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Review Articles

Targeting Induced Local Lesions in Genomes (TILLING): advances and opportunities for fast tracking crop breeding

, , , , , , & ORCID Icon show all
Pages 817-836 | Received 14 Feb 2021, Accepted 01 Jun 2023, Published online: 16 Jul 2023

References

  • Schmidt CW. Genetically modified foods: breeding uncertainty. Environ Health Perspect. 2005;113:A526–A533. doi: 10.1289/ehp.113-a526.
  • McCallum CM, Comai L, Greene EA, et al. Targeted screening for induced mutations. Nat Biotechnol. 2000;18:455–457. doi: 10.1038/74542.
  • Kurowska M, Daszkowska-Golec A, Gruszka D, et al. TILLING - a shortcut in functional genomics. J Appl Genetics. 2011;52:371–390. doi: 10.1007/s13353-011-0061-1.
  • Alonso JM, Ecker JR. Moving forward in reverse: genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nat Rev Genet. 2006;7:524–536. doi: 10.1038/nrg1893.
  • Till BJ, Reynolds SH, Weil C, et al. Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol. 2004;4:1–8. doi: 10.1186/1471-2229-4-12.
  • Banik M, Liu S, Yu K, et al. Molecular TILLING and EcoTILLING : effective tools for mutant gene detection in plants. Genes Genomes Genomics. 2007;1:123–131.
  • Barkley N, Wang M. Application of TILLING and EcoTILLING as reverse genetic approaches to elucidate the function of genes in plants and animals. Curr Genomics. 2008;9:212–226.
  • Dessalegn O. Current status of Targeting Induced Local Lesions IN Genomes (TILLING) and its relevance to plant functional genomics, polymorphism assessment and plant breeding with relevant case studies on different crops. Adv Crop Sci Tech. 2017;05:1–4. doi: 10.4172/2329-8863.1000320.
  • Caldwell DG, McCallum N, Shaw P, et al. A structured mutant population for forward and reverse genetics in Barley (Hordeum vulgare L.). Plant J. 2004;40:143–150. doi: 10.1111/j.1365-313X.2004.02190.x.
  • Till BJ, Jankowicz-Cieslak J, Sági L, et al. Discovery of nucleotide polymorphisms in the Musa gene pool by Ecotilling. Theor Appl Genet. 2010;121:1381–1389. doi: 10.1007/s00122-010-1395-5.
  • Slade AJ, Knauf VC. TILLING moves beyond functional genomics into crop improvement. Transgenic Res. 2005;14:109–115. doi: 10.1007/s11248-005-2770-x.
  • Comai L, Young K, Till BJ, et al. Efficient discovery of DNA polymorphisms in natural populations by Ecotilling. Plant J. 2004;37:778–786. doi: 10.1111/j.0960-7412.2003.01999.x.
  • Raja RB, Agasimani S, Jaiswal S, et al. EcoTILLING by Sequencing reveals polymorphisms in genes encoding starch synthases that are associated with low glycemic response in rice. BMC Plant Biol. 2017;17:13. doi: 10.1186/s12870-016-0968-0.
  • Gilchrist EJ, Haughn GW. TILLING without a plough: a new method with applications for reverse genetics. Curr Opin Plant Biol. 2005;8:211–215. doi: 10.1016/j.pbi.2005.01.004.
  • Till BJ, Zerr T, Comai L, et al. A protocol for TILLING and Ecotilling in plants and animals. Nat Protoc. 2006;1:2465–2477. doi: 10.1038/nprot.2006.329.
  • Barkley NA, Wang ML, Gillaspie AG, et al. Discovering and verifying DNA polymorphisms in a mung bean [V. radiata (L.) R. Wilczek] collection by EcoTILLING and sequencing. BMC Res Notes. 2008;1:28. doi: 10.1186/1756-0500-1-28.
  • Qiao J, Cai M, Yan G, et al. High-throughput multiplex cpDNA resequencing clarifies the genetic diversity and genetic relationships among Brassica napus, Brassica rapa and Brassica oleracea. Plant Biotechnol J. 2016;14:409–418. doi: 10.1111/pbi.12395.
  • Irshad A, Guo H, Zhang S, et al. EcoTILLING reveals natural allelic variations in starch synthesis key gene TaSSIV and its haplotypes associated with higher thousand grain weight. Genes. 2019;10:307. doi: 10.3390/genes10040307.
  • Garvin MR, Gharrett AJ. DEco-TILLING: an inexpensive method for single nucleotide polymorphism discovery that reduces ascertainment bias. Mol Ecol Notes. 2007;7:735–746. doi: 10.1111/j.1471-8286.2007.01767.x.
  • Malomane DK, Reimer C, Weigend S, et al. Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics. 2018;19:22. doi: 10.1186/s12864-017-4416-9.
  • Wang G-X, Imaizumi T, Li W, et al. Self-EcoTILLING to identify single-nucleotide mutations in multigene family. Pestic Biochem Physiol. 2008;92:24–29. doi: 10.1016/j.pestbp.2008.05.001.
  • Bush SM, Krysan PJ. iTILLING: a personalized approach to the identification of induced mutations in Arabidopsis. Plant Physiol. 2010;154:25–35. doi: 10.1104/pp.110.159897.
  • Krysan P. Ice-Cap. A high-throughput method for capturing plant tissue samples for genotype analysis. Plant Physiol. 2004;135:1162–1169. doi: 10.1104/pp.104.040774.
  • Li X, Lassner M, Zhang Y. Deleteagene: a fast neutron deletion mutagenesis-based gene knockout system for plants. Comp Funct Genomics. 2002;3:158–160. doi: 10.1002/cfg.148.
  • Li X, Song Y, Century K, et al. A fast neutron deletion mutagenesis-based reverse genetics system for plants. Plant J. 2001;27:235–242. doi: 10.1046/j.1365-313x.2001.01084.x.
  • Rogers C, Wen J, Chen R, et al. Deletion-based reverse genetics in Medicago truncatula. Plant Physiol. 2009;151:1077–1086. doi: 10.1104/pp.109.142919.
  • Wang TL, Uauy C, Robson F, et al. TILLING in extremis. Plant Biotechnol J. 2012;10:761–772. doi: 10.1111/j.1467-7652.2012.00708.x.
  • Tsai H, Missirian V, Ngo KJ, et al. Production of a high-efficiency TILLING population through polyploidization. Plant Physiol. 2013;161:1604–1614. doi: 10.1104/pp.112.213256.
  • Uauy C, Paraiso F, Colasuonno P, et al. A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol. 2009;9:115. doi: 10.1186/1471-2229-9-115.
  • Holme IB, Gregersen PL, Brinch-Pedersen H. Induced genetic variation in crop plants by random or targeted mutagenesis: convergence and differences. Front Plant Sci. 2019;10:1–9. doi: 10.3389/fpls.2019.01468.
  • Slade AJ, Fuerstenberg SI, Loeffler D, et al. A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol. 2005;23:75–81. doi: 10.1038/nbt1043.
  • Elias R, Till BJ, Mba C, et al. Optimizing TILLING and Ecotilling techniques for potato (Solanum tuberosum L). BMC Res Notes. 2009;2:1–5. doi: 10.1186/1756-0500-2-141.
  • Jankowicz-Cieslak J, Huynh OA, Brozynska M, et al. Induction, rapid fixation and retention of mutations in vegetatively propagated banana. Plant Biotechnol J. 2012;10:1056–1066. doi: 10.1111/j.1467-7652.2012.00733.x.
  • Taheri S, Abdullah TL, Jain SM, et al. TILLING, high-resolution melting (HRM), and next-generation sequencing (NGS) techniques in plant mutation breeding. Mol Breed. 2017;37:40.
  • Guo Y, Abernathy B, Zeng Y, et al. TILLING by Sequencing to identify induced mutations in stress resistance genes of peanut (Arachis hypogaea). BMC Genomics. 2015;16:157. doi: 10.1186/s12864-015-1348-0.
  • Tsai H, Howell T, Nitcher R, et al. Discovery of rare mutations in populations: TILLING by Sequencing. Plant Physiol. 2011;156:1257–1268. doi: 10.1104/pp.110.169748.
  • Nida H, Blum S, Zielinski D, et al. Highly efficient de novo mutant identification in a Sorghum bicolor TILLING population using the ComSeq approach. Plant J. 2016;86:349–359. doi: 10.1111/tpj.13161.
  • Mo Y, Howell T, Vasquez-Gross H, et al. Mapping causal mutations by exome sequencing in a wheat TILLING population: a tall mutant case study. Mol Genet Genomics. 2018;293:463–477. doi: 10.1007/s00438-017-1401-6.
  • King R, Bird N, Ramirez-Gonzalez R, et al. Mutation scanning in wheat by exon capture and next-generation sequencing. PLoS One. 2015;10:e0137549. doi: 10.1371/journal.pone.0137549.
  • Krasileva KV, Vasquez-Gross HA, Howell T, et al. Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci. 2017;114:E913–E921.
  • Mascher M, Richmond TA, Gerhardt DJ, et al. Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J. 2013;76:494–505. doi: 10.1111/tpj.12294.
  • Schreiber M, Barakate A, Uzrek N, et al. A highly mutagenised barley (cv. Golden Promise) TILLING population coupled with strategies for screening-by-sequencing. Plant Methods. 2019;15:99. doi: 10.1186/s13007-019-0486-9.
  • Yano R, Hoshikawa K, Okabe Y, et al. Multiplex exome sequencing reveals genome-wide frequency and distribution of mutations in the ‘Micro-Tom’ targeting induced local lesions in genomes (TILLING) mutant library. Plant Biotechnol. 2019;36:223–231. doi: 10.5511/plantbiotechnology.19.0830a.
  • Gilchrist EJ, Sidebottom CHD, Koh CS, et al. A Mutant Brassica napus (Canola) population for the identification of new genetic diversity via TILLING and next generation sequencing. PLoS One. 2013;8:e84303. doi: 10.1371/journal.pone.0084303.
  • Reddy TV, Dwivedi S, Sharma NK. Development of TILLING by Sequencing platform towards enhanced leaf yield in tobacco. Ind Crops Prod. 2012;40:324–335. doi: 10.1016/j.indcrop.2012.03.031.
  • Kim H, Yoon M, Chun A, et al. Identification of novel mutations in the rice starch branching enzyme I gene via TILLING by Sequencing. Euphytica. 2018;214:94. doi: 10.1007/s10681-018-2174-7.
  • Kim S-I, Tai TH. Identification of novel rice low phytic acid mutations via TILLING by Sequencing. Mol Breeding. 2014;34:1717–1729. doi: 10.1007/s11032-014-0127-y.
  • Fanelli V, Ngo KJ, Thompson VL, et al. A TILLING by Sequencing approach to identify induced mutations in sunflower genes. Sci Rep. 2021;11:9885. doi: 10.1038/s41598-021-89237-w.
  • Thapa R, Carrero-Colón M, Rainey KM, et al. TILLING by Sequencing: a successful approach to identify rare alleles in soybean populations. Genes. 2019;10:1003. doi: 10.3390/genes10121003.
  • Marroni F, Pinosio S, Di Centa E, et al. Large-scale detection of rare variants via pooled multiplexed next-generation sequencing: towards next-generation Ecotilling. Plant J. 2011;67:736–745. doi: 10.1111/j.1365-313X.2011.04627.x.
  • Kumar APK, McKeown PC, Boualem A, et al. TILLING by Sequencing (TbyS) for targeted genome mutagenesis in crops. Mol Breed. 2017;37:14.
  • Irshad A, Guo H, Zhang S, et al. TILLING in cereal crops for allele expansion and mutation detection by using modern sequencing technologies. Agronomy. 2020;10:405. doi: 10.3390/agronomy10030405.
  • Lakhssassi N, Zhou Z, Liu S, et al. Soybean TILLING-by-sequencing + reveals the role of novel GmSACPD members in unsaturated fatty acid biosynthesis while maintaining healthy nodules. J Exp Bot. 2020;71:6969–6987. doi: 10.1093/jxb/eraa402.
  • Varadaraju A, Ramadoss BR, Gurunathan S, et al. TILLING by Sequencing (TbyS) reveals mutations in flowering control genes that are associated with altered plant architecture in Mungbean (Vigna radiata (L.) R. Wilczek). Genet Resour Crop Evol. 2021;68:849–864. doi: 10.1007/s10722-020-01028-w.
  • Elshire RJ, Glaubitz JC, Sun Q, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6:e19379. doi: 10.1371/journal.pone.0019379.
  • Poland JA, Brown PJ, Sorrells ME, et al. Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One. 2012;7:e32253. doi: 10.1371/journal.pone.0032253.
  • Missirian V, Comai L, Filkov V. Statistical mutation calling from sequenced overlapping DNA pools in TILLING experiments. BMC Bioinf. 2011;12:287. doi: 10.1186/1471-2105-12-287.
  • Gajek K, Janiak A, Korotko U, et al. Whole exome sequencing-based identification of a novel gene involved in root hair development in barley (Hordeum vulgare L). Int J Mol Sci. 2021;22:1–28.
  • van Dijk EL, Auger H, Jaszczyszyn Y, et al. Ten years of next-generation sequencing technology. Trends Genet. 2014;30:418–426. doi: 10.1016/j.tig.2014.07.001.
  • Li G, Jain R, Chern M, et al. The sequences of 1504 mutants in the model rice variety Kitaake facilitate rapid functional genomic studies. Plant Cell. 2017;29:1218–1231. doi: 10.1105/tpc.17.00154.
  • Sevanthi AV, Kandwal P, Kale PB, et al. Whole genome characterization of a few EMS-induced mutants of upland rice variety Nagina 22 reveals a staggeringly high frequency of SNPs which show high phenotypic plasticity towards the wild-type. Front Plant Sci. 2018;9:1–17. doi: 10.3389/fpls.2018.01179.
  • Ramkumar MK, Senthil Kumar S, Gaikwad K, et al. A novel stay-green mutant of rice with delayed leaf senescence and better harvest index confers drought tolerance. Plants. 2019;8:375. doi: 10.3390/plants8100375.
  • Comai L, Henikoff S. TILLING: practical single-nucleotide mutation discovery. Plant J. 2006;45:684–694. doi: 10.1111/j.1365-313X.2006.02670.x.
  • Madsen CK, Brinch-Pedersen H. A novel wheat q’ allele identified by forward genetic in silico TILLING. J Plant Physiol. 2020;251:153221. doi: 10.1016/j.jplph.2020.153221.
  • Till BJ, Reynolds SH, Greene EA, et al. Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res. 2003;13:524–530. doi: 10.1101/gr.977903.
  • Le Signor C, Savois V, Aubert G, et al. Optimizing TILLING populations for reverse genetics in Medicago truncatula. Plant Biotechnol J. 2009;7:430–441. doi: 10.1111/j.1467-7652.2009.00410.x.
  • Perry J, Brachmann A, Welham T, et al. TILLING in Lotus japonicus identified large allelic series for symbiosis genes and revealed a bias in functionally defective ethyl methane sulfonate alleles toward glycine replacements. Plant Physiol. 2009;151:1281–1291. doi: 10.1104/pp.109.142190.
  • Dalmais M, Antelme S, Ho-Yue-Kuang S, et al. A TILLING platform for functional genomics in Brachypodium distachyon. PLoS One. 2013;8:e65503. doi: 10.1371/journal.pone.0065503.
  • Gao Y-L, Yao X-F, Li W-Z, et al. An efficient TILLING platform for cultivated tobacco. J Integr Plant Biol. 2020;62:165–180. doi: 10.1111/jipb.12784.
  • Rawat N, Schoen A, Singh L, et al. TILL-D: an Aegilops tauschii TILLING resource for wheat improvement. Front Plant Sci. 2018;9:1–9. doi: 10.3389/fpls.2018.01665.
  • Gilchrist EJ, Haughn GW, Ying CC, et al. Use of Ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa. Mol Ecol. 2006;15:1367–1378. doi: 10.1111/j.1365-294X.2006.02885.x.
  • Dalmais M, Schmidt J, Le Signor C, et al. UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol. 2008;9:r43. doi: 10.1186/gb-2008-9-2-r43.
  • Boualem A, Fleurier S, Troadec C, et al. Development of a Cucumis sativus TILLinG platform for forward and reverse genetics. PLoS One. 2014;9:e97963. doi: 10.1371/journal.pone.0097963.
  • Vicente-Dólera N, Troadec C, Moya M, et al. First TILLING platform in Cucurbita pepo: a new mutant resource for gene function and crop improvement. PLoS One. 2014;9:e112743. doi: 10.1371/journal.pone.0112743.
  • Himelblau E, Gilchrist EJ, Buono K, et al. Forward and reverse genetics of rapid-cycling Brassica oleracea. Theor Appl Genet. 2009;118:953–961. doi: 10.1007/s00122-008-0952-7.
  • González M, Xu M, Esteras C, et al. Towards a TILLING platform for functional genomics in Piel de Sapo melons. BMC Res Notes. 2011;4:289. doi: 10.1186/1756-0500-4-289.
  • Okabe Y, Asamizu E, Ariizumi T, et al. Availability of Micro-Tom mutant library combined with TILLING in molecular breeding of tomato fruit shelf-life. Breed Sci. 2012;62:202–208. doi: 10.1270/jsbbs.62.202.
  • Minoia S, Petrozza A, D’Onofrio O, et al. A new mutant genetic resource for tomato crop improvement by TILLING technology. BMC Res Notes. 2010;3:69. doi: 10.1186/1756-0500-3-69.
  • Saito T, Ariizumi T, Okabe Y, et al. TOMATOMA: a novel tomato mutant database distributing micro-tom mutant collections. Plant Cell Physiol. 2011;52:283–296. doi: 10.1093/pcp/pcr004.
  • Sabetta W, Alba V, Blanco A, et al. sunTILL: a TILLING resource for gene function analysis in sunflower. Plant Methods. 2011;7:20. doi: 10.1186/1746-4811-7-20.
  • Kumar APK, Boualem A, Bhattacharya A, et al. SMART – Sunflower mutant population and reverse genetic tool for crop improvement. BMC Plant Biol. 2013;13:38. doi: 10.1186/1471-2229-13-38.
  • Stephenson P, Baker D, Girin T, et al. A rich TILLING resource for studying gene function in Brassica rapa. BMC Plant Biol. 2010;10:62. doi: 10.1186/1471-2229-10-62.
  • Harloff H-J, Lemcke S, Mittasch J, et al. A mutation screening platform for rapeseed (Brassica napus L.) and the detection of sinapine biosynthesis mutants. Theor Appl Genet. 2012;124:957–969. doi: 10.1007/s00122-011-1760-z.
  • Wang N, Wang Y, Tian F, et al. A functional genomics resource for Brassica napus: development of an EMS mutagenized population and discovery of FAE1 point mutations by TILLING. New Phytol. 2008;180:751–765. doi: 10.1111/j.1469-8137.2008.02619.x.
  • Maghuly F, Jankowicz-Cieslak J, Calari A, et al. Investigation of genetic variation in Jatropha curcas by Ecotilling and ISSR. BMC Proc. 2011;5: o 50. doi: 10.1186/1753-6561-5-S7-O50.
  • Chantreau M, Grec S, Gutierrez L, et al. PT-Flax (phenotyping and TILLinG of flax): development of a flax (Linum usitatissimum L.) mutant population and TILLinG platform for forward and reverse genetics. BMC Plant Biol. 2013;13:1–13. doi: 10.1186/1471-2229-13-159.
  • Aslam U, Cheema HMN, Ahmad S, et al. COTIP: cotton TILLING platform, a resource for plant improvement and reverse genetic studies. Front Plant Sci. 2016;07. doi: 10.3389/fpls.2016.01863.
  • Till BJ, Cooper J, Tai TH, et al. Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol. 2007;7:1–12. doi: 10.1186/1471-2229-7-19.
  • Rawat N, Joshi A, Pumphrey M, et al. A TILLING resource for hard red winter wheat variety jagger. Crop Sci. 2019;59:1666–1671. doi: 10.2135/cropsci2019.01.0011.
  • Fruzangohar M, Kalashyan E, Kalambettu P, et al. Novel informatic tools to support functional annotation of the durum wheat genome. Front Plant Sci. 2019;10. doi: 10.3389/fpls.2019.01244.
  • Chawade A, Sikora P, Bräutigam M, et al. Development and characterization of an oat TILLING-population and identification of mutations in lignin and β-glucan biosynthesis genes. BMC Plant Biol. 2010;10:1–13. doi: 10.1186/1471-2229-10-86.
  • Szurman-Zubrzycka ME, Zbieszczyk J, Marzec M, et al. HorTILLUS—a rich and renewable source of induced mutations for forward/reverse genetics and pre-breeding programs in barley (Hordeum vulgare L.). Front Plant Sci. 2018;9:1–16. doi: 10.3389/fpls.2018.00216.
  • Talamè V, Bovina R, Sanguineti MC, et al. TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnol J. 2008;6:477–485. doi: 10.1111/j.1467-7652.2008.00341.x.
  • Jiao Y, Burke J, Chopra R, et al. A sorghum mutant resource as an efficient platform for gene discovery in grasses. Plant Cell. 2016;28:1551–1562. doi: 10.1105/tpc.16.00373.
  • Upadhyaya P, Tyagi K, Sarma S, et al. Natural variation in folate levels among tomato (Solanum lycopersicum) accessions. Food Chem. 2017;217:610–619. doi: 10.1016/j.foodchem.2016.09.031.
  • Xia Y, Ning Z, Bai G, et al. Allelic variations of a light harvesting chlorophyll A/B-binding protein gene (Lhcb1) associated with agronomic traits in barley. PLoS One. 2012;7:e37573. doi: 10.1371/journal.pone.0037573.
  • Bajaj D, Srivastava R, Nath M, et al. EcoTILLING-based association mapping efficiently delineates functionally relevant natural allelic variants of candidate genes governing agronomic traits in chickpea. Front Plant Sci. 2016;7:1–9. doi: 10.3389/fpls.2016.00450.
  • Mejlhede N, Kyjovska Z, Backes G, et al. EcoTILLING for the identification of allelic variation in the powdery mildew resistance genes mlo and Mla of barley. Plant Breed. 2006;125:461–467. doi: 10.1111/j.1439-0523.2006.01226.x.
  • Nieto C, Piron F, Dalmais M, et al. EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol. 2007;7:34. doi: 10.1186/1471-2229-7-34.
  • Ibiza VP, Cañizares J, Nuez F. EcoTILLING in Capsicum species: searching for new virus resistances. BMC Genomics. 2010;11:631. doi: 10.1186/1471-2164-11-631.
  • M J, Mie A, N M, et al. Efficient discovery of single-nucleotide variations in Cochliobolus sativus vegetative compatibility groups by Ecotilling. J Plant Biochem Physiol. 2018;06:1–5. doi: 10.4172/2329-9029.1000211.
  • Cseri A, Cserháti M, von Korff M, et al. Allele mining and haplotype discovery in barley candidate genes for drought tolerance. Euphytica. 2011;181:341–356. doi: 10.1007/s10681-011-0445-7.
  • Frerichmann SLM, Kirchhoff M, Müller AE, et al. EcoTILLING in Beta vulgaris reveals polymorphisms in the FLC-like gene BvFL1that are associated with annuality and winter hardiness. BMC Plant Biol. 2013;13:52. doi: 10.1186/1471-2229-13-52.
  • Wang G-X, Tan M-K, Rakshit S, et al. Discovery of single-nucleotide mutations in acetolactate synthase genes by Ecotilling. Pestic Biochem Physiol. 2007;88:143–148. doi: 10.1016/j.pestbp.2006.10.006.
  • Hoshino T, Watanabe S, Takagi Y, et al. A novel GmFAD3-2a mutant allele developed through TILLING reduces α-linolenic acid content in soybean seed oil. Breed Sci. 2014;64:371–377. doi: 10.1270/jsbbs.64.371.
  • Dierking EC, Bilyeu KD. New sources of soybean seed meal and oil composition traits identified through TILLING. BMC Plant Biol. 2009;9:89. doi: 10.1186/1471-2229-9-89.
  • Knoll JE, Ramos ML, Zeng Y, et al. TILLING for allergen reduction and improvement of quality traits in peanut (Arachis hypogaea L.). BMC Plant Biol. 2011;11:81. doi: 10.1186/1471-2229-11-81.
  • Zeng Y-D, Sun J-L, Bu S-H, et al. EcoTILLING revealed SNPs in GhSus genes that are associated with fiber- and seed-related traits in upland cotton. Sci Rep. 2016;6:29250. doi: 10.1038/srep29250.
  • Negrão S, Almadanim C, Pires I, et al. Use of EcoTILLING to identify natural allelic variants of rice candidate genes involved in salinity tolerance. Plant Genet Res. 2011;9:300–304. 2011/05/25. doi: 10.1017/S1479262111000566.
  • Marko D, El-Shershaby A, Carriero F, et al. Identification and characterization of a thermotolerant TILLING allele of heat shock binding protein 1 in tomato. Genes. 2019;10:516. doi: 10.3390/genes10070516.
  • Yu S, Liao F, Wang F, et al. Identification of rice transcription factors associated with drought tolerance using the Ecotilling method. PLoS One. 2012;7:e30765. doi: 10.1371/journal.pone.0030765.
  • Borrill P, Harrington SA, Simmonds J, et al. Identification of transcription factors regulating senescence in wheat through gene regulatory network modelling. Plant Physiol. 2019;180:1740–1755. doi: 10.1104/pp.19.00380.
  • Cerri MR, Frances L, Kelner A, et al. The symbiosis-related ERN transcription factors act in concert to coordinate rhizobial host root infection. Plant Physiol. 2016;171:1037–1054. doi: 10.1104/pp.16.00230.
  • Gilchrist E, Haughn G. Reverse genetics techniques: engineering loss and gain of gene function in plants. Brief Funct Genomics. 2010;9:103–110. doi: 10.1093/bfgp/elp059.
  • Wang W, Simmonds J, Pan Q, et al. Gene editing and mutagenesis reveal inter-cultivar differences and additivity in the contribution of TaGW2 homoeologues to grain size and weight in wheat. Theor Appl Genet. 2018;131:2463–2475. doi: 10.1007/s00122-018-3166-7.

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