CRISPR/Cas9: A Practical Approach in Date Palm Genome Editing

The genetic modifications through breeding of crop plants have long been used to improve the yield and quality. However, precise genome editing (GE) could be a very useful supplementary tool for improvement of crop plants by targeted genome modifications. Various GE techniques including ZFNs (zinc finger nucleases), TALENs (transcription activator-like effector nucleases), and most recently clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 (CRISPR-associated protein 9)-based approaches have been successfully employed for various crop plants including fruit trees. CRISPR/Cas9-based approaches hold great potential in GE due to their simplicity, competency, and versatility over other GE techniques. However, to the best of our knowledge no such genetic improvement has ever been developed in date palm—an important fruit crop in Oasis agriculture. The applications of CRISPR/Cas9 can be a challenging task in date palm GE due to its large and complex genome, high rate of heterozygosity and outcrossing, in vitro regeneration and screening of mutants, high frequency of single-nucleotide polymorphism in the genome and ultimately genetic instability. In this review, we addressed the potential application of CRISPR/Cas9-based approaches in date palm GE to improve the sustainable date palm production. The availability of the date palm whole genome sequence has made it feasible to use CRISPR/Cas9 GE approach for genetic improvement in this species. Moreover, the future prospects of GE application in date palm are also addressed in this review.

[1]  G. Russo,et al.  De novo genome sequencing and comparative stage-specific transcriptomic analysis of Dirofilaria repens. , 2019, International journal for parasitology.

[2]  J. Flowers,et al.  Genomic Insights into Date Palm Origins , 2018, Genes.

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

[4]  Shouling Xu,et al.  CRISPR‐S: an active interference element for a rapid and inexpensive selection of genome‐edited, transgene‐free rice plants , 2017, Plant biotechnology journal.

[5]  Yunbo Luo,et al.  Multiplexed CRISPR/Cas9‐mediated metabolic engineering of γ‐aminobutyric acid levels in Solanum lycopersicum , 2017, Plant biotechnology journal.

[6]  Yang Bai,et al.  Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat , 2017, The Plant journal : for cell and molecular biology.

[7]  Jian‐Kang Zhu,et al.  Multiplex Gene Editing in Rice Using the CRISPR-Cpf1 System. , 2017, Molecular plant.

[8]  Y. Nishizawa,et al.  The receptor-like cytoplasmic kinase BSR1 mediates chitin-induced defense signaling in rice cells , 2017, Bioscience, biotechnology, and biochemistry.

[9]  N. Tuteja,et al.  Development of CRISPR/Cas9 mediated virus resistance in agriculturally important crops , 2017, Bioengineered.

[10]  Xiuping Zou,et al.  Engineering canker‐resistant plants through CRISPR/Cas9‐targeted editing of the susceptibility gene CsLOB1 promoter in citrus , 2017, Plant biotechnology journal.

[11]  Chun Wang,et al.  A simple and efficient method for CRISPR/Cas9-induced mutant screening. , 2017, Journal of genetics and genomics = Yi chuan xue bao.

[12]  C. Jung,et al.  CRISPR-Cas9 Targeted Mutagenesis Leads to Simultaneous Modification of Different Homoeologous Gene Copies in Polyploid Oilseed Rape (Brassica napus)1 , 2017, Plant Physiology.

[13]  Congmao Wang,et al.  Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion , 2017, Scientific Reports.

[14]  N. Smargiasso,et al.  Inactivation of the β(1,2)-xylosyltransferase and the α(1,3)-fucosyltransferase genes in Nicotiana tabacum BY-2 Cells by a Multiplex CRISPR/Cas9 Strategy Results in Glycoproteins without Plant-Specific Glycans , 2017, Front. Plant Sci..

[15]  Jian Li,et al.  Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice , 2017, Science China Life Sciences.

[16]  Kabin Xie,et al.  Discovery of rice essential genes by characterizing a CRISPR‐edited mutation of closely related rice MAP kinase genes , 2017, The Plant journal : for cell and molecular biology.

[17]  F. Dong,et al.  Polycistronic tRNA and CRISPR guide-RNA enables highly efficient multiplexed genome engineering in human cells. , 2017, Biochemical and biophysical research communications.

[18]  R. Viola,et al.  DNA-Free Genetically Edited Grapevine and Apple Protoplast Using CRISPR/Cas9 Ribonucleoproteins , 2016, Front. Plant Sci..

[19]  M. Nishimura,et al.  Genome-Wide Assessment of Efficiency and Specificity in CRISPR/Cas9 Mediated Multiple Site Targeting in Arabidopsis , 2016, PloS one.

[20]  V. Walbot,et al.  An Agrobacterium‐delivered CRISPR/Cas9 system for high‐frequency targeted mutagenesis in maize , 2016, Plant biotechnology journal.

[21]  Yi Zhang,et al.  Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA , 2016, Nature Communications.

[22]  Yuriko Osakabe,et al.  Efficient Genome Editing in Apple Using a CRISPR/Cas9 system , 2016, Scientific Reports.

[23]  Wei Zhang,et al.  High-efficiency CRISPR/Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize , 2016, BMC Biotechnology.

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

[25]  Morad M. Mokhtar,et al.  Genic and Intergenic SSR Database Generation, SNPs Determination and Pathway Annotations, in Date Palm (Phoenix dactylifera L.) , 2016, PloS one.

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

[27]  Jian‐Kang Zhu,et al.  A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis , 2016, Plant Cell Reports.

[28]  Lingling Chen,et al.  Recent Advances in Genome Editing Using CRISPR/Cas9 , 2016, Front. Plant Sci..

[29]  A. Arzani,et al.  Smart Engineering of Genetic Resources for Enhanced Salinity Tolerance in Crop Plants , 2016 .

[30]  V. Orbović,et al.  Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4:dCsLOB1.3 infection. , 2016, Plant biotechnology journal.

[31]  J. Keith Joung,et al.  731. High-Fidelity CRISPR-Cas9 Nucleases with No Detectable Genome-Wide Off-Target Effects , 2016 .

[32]  Yaoguang Liu,et al.  Enhanced Rice Blast Resistance by CRISPR/Cas9-Targeted Mutagenesis of the ERF Transcription Factor Gene OsERF922 , 2016, PloS one.

[33]  C. N. Kanchiswamy DNA-free genome editing methods for targeted crop improvement , 2016, Plant Cell Reports.

[34]  N. Tuteja,et al.  The CRISPR/Cas Genome-Editing Tool: Application in Improvement of Crops , 2016, Front. Plant Sci..

[35]  M. Shafiq,et al.  CRISPR/Cas9: A Tool to Circumscribe Cotton Leaf Curl Disease , 2016, Front. Plant Sci..

[36]  Jun Yan,et al.  Corrigendum: Differential developmental requirement and peripheral regulation for dermal Vγ4 and Vγ6T17 cells in health and inflammation , 2016, Nature Communications.

[37]  Masafumi Mikami,et al.  Precision Targeted Mutagenesis via Cas9 Paired Nickases in Rice , 2016, Plant & cell physiology.

[38]  Ciaran M Lee,et al.  Nuclease Target Site Selection for Maximizing On-target Activity and Minimizing Off-target Effects in Genome Editing , 2016, Molecular therapy : the journal of the American Society of Gene Therapy.

[39]  David A. Scott,et al.  Rationally engineered Cas9 nucleases with improved specificity , 2015, Science.

[40]  Abdelouahhab Zaid,et al.  Whole genome re-sequencing of date palms yields insights into diversification of a fruit tree crop , 2015, Nature Communications.

[41]  C. Grubb,et al.  In silico characterization and Molecular modeling of double-strand break repair protein MRE11 from Phoenix dactylifera v deglet nour , 2015, Theoretical Biology and Medical Modelling.

[42]  R. Sunkar,et al.  A genome-wide identification of the miRNAome in response to salinity stress in date palm (Phoenix dactylifera L.) , 2015, Front. Plant Sci..

[43]  C. Barbas,et al.  Efficient delivery of nuclease proteins for genome editing in human stem cells and primary cells , 2015, Nature Protocols.

[44]  Soon Il Kwon,et al.  DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins , 2015, Nature Biotechnology.

[45]  Masayuki Endo,et al.  Corrigendum: Efficient amplification of self-gelling polypod-like structured DNA by rolling circle amplification and enzymatic digestion , 2015, Scientific Reports.

[46]  Chung-Jui Tsai,et al.  Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. , 2015, The New phytologist.

[47]  Chung-Jui Tsai,et al.  CRISPRing into the woods , 2015, GM crops & food.

[48]  B. Tyler,et al.  Efficient Disruption and Replacement of an Effector Gene in the Oomycete Phytophthora sojae using CRISPR/Cas9 , 2015, bioRxiv.

[49]  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.

[50]  Wei Liu,et al.  A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in Monocot and Dicot Plants. , 2015, Molecular plant.

[51]  Daniel F Voytas,et al.  Efficient Virus-Mediated Genome Editing in Plants Using the CRISPR/Cas9 System. , 2015, Molecular plant.

[52]  Chaofeng Li,et al.  Efficient CRISPR/Cas9-mediated Targeted Mutagenesis in Populus in the First Generation , 2015, Scientific Reports.

[53]  Martin J. Aryee,et al.  Engineered CRISPR-Cas9 nucleases with altered PAM specificities , 2015, Nature.

[54]  A. Al-Malki,et al.  Proteome Analysis for Understanding Abiotic Stress (Salinity and Drought) Tolerance in Date Palm (Phoenix dactylifera L.) , 2015, International journal of genomics.

[55]  J. Malek,et al.  A Genome-Wide Survey of Date Palm Cultivars Supports Two Major Subpopulations in Phoenix dactylifera , 2015, G3: Genes, Genomes, Genetics.

[56]  Robert J. Schmitz,et al.  Targeted genome modifications in soybean with CRISPR/Cas9 , 2015, BMC Biotechnology.

[57]  Kabin Xie,et al.  Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system , 2015, Proceedings of the National Academy of Sciences.

[58]  Wanfei Liu,et al.  Profiling microRNA expression during multi-staged date palm (Phoenix dactylifera L.) fruit development. , 2015, Genomics.

[59]  H. Puchta,et al.  The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. , 2014, The Plant journal : for cell and molecular biology.

[60]  Z. Lippman,et al.  Efficient Gene Editing in Tomato in the First Generation Using the Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-Associated9 System1 , 2014, Plant Physiology.

[61]  A. Mousavi,et al.  Genetic transformation of date palm (Phoenix dactylifera L. cv. ‘Estamaran’) via particle bombardment , 2014, Molecular Biology Reports.

[62]  M. Ikawa,et al.  Single-step generation of rabbits carrying a targeted allele of the tyrosinase gene using CRISPR/Cas9 , 2014, Experimental animals.

[63]  M. Spalding,et al.  Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice , 2014, Nucleic acids research.

[64]  Jian‐Kang Zhu,et al.  The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. , 2014, Plant biotechnology journal.

[65]  H. Puchta,et al.  Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. , 2014, The Plant journal : for cell and molecular biology.

[66]  Talal A. Zari,et al.  Whole Mitochondrial and Plastid Genome SNP Analysis of Nine Date Palm Cultivars Reveals Plastid Heteroplasmy and Close Phylogenetic Relationships among Cultivars , 2014, PloS one.

[67]  Nian Wang,et al.  Targeted Genome Editing of Sweet Orange Using Cas9/sgRNA , 2014, PloS one.

[68]  Botao Zhang,et al.  Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis , 2014, Proceedings of the National Academy of Sciences.

[69]  J. Keith Joung,et al.  Improving CRISPR-Cas nuclease specificity using truncated guide RNAs , 2014, Nature Biotechnology.

[70]  Jin-Soo Kim,et al.  Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases , 2014, Genome research.

[71]  Michael G Murray,et al.  Trait stacking via targeted genome editing. , 2013, Plant biotechnology journal.

[72]  Kabin Xie,et al.  RNA-guided genome editing in plants using a CRISPR-Cas system. , 2013, Molecular plant.

[73]  Guodong Huang,et al.  Site-specific gene targeting using transcription activator-like effector (TALE)-based nuclease in Brassica oleracea. , 2013, Journal of integrative plant biology.

[74]  Jian‐Kang Zhu,et al.  Application of the CRISPR-Cas system for efficient genome engineering in plants. , 2013, Molecular plant.

[75]  Luke A. Gilbert,et al.  CRISPR interference (CRISPRi) for sequence-specific control of gene expression , 2013, Nature Protocols.

[76]  R. Tuli,et al.  RNA-Guided Genome Editing for Target Gene Mutations in Wheat , 2013, G3: Genes, Genomes, Genetics.

[77]  S. Kamoun,et al.  Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system , 2013, Plant Methods.

[78]  D. Voytas,et al.  Targeted Mutagenesis of Arabidopsis thaliana Using Engineered TAL Effector Nucleases , 2013, G3: Genes, Genomes, Genetics.

[79]  Jeffry D. Sander,et al.  Targeted Deletion and Inversion of Tandemly Arrayed Genes in Arabidopsis thaliana Using Zinc Finger Nucleases , 2013, G3: Genes, Genomes, Genetics.

[80]  Xin Zhang,et al.  Targeted mutagenesis in rice using CRISPR-Cas system , 2013, Cell Research.

[81]  David A. Scott,et al.  Double Nicking by RNA-Guided CRISPR Cas9 for Enhanced Genome Editing Specificity , 2013, Cell.

[82]  Bing Yang,et al.  Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice , 2013, Nucleic acids research.

[83]  David R. Liu,et al.  High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity , 2013, Nature Biotechnology.

[84]  Zilong Ma,et al.  Characterization and Evolution of Conserved MicroRNA through Duplication Events in Date Palm (Phoenix dactylifera) , 2013, PloS one.

[85]  Qiang Lin,et al.  Genome sequence of the date palm Phoenix dactylifera L , 2013, Nature Communications.

[86]  Jun Li,et al.  Targeted genome modification of crop plants using a CRISPR-Cas system , 2013, Nature Biotechnology.

[87]  G. Church,et al.  CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering , 2013, Nature Biotechnology.

[88]  George M. Church,et al.  Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9 , 2013, Nature Biotechnology.

[89]  Eli J. Fine,et al.  DNA targeting specificity of RNA-guided Cas9 nucleases , 2013, Nature Biotechnology.

[90]  Luke A. Gilbert,et al.  CRISPR-Mediated Modular RNA-Guided Regulation of Transcription in Eukaryotes , 2013, Cell.

[91]  J. Keith Joung,et al.  High frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells , 2013, Nature Biotechnology.

[92]  D. Voytas,et al.  TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants , 2013, Plant Molecular Biology.

[93]  M. Rowicka,et al.  Nucleotide-resolution DNA double-strand breaks mapping by next-generation sequencing , 2013, Nature Methods.

[94]  Luke A. Gilbert,et al.  Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression , 2013, Cell.

[95]  P. Hooykaas,et al.  ZFN-mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation , 2012, Plant biotechnology journal.

[96]  G. He,et al.  Identification and characterization of gene-based SSR markers in date palm (Phoenix dactylifera L.) , 2012, BMC Plant Biology.

[97]  Daniel F. Voytas,et al.  Transcription Activator-Like Effector Nucleases Enable Efficient Plant Genome Engineering1[W][OA] , 2012, Plant Physiology.

[98]  Daniel F. Voytas,et al.  Simple Methods for Generating and Detecting Locus-Specific Mutations Induced with TALENs in the Zebrafish Genome , 2012, PLoS genetics.

[99]  A. Al-Sadi,et al.  Characterization and pathogenicity of fungi and oomycetes associated with root diseases of date palms in Oman , 2012 .

[100]  Wanfei Liu,et al.  Large-scale collection and annotation of gene models for date palm (Phoenix dactylifera, L.) , 2012, Plant Molecular Biology.

[101]  Asifullah Khan,et al.  The Chloroplast Genome Sequence of Date Palm (Phoenix dactylifera L. cv. ‘Aseel’) , 2012, Plant Molecular Biology Reporter.

[102]  Songnian Hu,et al.  A Complete Sequence and Transcriptomic Analyses of Date Palm (Phoenix dactylifera L.) Mitochondrial Genome , 2012, PloS one.

[103]  Zejian Guo,et al.  The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance , 2012, Journal of experimental botany.

[104]  Songnian Hu,et al.  High-throughput sequencing-based gene profiling on multi-staged fruit development of date palm (Phoenix dactylifera, L.) , 2012, Plant Molecular Biology.

[105]  Lin Fang,et al.  Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes , 2011, Nature Biotechnology.

[106]  S. Santoni,et al.  Biogeography of the date palm (Phoenix dactylifera L., Arecaceae): insights on the origin and on the structure of modern diversity , 2011 .

[107]  Yuge Li,et al.  A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes , 2011, Plant Methods.

[108]  Fabienne Bourgis,et al.  Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning , 2011, Proceedings of the National Academy of Sciences.

[109]  Jeremy D. DeBarry,et al.  De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera) , 2011, Nature Biotechnology.

[110]  J. Petrini,et al.  The MRE11 complex: starting from the ends , 2011, Nature Reviews Molecular Cell Biology.

[111]  Jun Yu,et al.  The Complete Chloroplast Genome Sequence of Date Palm (Phoenix dactylifera L.) , 2010, PloS one.

[112]  Y. Doyon,et al.  Precise genome modification in the crop species Zea mays using zinc-finger nucleases , 2009, Nature.

[113]  Ronnie J Winfrey,et al.  High frequency modification of plant genes using engineered zinc finger nucleases , 2009, Nature.

[114]  Jong Kyoung Kim,et al.  Arabidopsis Nuclear-Encoded Plastid Transit Peptides Contain Multiple Sequence Subgroups with Distinctive Chloroplast-Targeting Sequence Motifs[W] , 2008, The Plant Cell Online.

[115]  S. Udupa,et al.  Assessment of AFLP-based Genetic Relationships among Date Palm (Phoenix dactylifera L.) Varieties of Iraq , 2005 .

[116]  H. Puchta,et al.  Efficient Repair of Genomic Double-Strand Breaks by Homologous Recombination between Directly Repeated Sequences in the Plant Genome Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001727. , 2002, The Plant Cell Online.

[117]  Levi G. Lowder,et al.  Multiplexed Transcriptional Activation or Repression in Plants Using CRISPR-dCas9-Based Systems. , 2017, Methods in molecular biology.

[118]  Rainer Fischer,et al.  The CRISPR/Cas9 system for plant genome editing and beyond. , 2015, Biotechnology advances.

[119]  S. Jain,et al.  Date Palm Genetic Resources and Utilization , 2015, Springer Netherlands.

[120]  Q. Xia,et al.  CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum , 2014, Plant Molecular Biology.

[121]  Justin E. Anderson,et al.  Targeted mutagenesis for functional analysis of gene duplication in legumes. , 2013, Methods in molecular biology.

[122]  D. Voytas,et al.  Targeted mutagenesis in Arabidopsis using zinc-finger nucleases. , 2011, Methods in molecular biology.

[123]  S. Jain,et al.  Date Palm Biotechnology , 2011 .

[124]  M. Hanafy,et al.  Towards Sex Determination of Date Palm , 2011 .

[125]  H. Azadi,et al.  Enhancing date palm processing, marketing and pest control through organic culture. , 2008 .

[126]  K. A. Malik,et al.  Phage phiC31 integrase: a new tool in plastid genome engineering. , 2005, Trends in plant science.

[127]  M. Ferry,et al.  The Red Palm Weevil in the Mediterranean Area , 2002 .