A multi-purpose toolkit to enable advanced genome engineering in plants

Cermak, Tomas; Curtin, Shaun J.; Gil-Humanes, Javier; Čegan, Radim; Kono, Thomas J.  Y.; Konečná, Eva; Belanto, Joseph J.; Starker, Colby G.; Mathre, Jade W.; Greenstein, Rebecca L.; Voytas, Daniel F.

doi:10.1105/tpc.16.00922

Title: A multi-purpose toolkit to enable advanced genome engineering in plants

Abstract

Here, we report a comprehensive toolkit that enables targeted, specific modification of monocot and dicot genomes using a variety of genome engineering approaches. Our reagents, based on Transcription Activator-Like Effector Nucleases TALENs and the Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9 system, are systematized for fast, modular cloning and accommodate diverse regulatory sequences to drive reagent expression. Vectors are optimized to create either single or multiple gene knockouts and large chromosomal deletions. Moreover, integration of geminivirus-based vectors enables precise gene editing through homologous recombination. Regulation of transcription is also possible. A web-based tool streamlines vector selection and construction. One advantage of our platform is the use of the Csy-type (CRISPR system yersinia) ribonuclease 4 Csy4 and tRNA processing enzymes to simultaneously express multiple guide RNAs (gRNAs). For example, we demonstrate targeted deletions in up to six genes by expressing twelve gRNAs from a single transcript. Csy4 and tRNA expression systems are almost twice as effective in inducing mutations as gRNAs expressed from individual RNA polymerase III promoters. Mutagenesis can be further enhanced 2.5-fold by incorporating the Trex2 exonuclease. Finally, we demonstrate that Cas9 nickases induce gene targeting at frequencies comparable to native Cas9 when they are delivered on geminivirus replicons.more »« less

Authors:

Cermak, Tomas ^[1]; Curtin, Shaun J. ^[2]; Gil-Humanes, Javier ^[3]; Čegan, Radim ^[4]; Kono, Thomas J. Y. ^[5]; Konečná, Eva ^[1]; Belanto, Joseph J. ^[1]; Starker, Colby G. ^[1]; Mathre, Jade W. ^[1]; Greenstein, Rebecca L. ^[1]; Voytas, Daniel F. ^[1]

Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Genetics, Cell Biology & Development and Center for Genome Engineering
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Pathology and Dept. of Agronomy & Plant Genetics; USDA-ARS Cereal Disease Lab., St. Paul, MN (United States)
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Genetics, Cell Biology & Development and Center for Genome Engineering; Calyxt Inc., New Brighton, MN (United States)
Inst. of Biophysics of Chinese Academy of Sciences, Brno (Czech Republic). Dept. of Plant Developmental Genetics
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Agronomy & Plant Genetics

Publication Date:: Thu May 18 00:00:00 EDT 2017

Research Org.:: Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

OSTI Identifier:: 1423880

Grant/Contract Number:: sc0008769; IOS-1339209; IOS-1444511; IOS-1237993

Resource Type:: Accepted Manuscript

Journal Name:: The Plant Cell

Additional Journal Information:: Journal Volume: 29; Journal Issue: 6; Journal ID: ISSN 1040-4651

Publisher:: American Society of Plant Biologists

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Cermak, Tomas, Curtin, Shaun J., Gil-Humanes, Javier, Čegan, Radim, Kono, Thomas J.  Y., Konečná, Eva, Belanto, Joseph J., Starker, Colby G., Mathre, Jade W., Greenstein, Rebecca L., and Voytas, Daniel F. A multi-purpose toolkit to enable advanced genome engineering in plants.  United States: N. p., 2017. 
Web.  doi:10.1105/tpc.16.00922.

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                    Cermak, Tomas, Curtin, Shaun J., Gil-Humanes, Javier, Čegan, Radim, Kono, Thomas J.  Y., Konečná, Eva, Belanto, Joseph J., Starker, Colby G., Mathre, Jade W., Greenstein, Rebecca L., & Voytas, Daniel F. A multi-purpose toolkit to enable advanced genome engineering in plants.  United States.  https://doi.org/10.1105/tpc.16.00922

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                    Cermak, Tomas, Curtin, Shaun J., Gil-Humanes, Javier, Čegan, Radim, Kono, Thomas J.  Y., Konečná, Eva, Belanto, Joseph J., Starker, Colby G., Mathre, Jade W., Greenstein, Rebecca L., and Voytas, Daniel F. Thu .  
"A multi-purpose toolkit to enable advanced genome engineering in plants".  United States.  https://doi.org/10.1105/tpc.16.00922.  https://www.osti.gov/servlets/purl/1423880.

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@article{osti_1423880,

  title        = {A multi-purpose toolkit to enable advanced genome engineering in plants},

  author       = {Cermak, Tomas and Curtin, Shaun J. and Gil-Humanes, Javier and Čegan, Radim and Kono, Thomas J.  Y. and Konečná, Eva and Belanto, Joseph J. and Starker, Colby G. and Mathre, Jade W. and Greenstein, Rebecca L. and Voytas, Daniel F.},

  abstractNote = {Here, we report a comprehensive toolkit that enables targeted, specific modification of monocot and dicot genomes using a variety of genome engineering approaches. Our reagents, based on Transcription Activator-Like Effector Nucleases TALENs and the Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9 system, are systematized for fast, modular cloning and accommodate diverse regulatory sequences to drive reagent expression. Vectors are optimized to create either single or multiple gene knockouts and large chromosomal deletions. Moreover, integration of geminivirus-based vectors enables precise gene editing through homologous recombination. Regulation of transcription is also possible. A web-based tool streamlines vector selection and construction. One advantage of our platform is the use of the Csy-type (CRISPR system yersinia) ribonuclease 4 Csy4 and tRNA processing enzymes to simultaneously express multiple guide RNAs (gRNAs). For example, we demonstrate targeted deletions in up to six genes by expressing twelve gRNAs from a single transcript. Csy4 and tRNA expression systems are almost twice as effective in inducing mutations as gRNAs expressed from individual RNA polymerase III promoters. Mutagenesis can be further enhanced 2.5-fold by incorporating the Trex2 exonuclease. Finally, we demonstrate that Cas9 nickases induce gene targeting at frequencies comparable to native Cas9 when they are delivered on geminivirus replicons. The reagents have been successfully validated in tomato (Solanum lycopersicum), tobacco (Nicotiana tabacum), Medicago truncatula, wheat (Triticum aestivum), and barley (Hordeum vulgare).},

  doi          = {10.1105/tpc.16.00922},

  journal      = {The Plant Cell},

  number       = 6,

  volume       = 29,

  place        = {United States},

  year         = {Thu May 18 00:00:00 EDT 2017},

  month        = {Thu May 18 00:00:00 EDT 2017}

}

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DOI: 10.1371/journal.pone.0207723

A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

Oh, Youngbin; Lee, Bora; Kim, Hyeonjin
DOI: 10.21203/rs.2.21279/v4

Setaria Comes of Age: Meeting Report on the Second International Setaria Genetics Conference
journal, September 2017

Zhu, Chuanmei; Yang, Jiani; Shyu, Christine
Frontiers in Plant Science, Vol. 8
DOI: 10.3389/fpls.2017.01562

Editing Citrus Genome via SaCas9/sgRNA System
journal, December 2017

Jia, Hongge; Xu, Jin; Orbović, Vladimir
Frontiers in Plant Science, Vol. 8
DOI: 10.3389/fpls.2017.02135

Efficient Multiplex Genome Editing Induces Precise, and Self-Ligated Type Mutations in Tomato Plants
journal, July 2018

Hashimoto, Ryosuke; Ueta, Risa; Abe, Chihiro
Frontiers in Plant Science, Vol. 9
DOI: 10.3389/fpls.2018.00916

Modifications in Organic Acid Profiles During Fruit Development and Ripening: Correlation or Causation?
journal, November 2018

Batista-Silva, Willian; Nascimento, Vitor L.; Medeiros, David B.
Frontiers in Plant Science, Vol. 9
DOI: 10.3389/fpls.2018.01689

Bidirectional Promoter-Based CRISPR-Cas9 Systems for Plant Genome Editing
journal, September 2019

Ren, Qiurong; Zhong, Zhaohui; Wang, Yan
Frontiers in Plant Science, Vol. 10
DOI: 10.3389/fpls.2019.01173

Genome Editing in Plants: Exploration of Technological Advancements and Challenges
journal, November 2019

Vats, Sanskriti; Kumawat, Surbhi; Kumar, Virender
Cells, Vol. 8, Issue 11
DOI: 10.3390/cells8111386

A Review of the Interactions between Wheat and Wheat Pathogens: Zymoseptoria tritici, Fusarium spp. and Parastagonospora nodorum
journal, April 2018

Duba, Adrian; Goriewa-Duba, Klaudia; Wachowska, Urszula
International Journal of Molecular Sciences, Vol. 19, Issue 4
DOI: 10.3390/ijms19041138

CRISPRMatch: An Automatic Calculation and Visualization Tool for High-throughput CRISPR Genome-editing Data Analysis
journal, January 2018

You, Qi; Zhong, Zhaohui; Ren, Qiurong
International Journal of Biological Sciences, Vol. 14, Issue 8
DOI: 10.7150/ijbs.24581

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Title: A multi-purpose toolkit to enable advanced genome engineering in plants

Abstract

Citation Formats

Considerations in adapting CRISPR/Cas9 in nongenetic model plant systems journal, January 2020

Protein expression and gene editing in monocots using foxtail mosaic virus vectors journal, November 2019

Editing the Medicago truncatula Genome: Targeted Mutagenesis Using the CRISPR-Cas9 Reagent book, January 2018

Genome Editing in Potato with CRISPR/Cas9 book, January 2019

CRISPR/Cas9-Mediated Gene Editing Tool and Fathomless Genetic and Metabolic Engineering Applications in Plants book, January 2018

Advanced genetic tools enable synthetic biology in the oleaginous microalgae Nannochloropsis sp. journal, March 2018

CRISPR/Cas-mediated gene targeting in plants: finally a turn for the better for homologous recombination journal, January 2019

Optimized Cas9 expression systems for highly efficient Arabidopsis genome editing facilitate isolation of complex alleles in a single generation journal, February 2019

CRISPR-based genome editing in wheat: a comprehensive review and future prospects journal, April 2019

Shortened snRNA promoters for efficient CRISPR/Cas-based multiplex genome editing in monocot plants journal, January 2020

CRISPR/Cas-mediated genome editing for crop improvement: current applications and future prospects journal, December 2018

From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas journal, August 2019

A novel CRISPR/Cas9 system for efficiently generating Cas9-free multiplex mutants in Arabidopsis journal, November 2019

Efficient expression of multiple guide RNAs for CRISPR/Cas genome editing journal, January 2020

De novo domestication of wild tomato using genome editing journal, October 2018

Domestication of wild tomato is accelerated by genome editing journal, October 2018

A method for the production and expedient screening of CRISPR/Cas9-mediated non-transgenic mutant plants journal, March 2018

Rapid and user-friendly open-source CRISPR/Cas9 system for single- or multi-site editing of tomato genome journal, January 2019

Plant gene editing through de novo induction of meristems journal, December 2019

Prime genome editing in rice and wheat journal, March 2020

Targeted mutagenesis in wheat microspores using CRISPR/Cas9 journal, April 2018

Facilitating gene editing in potato: a Single-Nucleotide Polymorphism (SNP) map of the Solanum tuberosum L. cv. Desiree genome journal, February 2020

BCL6 corepressor contributes to Th17 cell formation by inhibiting Th17 fate suppressors journal, May 2019

Does co-transcriptional regulation of alternative splicing mediate plant stress responses? journal, February 2019

Gene editing in plants: progress and challenges journal, January 2019

YSL3-mediated copper distribution is required for fertility, grain yield, and size in Brachypodium posted_content, December 2019

Translocation and duplication from CRISPR-Cas9 editing in Arabidopsis thaliana posted_content, August 2018

CRISPR-TSKO facilitates efficient cell type-, tissue-, or organ-specific mutagenesis in Arabidopsis posted_content, June 2019

Building customizable auto-luminescent luciferase-based reporters in plants posted_content, October 2019

Genomic Outcomes of Haploid Induction Crosses in Potato (Solanum tuberosum L.) posted_content, October 2019

Using CRISPR/Cas9 genome editing in tomato to create a gibberellin-responsive dominant dwarf DELLA allele journal, June 2018

Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing journal, January 2019

Efficient induction of heritable inversions in plant genomes using the CRISPR /Cas system journal, April 2019

Genetic Modification for Wheat Improvement: From Transgenesis to Genome Editing journal, March 2019

How to start your monocot CRISPR/Cas project: plasmid design, efficiency detection, and offspring analysis journal, February 2020

Integration, abundance, and transmission of mutations and transgenes in a series of CRISPR/Cas9 soybean lines journal, February 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering journal, March 2020

SWISS: multiplexed orthogonal genome editing in plants with a Cas9 nickase and engineered CRISPR RNA scaffolds journal, June 2020

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis journal, January 2019

CBF-dependent and CBF-independent regulatory pathways contribute to the differences in freezing tolerance and cold-regulated gene expression of two Arabidopsis ecotypes locally adapted to sites in Sweden and Italy journal, December 2018

A Dual sgRNA Approach for Functional Genomics in Arabidopsis thaliana journal, June 2018

Genomic Outcomes of Haploid Induction Crosses in Potato ( Solanum tuberosum L.) journal, December 2019

Efficient Multiplex Genome Editing Induces Precise, and Self-Ligated Type Mutations in Tomato Plants journal, July 2018

Modifications in Organic Acid Profiles During Fruit Development and Ripening: Correlation or Causation? journal, November 2018

Bidirectional Promoter-Based CRISPR-Cas9 Systems for Plant Genome Editing journal, September 2019

Genome Editing in Plants: Exploration of Technological Advancements and Challenges journal, November 2019

Cas Endonuclease Technology—A Quantum Leap in the Advancement of Barley and Wheat Genetic Engineering journal, May 2019

TCR Affinity Biases Th Cell Differentiation by Regulating CD25, Eef1e1, and Gbp2 journal, March 2019

Optimized Cas9 expression systems for highly efficient Arabidopsis genome editing facilitate isolation of complex alleles in a single generation posted_content, August 2018

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis posted_content, September 2018

A multiplex guide RNA expression system and its efficacy for plant genome engineering posted_content, March 2020

From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas text, January 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering posted_content, March 2020

Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system text, January 2019

Comparison of efficiency and specificity of CRISPR-associated (Cas) nucleases in plants: An expanded toolkit for precision genome engineering journal, February 2019

A multiplex guide RNA expression system and its efficacy for plant genome engineering posted_content, March 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering posted_content, March 2020

Considerations in adapting CRISPR/Cas9 in nongenetic model plant systems journal, January 2020

Protein expression and gene editing in monocots using foxtail mosaic virus vectors journal, November 2019

A method for the production and expedient screening of CRISPR/Cas9-mediated non-transgenic mutant plants journal, March 2018

Rapid and user-friendly open-source CRISPR/Cas9 system for single- or multi-site editing of tomato genome journal, January 2019

CRISPR/Cas9-induced Targeted Mutagenesis and Gene Replacement to Generate Long-shelf Life Tomato Lines journal, September 2017

A unified multi-kingdom Golden Gate cloning platform journal, July 2019

Facilitating gene editing in potato: a Single-Nucleotide Polymorphism (SNP) map of the Solanum tuberosum L. cv. Desiree genome journal, February 2020

BCL6 corepressor contributes to Th17 cell formation by inhibiting Th17 fate suppressors journal, May 2019

Transgenerational CRISPR-Cas9 Activity Facilitates Multiplex Gene Editing in Allopolyploid Wheat journal, February 2018

Does co-transcriptional regulation of alternative splicing mediate plant stress responses? journal, February 2019

In Planta Processing of the SpCas9–gRNA Complex journal, October 2017

Homology-directed repair of a defective glabrous gene in Arabidopsis with Cas9-based gene targeting posted_content, January 2018

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis posted_content, September 2018

CRISPR/Cas9 and TALENs generate heritable mutations for genes involved in small RNA processing of Glycine max and Medicago truncatula journal, December 2017

Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single-cell mutation detection to mutant plant regeneration journal, January 2018

Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus journal, April 2018

Characterization of a semidominant dwarfingPROCERAallele identified in a screen for CRISPR/Cas9-induced suppressors of loss-of-function alleles journal, November 2018

Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing journal, January 2019

Genetic Modification for Wheat Improvement: From Transgenesis to Genome Editing journal, March 2019

How to start your monocot CRISPR/Cas project: plasmid design, efficiency detection, and offspring analysis journal, February 2020

Considerations in adapting CRISPR/Cas9 in nongenetic model plant systems
journal, January 2020

Protein expression and gene editing in monocots using foxtail mosaic virus vectors
journal, November 2019

Editing the Medicago truncatula Genome: Targeted Mutagenesis Using the CRISPR-Cas9 Reagent
book, January 2018

Genome Editing in Potato with CRISPR/Cas9
book, January 2019

CRISPR/Cas9-Mediated Gene Editing Tool and Fathomless Genetic and Metabolic Engineering Applications in Plants
book, January 2018

Advanced genetic tools enable synthetic biology in the oleaginous microalgae Nannochloropsis sp.
journal, March 2018

CRISPR/Cas-mediated gene targeting in plants: finally a turn for the better for homologous recombination
journal, January 2019

Optimized Cas9 expression systems for highly efficient Arabidopsis genome editing facilitate isolation of complex alleles in a single generation
journal, February 2019

CRISPR-based genome editing in wheat: a comprehensive review and future prospects
journal, April 2019

Shortened snRNA promoters for efficient CRISPR/Cas-based multiplex genome editing in monocot plants
journal, January 2020

CRISPR/Cas-mediated genome editing for crop improvement: current applications and future prospects
journal, December 2018

From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas
journal, August 2019

A novel CRISPR/Cas9 system for efficiently generating Cas9-free multiplex mutants in Arabidopsis
journal, November 2019

Efficient expression of multiple guide RNAs for CRISPR/Cas genome editing
journal, January 2020

De novo domestication of wild tomato using genome editing
journal, October 2018

Domestication of wild tomato is accelerated by genome editing
journal, October 2018

A method for the production and expedient screening of CRISPR/Cas9-mediated non-transgenic mutant plants
journal, March 2018

Rapid and user-friendly open-source CRISPR/Cas9 system for single- or multi-site editing of tomato genome
journal, January 2019

Plant gene editing through de novo induction of meristems
journal, December 2019

Prime genome editing in rice and wheat
journal, March 2020

Targeted mutagenesis in wheat microspores using CRISPR/Cas9
journal, April 2018

Facilitating gene editing in potato: a Single-Nucleotide Polymorphism (SNP) map of the Solanum tuberosum L. cv. Desiree genome
journal, February 2020

BCL6 corepressor contributes to Th17 cell formation by inhibiting Th17 fate suppressors
journal, May 2019

Does co-transcriptional regulation of alternative splicing mediate plant stress responses?
journal, February 2019

Gene editing in plants: progress and challenges
journal, January 2019

YSL3-mediated copper distribution is required for fertility, grain yield, and size in Brachypodium
posted_content, December 2019

Translocation and duplication from CRISPR-Cas9 editing in Arabidopsis thaliana
posted_content, August 2018

CRISPR-TSKO facilitates efficient cell type-, tissue-, or organ-specific mutagenesis in Arabidopsis
posted_content, June 2019

Building customizable auto-luminescent luciferase-based reporters in plants
posted_content, October 2019

Genomic Outcomes of Haploid Induction Crosses in Potato (Solanum tuberosum L.)
posted_content, October 2019

Using CRISPR/Cas9 genome editing in tomato to create a gibberellin-responsive dominant dwarf DELLA allele
journal, June 2018

Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing
journal, January 2019

Efficient induction of heritable inversions in plant genomes using the CRISPR /Cas system
journal, April 2019

Genetic Modification for Wheat Improvement: From Transgenesis to Genome Editing
journal, March 2019

How to start your monocot CRISPR/Cas project: plasmid design, efficiency detection, and offspring analysis
journal, February 2020

Integration, abundance, and transmission of mutations and transgenes in a series of CRISPR/Cas9 soybean lines
journal, February 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering
journal, March 2020

SWISS: multiplexed orthogonal genome editing in plants with a Cas9 nickase and engineered CRISPR RNA scaffolds
journal, June 2020

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis
journal, January 2019

CBF-dependent and CBF-independent regulatory pathways contribute to the differences in freezing tolerance and cold-regulated gene expression of two Arabidopsis ecotypes locally adapted to sites in Sweden and Italy
journal, December 2018

A Dual sgRNA Approach for Functional Genomics in Arabidopsis thaliana
journal, June 2018

Genomic Outcomes of Haploid Induction Crosses in Potato ( Solanum tuberosum L.)
journal, December 2019

Efficient Multiplex Genome Editing Induces Precise, and Self-Ligated Type Mutations in Tomato Plants
journal, July 2018

Modifications in Organic Acid Profiles During Fruit Development and Ripening: Correlation or Causation?
journal, November 2018

Bidirectional Promoter-Based CRISPR-Cas9 Systems for Plant Genome Editing
journal, September 2019

Genome Editing in Plants: Exploration of Technological Advancements and Challenges
journal, November 2019

Cas Endonuclease Technology—A Quantum Leap in the Advancement of Barley and Wheat Genetic Engineering
journal, May 2019

TCR Affinity Biases Th Cell Differentiation by Regulating CD25, Eef1e1, and Gbp2
journal, March 2019

Optimized Cas9 expression systems for highly efficient Arabidopsis genome editing facilitate isolation of complex alleles in a single generation
posted_content, August 2018

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis
posted_content, September 2018

A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas
text, January 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system
text, January 2019

Comparison of efficiency and specificity of CRISPR-associated (Cas) nucleases in plants: An expanded toolkit for precision genome engineering
journal, February 2019

A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

Considerations in adapting CRISPR/Cas9 in nongenetic model plant systems
journal, January 2020

Protein expression and gene editing in monocots using foxtail mosaic virus vectors
journal, November 2019

A method for the production and expedient screening of CRISPR/Cas9-mediated non-transgenic mutant plants
journal, March 2018

Rapid and user-friendly open-source CRISPR/Cas9 system for single- or multi-site editing of tomato genome
journal, January 2019

CRISPR/Cas9-induced Targeted Mutagenesis and Gene Replacement to Generate Long-shelf Life Tomato Lines
journal, September 2017

A unified multi-kingdom Golden Gate cloning platform
journal, July 2019

Facilitating gene editing in potato: a Single-Nucleotide Polymorphism (SNP) map of the Solanum tuberosum L. cv. Desiree genome
journal, February 2020

BCL6 corepressor contributes to Th17 cell formation by inhibiting Th17 fate suppressors
journal, May 2019

Transgenerational CRISPR-Cas9 Activity Facilitates Multiplex Gene Editing in Allopolyploid Wheat
journal, February 2018

Does co-transcriptional regulation of alternative splicing mediate plant stress responses?
journal, February 2019

In Planta Processing of the SpCas9–gRNA Complex
journal, October 2017

Homology-directed repair of a defective glabrous gene in Arabidopsis with Cas9-based gene targeting
posted_content, January 2018

Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis
posted_content, September 2018

CRISPR/Cas9 and TALENs generate heritable mutations for genes involved in small RNA processing of Glycine max and Medicago truncatula
journal, December 2017

Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single-cell mutation detection to mutant plant regeneration
journal, January 2018

Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus
journal, April 2018

Characterization of a semidominant dwarfingPROCERAallele identified in a screen for CRISPR/Cas9-induced suppressors of loss-of-function alleles
journal, November 2018

Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing
journal, January 2019

Genetic Modification for Wheat Improvement: From Transgenesis to Genome Editing
journal, March 2019

How to start your monocot CRISPR/Cas project: plasmid design, efficiency detection, and offspring analysis
journal, February 2020

Intron-Based Single Transcript Unit CRISPR Systems for Plant Genome Editing
journal, February 2020

Integration, abundance, and transmission of mutations and transgenes in a series of CRISPR/Cas9 soybean lines
journal, February 2020

Perfectly matched 20-nucleotide guide RNA sequences enable robust genome editing using high-fidelity SpCas9 nucleases
journal, October 2017