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

doi:10.1007/s11032-017-0620-1

Molecular Breeding

February 2017, 37:14

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

Authors
Authors and affiliations

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

Review

First Online:: 23 January 2017

Received:: 03 October 2016
Accepted:: 02 January 2017

DOI: 10.1007/s11032-017-0620-1

Cite this article as:: Kumar, A.P.K., McKeown, P.C., Boualem, A. et al. Mol Breeding (2017) 37: 14. doi:10.1007/s11032-017-0620-1

1 Citations
11 Shares
674 Downloads

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

Abbott A (2015) Europe’s genetically edited plants stuck in legal limbo. Nature 528:319–320CrossRefPubMedGoogle Scholar
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
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
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 6
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
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
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
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
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
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
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
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
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 pathology
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
Cooper HD, Spillane C, Hodgkin T (2001) Broadening the genetic base of crop production. CABI
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
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
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
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
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 5
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
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
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
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
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
Gross BL, Olsen KM (2010) Genetic perspectives on crop domestication. Trends Plant Sci 15(9):529–537CrossRefPubMedPubMedCentralGoogle Scholar
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
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
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
Huang S, Weigel D, Beachy RN, Li J (2016) A proposed regulatory framework for genome-edited crops. Nat Genet 48(2):109CrossRefPubMedGoogle Scholar
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
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
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
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
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
Ledford H (2016) Titanic clash over CRISPR patents turns ugly. Nature 537(7621):460–461CrossRefPubMedGoogle Scholar
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
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
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
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
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
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 Press
Meyer RS, Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14(12):840–852CrossRefPubMedGoogle Scholar
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
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
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
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
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
Murphy D (2007) Plant breeding and biotechnology. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
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
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
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
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
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
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
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
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
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:1–9
Ricroch AE, Ammann K, Kuntz M (2016a) Editing EU legislation to fit plant genome editing. EMBO reports: e201643099
Ricroch AE, Ammann K, Kuntz M (2016b) Editing EU legislation to fit plant genome editing. EMBO Rep. doi:10.15252/embr.201643099 PubMedGoogle Scholar
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
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
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
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
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
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
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
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
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
Slade AJ, Knauf VC (2005) TILLING moves beyond functional genomics into crop improvement. Transgenic Res 14(2):109–115CrossRefPubMedGoogle Scholar
Smyth SJ (2016) Canadian regulatory perspectives on genome engineered crops. GM Crops Food: 0. doi:10.1080/21645698.2016.1257468
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
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:67–134
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
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: 1–14
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
Sulpice R, McKeown PC (2015) Moving towards a comprehensive map of central plant metabolism. Annual review of plant biology 66 (1)
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
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
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
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
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
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
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
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
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
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
Van Hintum TJL, Brown AHD, Spillane C, Hodgkin T Core collections of Plant Genetic Resources. 2000 In: IPGRI technical bulletin, IPGRI, Rome. pp 1–48
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
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
Visendi P, Batley J, Edwards D (2013) Next generation characterisation of cereal genomes for marker discovery. Biology 2(4):1357–1377CrossRefPubMedPubMedCentralGoogle Scholar
Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12(6):e1001877CrossRefPubMedPubMedCentralGoogle Scholar
Waltz E (2016) Gene-edited CRISPR mushroom escapes US regulation. Nature 532(7599):293. doi:10.1038/nature.2016.19754 CrossRefPubMedGoogle Scholar
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
Wang T, Uauy C, Till B, Liu CM (2010) TILLING and associated technologies. J Integr Plant Biol 52(11):1027–1030CrossRefPubMedGoogle Scholar
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
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
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
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
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
Weil CF (2009) TILLING in grass species. Plant Physiol 149(1):158–164. doi:10.1104/pp.108.128785 CrossRefPubMedPubMedCentralGoogle Scholar
Wolt JD, Wang K, Yang B (2015) The regulatory status of genome-edited crops. Plant Biotechnol J. doi:10.1111/pbi.12444 PubMedPubMedCentralGoogle Scholar
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
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

Funding information

Funder Name	Grant Number	Funding Note
Science Foundation Ireland	08/IN.1/B1931

Copyright information

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
Email authorView author's OrcID profile

1.Genetics and Biotechnology Lab, Plant & AgriBiosciences Research Centre (PABC), School of Natural Sciences, C306 Áras de BrúnNational University of Ireland GalwayGalwayIreland
2.Bench Bio Pvt.LtdVapiIndia
3.Unité de Recherche en Génomique Végétale (URGV)ÉvryFrance
4.Metabolic Biology DepartmentJohn Innes CentreNorwichUK

Personalised recommendations

Actions

Unlimited access to the full article
Instant download
Include local sales tax if applicable

Subscribe to Journal

Get Access to

Molecular Breeding

for the whole of 2017

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

Abstract

Keywords

Funding information

Copyright information

Authors and Affiliations

Personalised recommendations

Cookies