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

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.

[1]  Camilo Cornejo,et al.  Genetically engineered crops: from idea to product. , 2014, Annual review of plant biology.

[2]  Yanpeng Wang,et al.  CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture. , 2019, Annual review of plant biology.

[3]  Y. Zong,et al.  Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9 , 2016, Nature Plants.

[4]  G. Moran.  4-Hydroxyphenylpyruvate dioxygenase. , 2005, Archives of biochemistry and biophysics.

[5]  Naoko Ohkama-Ohtsu,et al.  A γ-Glutamyl Transpeptidase-Independent Pathway of Glutathione Catabolism to Glutamate via 5-Oxoproline in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[6]  D. Shaner,et al.  Imidazolinone-tolerant crops: history, current status and future. , 2005, Pest management science.

[7]  Simon Sretenovic,et al.  The emerging and uncultivated potential of CRISPR technology in plant science , 2019, Nature Plants.

[8]  S. Powles,et al.  Resistance to AHAS inhibitor herbicides: current understanding. , 2014, Pest management science.

[9]  T. Niderman,et al.  Evaluating anthranilate synthase as a herbicide target , 1997, Weed Science.

[10]  Zhongsen Li,et al.  Cas9-Guide RNA Directed Genome Editing in Soybean[OPEN] , 2015, Plant Physiology.

[11]  Yi Ren,et al.  Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing , 2018, Plant Cell Reports.

[12]  J. Stewart,et al.  Mutations in the red rice ALS gene associated with resistance to imazethapyr , 2005, Weed Science.

[13]  R. Bock,et al.  A highly efficient sulfadiazine selection system for the generation of transgenic plants and algae , 2018, Plant Biotechnology Journal.

[14]  S. Powles,et al.  AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth , 2010, Journal of experimental botany.

[15]  Beum-Chang Kang,et al.  Precision genome engineering through adenine base editing in plants , 2018, Nature Plants.

[16]  M. Crespi,et al.  CRISPR directed evolution of the spliceosome for resistance to splicing inhibitors , 2019, Genome Biology.

[17]  Robert Ascenzi,et al.  Molecular and biochemical characterization of an induced mutation conferring imidazolinone resistance in sunflower , 2008, Theoretical and Applied Genetics.

[18]  Xiaoyuan Wang,et al.  Acetohydroxyacid synthases: evolution, structure, and function , 2016, Applied Microbiology and Biotechnology.

[19]  W. Gray,et al.  A Gain-of-Function Mutation in the Arabidopsis Pleiotropic Drug Resistance Transporter PDR9 Confers Resistance to Auxinic Herbicides1 , 2006, Plant Physiology.

[20]  Jerry M. Green.  Review of Glyphosate and Als-inhibiting Herbicide Crop Resistance and Resistant Weed Management , 2007, Weed Technology.

[21]  L. De Veylder,et al.  Genome Editing-Based Engineering of CESA3 Dual Cellulose-Inhibitor-Resistant Plants1[OPEN] , 2019, Plant Physiology.

[22]  S. Toki,et al.  Creation of herbicide-tolerant crops by gene targeting , 2013 .

[23]  Yong-song Zhang,et al.  Action mechanisms of acetolactate synthase-inhibiting herbicides ☆ , 2007 .

[24]  M. Traber,et al.  Vitamin E levels in soybean (Glycine max (L.) Merr.) expressing a p-hydroxyphenylpyruvate gene from oat (Avena sativa L.). , 2014, Journal of agricultural and food chemistry.

[25]  S. Robinson,et al.  Food Security: The Challenge of Feeding 9 Billion People , 2010, Science.

[26]  P. Sikkema,et al.  Potential Corn Yield Losses from Weeds in North America , 2016, Weed Technology.

[27]  Ganesh M. Kishore,et al.  Development, identification, and characterization of a glyphosate-tolerant soybean line , 1995 .

[28]  David R. Liu,et al.  Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage , 2016, Nature.

[29]  T. Sprink,et al.  DNA-Free Genome Editing: Past, Present and Future , 2019, Front. Plant Sci..

[30]  H. Godfray,et al.  The challenge of feeding 9–10 billion people equitably and sustainably , 2013, The Journal of Agricultural Science.

[31]  Wenchao Yang,et al.  4-Hydroxyphenylpyruvate Dioxygenase Inhibitors: From Chemical Biology to Agrochemicals. , 2017, Journal of agricultural and food chemistry.

[32]  M. Healy-Fried,et al.  Molecular basis for the herbicide resistance of Roundup Ready crops , 2006, Proceedings of the National Academy of Sciences.

[33]  T. A. Lincoln,et al.  Oligonucleotide-Mediated Genome Editing Provides Precision and Function to Engineered Nucleases and Antibiotics in Plants[OPEN] , 2016, Plant Physiology.

[34]  R. Appels,et al.  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 , 2008, Molecular Breeding.

[35]  F. Nogué,et al.  Transgene-Free Genome Editing in Tomato and Potato Plants Using Agrobacterium-Mediated Delivery of a CRISPR/Cas9 Cytidine Base Editor , 2019, International journal of molecular sciences.

[36]  A. Millar,et al.  Mitochondrial Defects Confer Tolerance against Cellulose Deficiency , 2016, Plant Cell.

[37]  Corinne Herouet-Guicheney,et al.  Safety evaluation of the double mutant 5-enol pyruvylshikimate-3-phosphate synthase (2mEPSPS) from maize that confers tolerance to glyphosate herbicide in transgenic plants. , 2009, Regulatory toxicology and pharmacology : RTP.

[38]  N. Rizzo,et al.  Broad 4-Hydroxyphenylpyruvate Dioxygenase Inhibitor Herbicide Tolerance in Soybean with an Optimized Enzyme and Expression Cassette[W][OPEN] , 2014, Plant Physiology.

[39]  D. Voytas,et al.  Geminivirus-Mediated Genome Editing in Potato (Solanum tuberosum L.) Using Sequence-Specific Nucleases , 2016, Front. Plant Sci..

[40]  W. Kabsch,et al.  Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Yaling Song.  Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. , 2014, Journal of integrative plant biology.

[42]  J. Qiu,et al.  Progress and prospects in plant genome editing , 2017, Nature Plants.

[43]  C. Preston,et al.  A Decade of Glyphosate-Resistant Lolium around the World: Mechanisms, Genes, Fitness, and Agronomic Management , 2009, Weed Science.

[44]  S. Knapp,et al.  Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower , 2004, Theoretical and Applied Genetics.

[45]  Loredano Pollegioni,et al.  Molecular basis of glyphosate resistance – different approaches through protein engineering , 2011, The FEBS journal.

[46]  J. Ortega,et al.  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 , 2018, PloS one.

[47]  Jun Yu Li,et al.  A cheminformatics review of auxins as herbicides. , 2018, Journal of experimental botany.

[48]  Liping Wei,et al.  Identification of a Glyphosate-Resistant Mutant of Rice 5-Enolpyruvylshikimate 3-Phosphate Synthase Using a Directed Evolution Strategy1[W][OA] , 2005, Plant Physiology.

[49]  S. Powles,et al.  Evolution in action: plants resistant to herbicides. , 2010, Annual review of plant biology.

[50]  R. Rutledge,et al.  An acetohydroxy acid synthase mutant reveals a single site involved in multiple herbicide resistance , 1995, Molecular and General Genetics MGG.

[51]  L. Guddat,et al.  Comprehensive understanding of acetohydroxyacid synthase inhibition by different herbicide families , 2017, Proceedings of the National Academy of Sciences.

[52]  A. Rose,et al.  Arabidopsis phosphoribosylanthranilate isomerase: molecular genetic analysis of triplicate tryptophan pathway genes. , 1995, The Plant cell.

[53]  M. Jasieniuk,et al.  Deciphering the evolution of herbicide resistance in weeds. , 2013, Trends in genetics : TIG.

[54]  Joshua K Young,et al.  Targeted Mutagenesis, Precise Gene Editing, and Site-Specific Gene Insertion in Maize Using Cas9 and Guide RNA[OPEN] , 2015, Plant Physiology.

[55]  Ahmed Mahas,et al.  Plant Genome Engineering for Targeted Improvement of Crop Traits , 2019, Front. Plant Sci..

[56]  E. Bermudez,et al.  Desensitizing plant EPSP synthase to glyphosate: Optimized global sequence context accommodates a glycine-to-alanine change in the active site , 2018, The Journal of Biological Chemistry.

[57]  Yunde Zhao,et al.  Precise gene replacement in rice by RNA transcript-templated homologous recombination , 2019, Nature Biotechnology.

[58]  M. Graham,et al.  Isolation of acetolactate synthase homologs in common sunflower , 2003, Weed Science.

[59]  S. Shoemaker,et al.  Public perception of genetically-modified (GM) food: A Nationwide Chinese Consumer Study , 2018, npj Science of Food.

[60]  H. Albert,et al.  Molecular and phenotypic characterization of Als1 and Als2 mutations conferring tolerance to acetolactate synthase herbicides in soybean , 2014, Pest management science.

[61]  Mazhar Adli,et al.  The CRISPR tool kit for genome editing and beyond , 2018, Nature Communications.

[62]  S. Kaundun.  Resistance to acetyl-CoA carboxylase-inhibiting herbicides. , 2014, Pest management science.

[63]  M. Subramanian,et al.  A Naturally Occurring Point Mutation Confers Broad Range Tolerance to Herbicides That Target Acetolactate Synthase (*) , 1995, The Journal of Biological Chemistry.

[64]  S. Powles,et al.  Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species , 2012, Heredity.

[65]  D. Guttman,et al.  Forward chemical genetic screens in Arabidopsis identify genes that influence sensitivity to the phytotoxic compound sulfamethoxazole , 2012, BMC Plant Biology.

[66]  D. Shaner,et al.  Development and characterization of mutant winter wheat (Triticum aestivum L.) accessions resistant to the herbicide quizalofop , 2014, Theoretical and Applied Genetics.

[67]  G. Venkataraman,et al.  CRISPR for Crop Improvement: An Update Review , 2018, Front. Plant Sci..

[68]  Yunde Zhao,et al.  Engineering Herbicide-Resistant Rice Plants through CRISPR/Cas9-Mediated Homologous Recombination of Acetolactate Synthase. , 2016, Molecular plant.

[69]  A. Kondo,et al.  Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems , 2016, Science.

[70]  D. Voytas,et al.  Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava , 2018, Plant biotechnology journal.

[71]  Kathleen Y. Lee,et al.  The molecular basis of sulfonylurea herbicide resistance in tobacco , 1988, The EMBO journal.

[72]  M. K. Reddy,et al.  Co-expression of P173S Mutant Rice EPSPS and igrA Genes Results in Higher Glyphosate Tolerance in Transgenic Rice , 2018, Front. Plant Sci..

[73]  C. Chong,et al.  Amino acid residues conferring herbicide tolerance in tobacco acetolactate synthase. , 2000, Biochemical and biophysical research communications.

[74]  Stephen O Duke,et al.  Perspectives on transgenic, herbicide-resistant crops in the United States almost 20 years after introduction. , 2015, Pest management science.

[75]  Xingliang Ma,et al.  CRISPR/Cas9 Platforms for Genome Editing in Plants: Developments and Applications. , 2016, Molecular plant.

[76]  M. Shimizu,et al.  Selectable Tolerance to Herbicides by Mutated Acetolactate Synthase Genes Integrated into the Chloroplast Genome of Tobacco1[OA] , 2008, Plant Physiology.

[77]  S. Duke,et al.  Glyphosate: a once-in-a-century herbicide. , 2008, Pest management science.

[78]  A. Capt,et al.  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‐FGϕ72–2 soybean , 2018, Regulatory toxicology and pharmacology : RTP.

[79]  C. Pozniak,et al.  Physiological and Molecular Characterization of Mutation‐Derived Imidazolinone Resistance in Spring Wheat , 2004 .

[80]  R. Last,et al.  The Arabidopsis thaliana trp5 Mutant Has a Feedback-Resistant Anthranilate Synthase and Elevated Soluble Tryptophan , 1996, Plant physiology.

[81]  N. Bascomb,et al.  Biochemical mechanism and molecular basis for ALS-inhibiting herbicide resistance in sugarbeet (Beta vulgaris) somatic cell selections , 1998 .

[82]  T. Hawkes,et al.  Characterization of 4-hydroxyphenylpyruvate dioxygenases, inhibition by herbicides and engineering for herbicide tolerance in crops. , 2019, Pesticide biochemistry and physiology.

[83]  J. Napier,et al.  The challenges of delivering genetically modified crops with nutritional enhancement traits , 2019, Nature Plants.

[84]  J. Jacquot,et al.  The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. , 2008, Annual review of plant biology.

[85]  S. Duke,et al.  Overview of glyphosate-resistant weeds worldwide. , 2018, Pest management science.

[86]  Christopher Preston,et al.  Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia , 1998, Weed Science.

[87]  Akihiko Kondo,et al.  Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion , 2017, Nature Biotechnology.

[88]  Yuan Zong,et al.  Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing , 2019, Nature Plants.

[89]  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 , 2014, Food Security.

[90]  Caixia Gao,et al.  Applications and potential of genome editing in crop improvement , 2018, Genome Biology.

[91]  R. de Prado,et al.  Pro-106-Ser mutation and EPSPS overexpression acting together simultaneously in glyphosate-resistant goosegrass (Eleusine indica) , 2017, Scientific Reports.

[92]  M. Matringe,et al.  p-Hydroxyphenylpyruvate dioxygenase inhibitor-resistant plants. , 2005, Pest management science.

[93]  Y. Joung,et al.  CRISPR/Cas-mediated genome editing for crop improvement: current applications and future prospects , 2018, Plant Biotechnology Reports.