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Application of CRISPR/Cas9-mediated gene editing for the development of herbicide-resistant plants

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Abstract

Herbicide resistance is one of the most important traits for plant biotechnology, which is widely used to improve agricultural efficiency by controlling weeds and also used as a selectable marker during genetic engineering by the transformation. For these reasons, new technologies for conferring herbicide resistance to plants are continuously developing, in which CRISPR/Cas9-mediated gene editing methods enable precise modifications of DNA sequences and offer a great promise for the improvement of crops. Here, we review recent advances in developing herbicide-resistant plants by the CRISPR/Cas9-mediated gene editing technology, targeting on endogenous genes such as acetolactate synthase (ALS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), cellulose synthase A catalytic subunit 3 (CESA3), and splicing factor 3B subunit 1 (SF3B1). In addition, we also introduce possible candidate genes to develop herbicide-resistant plants by generating loss-of-function mutations using the CRISPR/Cas9 system.

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References

  • Adli M (2018) The CRISPR tool kit for genome editing and beyond. Nat Commun 9:1911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bernasconi P, Woodworth AR, Rosen BA, Subramanian MV, Siehl DL (1995) A naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase. J Biol Chem 270:17381–17385

    Article  CAS  PubMed  Google Scholar 

  • Butler NM, Baltes NJ, Voytas DF, Douches DS (2016) Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front Plant Sci 7:1045

    Article  PubMed  PubMed Central  Google Scholar 

  • Butt H, Eid A, Momin AA, Bazin J, Crespi M, Arold ST, Mahfouz MM (2019) CRISPR directed evolution of the spliceosome for resistance to splicing inhibitors. Genome Biol 20:73

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen K, Wang Y, Zhang R, Zhang H, Gao C (2019) CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol 70:667–697

    Article  CAS  PubMed  Google Scholar 

  • Chong CK, Choi JD (2000) Amino acid residues conferring herbicide tolerance in tobacco acetolactate synthase. Biochem Biophys Res Commun 279:462–467

    Article  CAS  PubMed  Google Scholar 

  • Cui K, Shoemaker SP (2018) Public perception of genetically-modified (GM) food: a nationwide Chinese consumer study. NPJ Sci Food 2:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Delye C, Jasieniuk M, Le Corre V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649–658

    Article  CAS  PubMed  Google Scholar 

  • Dong Y, Ng E, Lu J, Fenwick T, Tao Y, Bertain S, Sandoval M, Bermudez E, Hou Z, Patten P, Lassner M, Siehl D (2019) Desensitizing plant EPSP synthase to glyphosate: optimized global sequence context accommodates a glycine-to-alanine change in the active site. J Biol Chem 294:716–725

    Article  CAS  PubMed  Google Scholar 

  • Dreesen R, Capt A, Oberdoerfer R, Coats I, Pallett KE (2018) Characterization and safety evaluation of HPPD W336, a modified 4-hydroxyphenylpyruvate dioxygenase protein, and the impact of its expression on plant metabolism in herbicide-tolerant MST-FGO72-2 soybean. Regul Toxicol Pharmacol 97:170–185

    Article  CAS  PubMed  Google Scholar 

  • Duke SO (2015) Perspectives on transgenic, herbicide-resistant crops in the United States almost 20 years after introduction. Pest Manag Sci 71:652–657

    Article  CAS  PubMed  Google Scholar 

  • Duke SO, Powles SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325

    Article  CAS  PubMed  Google Scholar 

  • Endo M, Toki S (2013) Creation of herbicide-tolerant crops by gene targeting. J Pestic Sci 38:49–59

    Article  CAS  Google Scholar 

  • Fartyal D, Agarwal A, James D, Borphukan B, Ram B, Sheri V, Yadav R, Manna M, Varakumar P, Achary VMM, Reddy MK (2018) Co-expression of P173S mutant rice EPSPS and igrA genes results in higher glyphosate tolerance in transgenic rice. Front Plant Sci 9:144

    Article  PubMed  PubMed Central  Google Scholar 

  • Funke T, Han H, Healy-Fried ML, Fischer M, Schonbrunn E (2006) Molecular basis for the herbicide resistance of Roundup Ready crops. Proc Natl Acad Sci USA 103:13010–13015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia MD, Nouwens A, Lonhienne TG, Guddat LW (2017) Comprehensive understanding of acetohydroxyacid synthase inhibition by different herbicide families. Proc Natl Acad Sci USA 114:E1091–E1100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2017) Programmable base editing of AT to GC in genomic DNA without DNA cleavage. Nature 551:464–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gherekhloo J, Fernandez-Moreno PT, Alcantara-de la Cruz R, Sanchez-Gonzalez E, Cruz-Hipolito HE, Dominguez-Valenzuela JA, De Prado R (2017) Pro-106-Ser mutation and EPSPS overexpression acting together simultaneously in glyphosate-resistant goosegrass (Eleusine indica). Sci Rep 7:6702

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Godfray HCJ (2014) The challenge of feeding 9–10 billion people equitably and sustainably. J Agric Sci 152:S2–S8

    Article  Google Scholar 

  • Godfray HC, 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 

  • Green JM (2007) Review of glyphosate and ALS-inhibiting herbicide crop resistance and resistant weed management. Weed Technol 21:547–558

    Article  CAS  Google Scholar 

  • Hattori J, Brown D, Mourad G, Labbe H, Ouellet T, Sunohara G, Rutledge R, King J, Miki B (1995) An acetohydroxy acid synthase mutant reveals a single-site involved in multiple herbicide resistance. Mol Gen Genet 246:419–425

    Article  CAS  PubMed  Google Scholar 

  • Hawkes TR, Langford MP, Viner R, Blain RE, Callaghan FM, Mackay EA, Hogg BV, Singh S, Dale RP (2019) Characterization of 4-hydroxyphenylpyruvate dioxygenases, inhibition by herbicides and engineering for herbicide tolerance in crops. Pest Biochem Physiol 156:9–28

    Article  CAS  Google Scholar 

  • Heap I, Duke SO (2018) Overview of glyphosate-resistant weeds worldwide. Pest Manag Sci 74:1040–1049

    Article  CAS  PubMed  Google Scholar 

  • Herouet-Guicheney C, Rouquie D, Freyssinet M, Currier T, Martone A, Zhou J, Bates EE, Ferullo JM, Hendrickx K, Rouan D (2009) Safety evaluation of the double mutant 5-enol pyruvylshikimate-3-phosphate synthase (2mEPSPS) from maize that confers tolerance to glyphosate herbicide in transgenic plants. Regul Toxicol Pharmacol 54:143–153

    Article  CAS  PubMed  Google Scholar 

  • Hu Z, Vanderhaeghen R, Cools T, Wang Y, De Clercq I, Leroux O, Nguyen L, Belt K, Millar AH, Audenaert D, Hilson P, Small I, Mouille G, Vernhettes S, Van Breusegem F, Whelan J, Hofte H, De Veylder L (2016) Mitochondrial defects confer tolerance against cellulose deficiency. Plant Cell 28:2276–2290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu ZB, Zhang T, Rombaut D, Decaestecker W, Xing AM, D'Haeyer S, Hofer R, Vercauteren I, Karimi M, Jacobs T, De Veylder L (2019) Genome editing-based engineering of CESA3 dual cellulose-inhibitor-resistant plants. Plant Physiol 180:827–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A, Boyher A, Starker CG, Bart R, Voytas DF, Taylor NJ (2018) Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol J 16:1275–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito H, Gray WM (2006) A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol 142:63–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaganathan D, Ramasamy K, Sellamuthu G, Jayabalan S, Venkataraman G (2018) CRISPR for crop improvement: an update review. Front Plant Sci 9:985

    Article  PubMed  PubMed Central  Google Scholar 

  • Jang G, Joung YH (2019) CRISPR/Cas-mediated genome editing for crop improvement: current applications and future prospects. Plant Biotechnol Rep 13:1–10

    Article  Google Scholar 

  • Kang BC, Yun JY, Kim ST, Shin Y, Ryu J, Choi M, Woo JW, Kim JS (2018) Precision genome engineering through adenine base editing in plants. Nat Plants 4:427–431

    Article  CAS  PubMed  Google Scholar 

  • Kaundun SS (2014) Resistance to acetyl-CoA carboxylase-inhibiting herbicides. Pest Manag Sci 70:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Kolkman JM, Slabaugh MB, Bruniard JM, Berry S, Bushman BS, Olungu C, Maes N, Abratti G, Zambelli A, Miller JF, Leon A, Knapp SJ (2004) Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower. Theor Appl Genet 109:1147–1159

    Article  CAS  PubMed  Google Scholar 

  • Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer CM, Launis KL, Traber MG, Ward DP (2014) Vitamin E levels in soybean (Glycine max (L.) Merr.) expressing a p-hydroxyphenylpyruvate gene from oat (Avena sativa L.). J Agric Food Chem 62:3453–3457

    Article  CAS  PubMed  Google Scholar 

  • Lee KY, Townsend J, Tepperman J, Black M, Chui CF, Mazur B, Dunsmuir P, Bedbrook J (1988) The molecular basis of sulfonylurea herbicide resistance in tobacco. EMBO J 7:1241–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Last RL (1996) The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol 110:51–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Zhao J, Rose AB, Schmidt R, Last RL (1995) Arabidopsis phosphoribosylanthranilate isomerase: molecular genetic analysis of triplicate tryptophan pathway genes. Plant Cell 7:447–461

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Barclay I, Jose K, Stefanova K, Appels R (2008) A mutation at the Ala122 position of acetohydroxyacid synthase (AHAS) located on chromosome 6D of wheat: improved resistance to imidazolinone and a faster assay for marker assisted selection. Mol Breed 22:217–225

    Article  CAS  Google Scholar 

  • Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM (2015) Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169:960–970

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li J, Meng XB, Zong Y, Chen KL, Zhang HW, Liu JX, Li JY, Gao CX (2016) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2:16139

    Article  CAS  PubMed  Google Scholar 

  • Li S, Li J, He Y, Xu M, Zhang J, Du W, Zhao Y, Xia L (2019) Precise gene replacement in rice by RNA transcript-templated homologous recombination. Nat Biotechnol 37:445–450

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Li Y, Wang X (2016) Acetohydroxyacid synthases: evolution, structure, and function. Appl Microbiol Biotechnol 100:8633–8649

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Zhu Q, Chen Y, Liu YG (2016) CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9:961–974

    Article  CAS  PubMed  Google Scholar 

  • Matringe M, Sailland A, Pelissier B, Rolland A, Zink O (2005) p-Hydroxyphenylpyruvate dioxygenase inhibitor-resistant plants. Pest Manag Sci 61:269–276

    Article  CAS  PubMed  Google Scholar 

  • Metje-Sprink J, Menz J, Modrzejewski D, Sprink T (2018) DNA-free genome editing: past, present and future. Front Plant Sci 9:1957

    Article  PubMed  Google Scholar 

  • Moran GR (2005) 4-Hydroxyphenylpyruvate dioxygenase. Arch Biochem Biophys 433:117–128

    Article  CAS  PubMed  Google Scholar 

  • Napier JA, Haslam RP, Tsalavouta M, Sayanova O (2019) The challenges of delivering genetically modified crops with nutritional enhancement traits. Nat Plants 5:563–567

    Article  PubMed  Google Scholar 

  • Ndikuryayo F, Moosavi B, Yang WC, Yang GF (2017) 4-Hydroxyphenylpyruvate dioxygenase inhibitors: from chemical biology to agrochemicals. J Agric Food Chem 65:8523–8537

    Article  CAS  PubMed  Google Scholar 

  • Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M, Tabata M, Mochizuki M, Miyabe A, Araki M, Hara KY, Shimatani Z, Kondo A (2016) Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:aaf8729

    Article  PubMed  CAS  Google Scholar 

  • Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A gamma-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortega JL, Rajapakse W, Bagga S, Apodaca K, Lucero Y, Sengupta-Gopalan C (2018) An intragenic approach to confer glyphosate resistance in chile (Capsicum annuum) by introducing an in vitro mutagenized chile EPSPS gene encoding for a glyphosate resistant EPSPS protein. PLoS ONE 13:e0194666

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ostlie M, Haley SD, Anderson V, Shaner D, Manmathan H, Beil C, Westra P (2015) Development and characterization of mutant winter wheat (Triticum aestivum L.) accessions resistant to the herbicide quizalofop. Theor Appl Genet 128:343–351

    Article  CAS  PubMed  Google Scholar 

  • Padgette SR, Kolacz KH, Delannay X, Re DB, Lavallee BJ, Tinius CN, Rhodes WK, Otero YI, Barry GF, Eichholtz DA, Peschke VM, Nida DL, Taylor NB, Kishore GM (1995) Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci 35:1451–1461

    Article  CAS  Google Scholar 

  • Pollegioni L, Schonbrunn E, Siehl D (2011) Molecular basis of glyphosate resistance-different approaches through protein engineering. FEBS J 278:2753–2766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powles SB, Yu Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347

    Article  CAS  PubMed  Google Scholar 

  • Powles SB, Lorraine-Colwill DF, Dellow JJ, Preston C (1998) Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed Sci 46:604–607

    Article  CAS  Google Scholar 

  • Pozniak CJ, Birk IT, O'Donoughue LS, Menard C, Hucl PJ, Singh BK (2004) Physiological and molecular characterization of mutation-derived imidazolinone resistance in spring wheat. Crop Sci 44:1434–1443

    Article  CAS  Google Scholar 

  • Prado JR, Segers G, Voelker T, Carson D, Dobert R, Phillips J, Cook K, Cornejo C, Monken J, Grapes L, Reynolds T, Martino-Catt S (2014) Genetically engineered crops: from idea to product. Annu Rev Plant Biol 65:769–790

    Article  CAS  PubMed  Google Scholar 

  • Preston C, Wakelin AM, Dolman FC, Bostamam Y, Boutsalis P (2009) A decade of glyphosate-resistant Lolium around the world: mechanisms, genes, fitness, and agronomic management. Weed Sci 57:435–441

    Article  CAS  Google Scholar 

  • Quareshy M, Prusinska J, Li J, Napier R (2018) A cheminformatics review of auxins as herbicides. J Exp Bot 69:265–275

    Article  CAS  PubMed  Google Scholar 

  • Rajguru SN, Burgos NR, Shivrain VK, Stewart JM (2005) Mutations in the red rice ALS gene associated with resistance to imazethapyr. Weed Sci 53:567–577

    Article  CAS  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  CAS  PubMed  Google Scholar 

  • Sala C, Bulos M, Echarte M, Whitt S, Ascenzi R (2008) Molecular and biochemical characterization of an induced mutation conferring imidazolinone resistance in sunflower. Theor Appl Genet 118:105–112

    Article  CAS  PubMed  Google Scholar 

  • Sauer NJ, Narvaez-Vasquez J, Mozoruk J, Miller RB, Warburg ZJ, Woodward MJ, Mihiret YA, Lincoln TA, Segami RE, Sanders SL, Walker KA, Beetham PR, Schopke CR, Gocal GF (2016) Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol 170:1917–1928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schonbrunn E, Eschenburg S, Shuttleworth WA, Schloss JV, Amrhein N, Evans JN, Kabsch W (2001) Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail. Proc Natl Acad Sci USA 98:1376–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber KJ, Austin RS, Gong Y, Zhang J, Fung P, Wang PW, Guttman DS, Desveaux D (2012) Forward chemical genetic screens in Arabidopsis identify genes that influence sensitivity to the phytotoxic compound sulfamethoxazole. BMC Plant Biol 12:226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedeek KEM, Mahas A, Mahfouz M (2019) Plant genome engineering for targeted improvement of crop traits. Front Plant Sci 10:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K, Ezura H, Nishida K, Ariizumi T, Kondo A (2017) Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35:441–443

    Article  CAS  PubMed  Google Scholar 

  • Shimizu M, Goto M, Hanai M, Shimizu T, Izawa N, Kanamoto H, Tomizawa K, Yokota A, Kobayashi H (2008) Selectable tolerance to herbicides by mutated acetolactate synthase genes integrated into the chloroplast genome of tobacco. Plant Physiol 147:1976–1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siehl DL, Subramanian MV, Walters EW, Blanding JH, Niderman T, Weinmann C (1997) Evaluating anthranilate synthase as a herbicide target. Weed Sci 45:628–633

    Article  CAS  Google Scholar 

  • Siehl DL, Tao Y, Albert H, Dong Y, Heckert M, Madrigal A, Lincoln-Cabatu B, Lu J, Fenwick T, Bermudez E, Sandoval M, Horn C, Green JM, Hale T, Pagano P, Clark J, Udranszky IA, Rizzo N, Bourett T, Howard RJ, Johnson DH, Vogt M, Akinsola G, Castle LA (2014) Broad 4-hydroxyphenylpyruvate dioxygenase inhibitor herbicide tolerance in soybean with an optimized enzyme and expression cassette. Plant Physiol 166:1162–1176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soltani N, Dille JA, Burke IC, Everman WJ, VanGessel MJ, Davis VM, Sikkema PH (2016) Potential corn yield losses from weeds in North America. Weed Technol 30:979–984

    Article  Google Scholar 

  • Song YL (2014) Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-d) as an herbicide. J Integr Plant Biol 56:106–113

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9:628–631

    Article  CAS  PubMed  Google Scholar 

  • Sundstrom J, Albihn A, Boqvist S, Ljungvall K, Marstorp H, Martiin C, Nyberg K, Vagsholm I, Yuen J, Magnusson U (2014) Future threats to agricultural food production posed by environmental degradation, climate change, and animal and plant diseases - a risk analysis in three economic and climate settings. Food Secur 6:201–215

    Article  Google Scholar 

  • 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 169:931–945

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabatabaei I, Dal Bosco C, Bednarska M, Ruf S, Meurer J, Bock R (2019) A highly efficient sulfadiazine selection system for the generation of transgenic plants and algae. Plant Biotechnol J 17:638–649

    Article  CAS  PubMed  Google Scholar 

  • Tan S, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61:246–257

    Article  CAS  PubMed  Google Scholar 

  • Tian SW, Jiang LJ, Cui XX, Zhang J, Guo SG, Li MY, Zhang HY, Ren Y, Gong GY, Zong M, Liu F, Chen QJ, Xu Y (2018) Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep 37:1353–1356

    Article  CAS  PubMed  Google Scholar 

  • Veillet F, Perrot L, Chauvin L, Kermarrec MP, Guyon-Debast A, Chauvin JE, Nogue F, Mazier M (2019) Transgene-free genome editing in tomato and potato plants using Agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci 20:402

    Article  PubMed Central  CAS  Google Scholar 

  • Walter KL, Strachan SD, Ferry NM, Albert HH, Castle LA, Sebastian SA (2014) Molecular and phenotypic characterization of Als1 and Als2 mutations conferring tolerance to acetolactate synthase herbicides in soybean. Pest Manag Sci 70:1831–1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White AD, Graham MA, Owen MDK (2003) Isolation of acetolactate synthase homologs in common sunflower. Weed Sci 51:845–853

    Article  CAS  Google Scholar 

  • Wright TR, Bascomb NF, Sturner SF, Penner D (1998) Biochemical mechanism and molecular basis for ALS-inhibiting herbicide resistance in sugarbeet (Beta vulgaris) somatic cell selections. Weed Sci 46:13–23

    Article  CAS  Google Scholar 

  • Yin K, Gao C, Qiu JL (2017) Progress and prospects in plant genome editing. Nat Plants 3:17107

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Powles SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Han H, Vila-Aiub MM, Powles SB (2010) AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61:3925–3934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Ahmad-Hamdani MS, Han H, Christoffers MJ, Powles SB (2013) Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110:220–231

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Massel K, Godwin ID, Gao C (2018) Applications and potential of genome editing in crop improvement. Genome Biol 19:210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Liu J, Chai Z, Chen S, Bai Y, Zong Y, Chen K, Li J, Jiang L, Gao C (2019a) Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing. Nat Plants 5:480–485

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Malzahn AA, Sretenovic S, Qi Y (2019b) The emerging and uncultivated potential of CRISPR technology in plant science. Nat Plants 5:778–794

    Article  PubMed  Google Scholar 

  • Zhou M, Xu H, Wei X, Ye Z, Wei L, Gong W, Wang Y, Zhu Z (2006) Identification of a glyphosate-resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy. Plant Physiol 140:184–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Liu W, Zhang Y, Liu KK (2007) Action mechanisms of acetolactate synthase-inhibiting herbicides. Pest Biochem Physiol 89:89–96

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dong-Ju Jeon for taking pictures of the oxp1 mutant. This research was supported by Next-Generation BioGreen 21 Program from Rural Development Administration, Republic of Korea (Grant no. PJ01325301), and in part by Basic Science Research Program through the National Research Foundation of Korea (NRF) (Grant no. 2017R1A2B4010349).

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  1. Department of Biotechnology and Kumho Life Science Laboratory, Chonnam National University, Gwangju, 61186, Republic of Korea

    Yun-Jeong Han & Jeong-Il Kim

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Han, YJ., Kim, JI. Application of CRISPR/Cas9-mediated gene editing for the development of herbicide-resistant plants. Plant Biotechnol Rep 13, 447–457 (2019). https://doi.org/10.1007/s11816-019-00575-8

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