer R, Capell T, Schillberg S, Christou P (2016) Characteristics of genome editing mutations in cereal crops. Trends Plant Sci. doi:10.1016/j.tplants.2016.08.009 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Anishkumar P. K. Kumar
    • 1
    • 2
  • Peter C. McKeown
    • 1
  • Adnane Boualem
    • 3
  • Peter Ryder
    • 1
  • Galina Brychkova
    • 1
  • Abdelhafid Bendahmane
    • 3
  • Abhimanyu Sarkar
    • 4
  • Manash Chatterjee
    • 1
    • 2
  • Charles Spillane
    • 1
  1. 1.Genetics and Biotechnology Lab, Plant & AgriBiosciences Research Centre (PABC), School of Natural Sciences, C306 Áras de BrúnNational University of Ireland GalwayGalwayIreland
  2. 2.Bench Bio Pvt.LtdVapiIndia
  3. 3.Unité de Recherche en Génomique Végétale (URGV)ÉvryFrance
  4. 4.Metabolic Biology DepartmentJohn Innes CentreNorwichUK

Personalised recommendations