Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research

Liu, Degao; Hu, Rongbin; Palla, Kaitlin J.; Tuskan, Gerald A.; Yang, Xiaohan

doi:10.1016/j.pbi.2016.01.007

Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research

Journal Article · Wed Feb 17 23:00:00 EST 2016 · Current Opinion in Plant Biology

DOI:https://doi.org/10.1016/j.pbi.2016.01.007· OSTI ID:1355869

Liu, Degao ^[1]; Hu, Rongbin ^[1]; Palla, Kaitlin J. ^[1]; Tuskan, Gerald A. ^[1]; Yang, Xiaohan ^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

Genome editing with site-specific nucleases has become a powerful tool for functional characterization of plant genes and genetic improvement of agricultural crops. Among the various site-specific nuclease-based technologies available for genome editing, the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated protein 9 (Cas9) systems have shown the greatest potential for rapid and efficient editing of genomes in plant species. Here, this article reviews the current status of application of CRISPR/Cas9 to plant genomics research, with a focus on loss-of-function and gain-of-function analysis of individual genes in the context of perennial plants and the potential application of CRISPR/Cas9 to perturbation of gene expression, as well as identification and analysis of gene modules as part of an accelerated domestication and synthetic biology effort.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; SC0008834

OSTI ID:: 1355869

Alternate ID(s):: OSTI ID: 1352955

Journal Information:: Current Opinion in Plant Biology, Journal Name: Current Opinion in Plant Biology Journal Issue: C Vol. 30; ISSN 1369-5266

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Scaling nitrogen and carbon interactions: what are the consequences of biological buffering? Weston, David J.; Rogers, Alistair; Tschaplinski, Timothy J. Ecology and Evolution, Vol. 5, Issue 14 https://doi.org/10.1002/ece3.1565	journal	June 2015
Transformation of cotton (Gossypium hirsutum L.) by Agrobacterium tumefaciens and regeneration of transgenic plants Firoozabady, Ebrahim; DeBoer, David L.; Merlo, Donald J. Plant Molecular Biology, Vol. 10, Issue 2 https://doi.org/10.1007/BF00016148	journal	January 1987
High efficiency poplar transformation Cseke, Leland J.; Cseke, Sarah Beth; Podila, Gopi K. Plant Cell Reports, Vol. 26, Issue 9 https://doi.org/10.1007/s00299-007-0365-0	journal	May 2007
Efficient Agrobacterium tumefaciens-mediated transformation using embryogenic suspension cultures in sweetpotato, Ipomoea batatas (L.) Lam. Yu, Bo; Zhai, Hong; Wang, Yuping Plant Cell, Tissue and Organ Culture, Vol. 90, Issue 3 https://doi.org/10.1007/s11240-007-9265-9	journal	July 2007
Genetic transformation of citrus protoplasts and regeneration of transgenic plants Vardi, Aliza; Bleichman, Shlomit; Aviv, Dvora Plant Science, Vol. 69, Issue 2 https://doi.org/10.1016/0168-9452(90)90118-8	journal	January 1990
Short-rotation woody crop supply systems in the United States: what do we know and what do we need to know? Tuskan, G. A. Biomass and Bioenergy, Vol. 14, Issue 4 https://doi.org/10.1016/S0961-9534(97)10065-4	journal	April 1998
The CRISPR/Cas9 system for plant genome editing and beyond Bortesi, Luisa; Fischer, Rainer Biotechnology Advances, Vol. 33, Issue 1 https://doi.org/10.1016/j.biotechadv.2014.12.006	journal	January 2015
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression Qi, Lei S.; Larson, Matthew H.; Gilbert, Luke A. Cell, Vol. 152, Issue 5, p. 1173-1183 https://doi.org/10.1016/j.cell.2013.02.022	journal	February 2013
Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System Chen, Baohui; Gilbert, Luke A.; Cimini, Beth A. Cell, Vol. 155, Issue 7 https://doi.org/10.1016/j.cell.2013.12.001	journal	December 2013
Engineering Complex Synthetic Transcriptional Programs with CRISPR RNA Scaffolds Zalatan, Jesse G.; Lee, Michael E.; Almeida, Ricardo Cell, Vol. 160, Issue 1-2 https://doi.org/10.1016/j.cell.2014.11.052	journal	January 2015
A Genome-wide CRISPR Screen in Primary Immune Cells to Dissect Regulatory Networks Parnas, Oren; Jovanovic, Marko; Eisenhaure, Thomas M. Cell, Vol. 162, Issue 3 https://doi.org/10.1016/j.cell.2015.06.059	journal	July 2015
Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota Mimee, Mark; Tucker, Alex C.; Voigt, Christopher A. Cell Systems, Vol. 1, Issue 1 https://doi.org/10.1016/j.cels.2015.06.001	journal	July 2015
CRISPR-Cas9-based Photoactivatable Transcription System Nihongaki, Yuta; Yamamoto, Shun; Kawano, Fuun Chemistry & Biology, Vol. 22, Issue 2 https://doi.org/10.1016/j.chembiol.2014.12.011	journal	February 2015
Gene module level analysis: identification to networks and dynamics Wang, Xuewei; Dalkic, Ertugrul; Wu, Ming Current Opinion in Biotechnology, Vol. 19, Issue 5 https://doi.org/10.1016/j.copbio.2008.07.011	journal	October 2008
Editing plant genomes with CRISPR/Cas9 Belhaj, Khaoula; Chaparro-Garcia, Angela; Kamoun, Sophien Current Opinion in Biotechnology, Vol. 32 https://doi.org/10.1016/j.copbio.2014.11.007	journal	April 2015
A CRISPR/Cas9 Vector System for Tissue-Specific Gene Disruption in Zebrafish Ablain, Julien; Durand, Ellen M.; Yang, Song Developmental Cell, Vol. 32, Issue 6 https://doi.org/10.1016/j.devcel.2015.01.032	journal	March 2015
A modular gene targeting system for sequential transgene stacking in plants Kumar, Sandeep; AlAbed, Diaa; Worden, Andrew Journal of Biotechnology, Vol. 207 https://doi.org/10.1016/j.jbiotec.2015.04.006	journal	August 2015
A Genome-Wide CRISPR Library for High-Throughput Genetic Screening in Drosophila Cells Bassett, Andrew R.; Kong, Lesheng; Liu, Ji-Long Journal of Genetics and Genomics, Vol. 42, Issue 6 https://doi.org/10.1016/j.jgg.2015.03.011	journal	June 2015
CRISPR/Cas9-mediated genome editing and gene replacement in plants: Transitioning from lab to field Schaeffer, Scott M.; Nakata, Paul A. Plant Science, Vol. 240 https://doi.org/10.1016/j.plantsci.2015.09.011	journal	November 2015
Accelerating the domestication of forest trees in a changing world Harfouche, Antoine; Meilan, Richard; Kirst, Matias Trends in Plant Science, Vol. 17, Issue 2 https://doi.org/10.1016/j.tplants.2011.11.005	journal	February 2012
Efficient transient transformation of suspension culture-derived apple protoplasts Maddumage, Ratnasiri; Fung, Raymond M. W.; Weir, Iona Plant Cell, Tissue and Organ Culture, Vol. 70, Issue 1, p. 77-82 https://doi.org/10.1023/A:1016073611902	journal	January 2002
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Fire, Andrew; Xu, SiQun; Montgomery, Mary K. Nature, Vol. 391, Issue 6669 https://doi.org/10.1038/35888	journal	February 1998
The genome of Eucalyptus grandis Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A. Nature, Vol. 510, Issue 7505 https://doi.org/10.1038/nature13308	journal	June 2014
Targeted genome modification of crop plants using a CRISPR-Cas system Shan, Qiwei; Wang, Yanpeng; Li, Jun Nature Biotechnology, Vol. 31, Issue 8 https://doi.org/10.1038/nbt.2650	journal	August 2013
Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9 Li, Jian-Feng; Norville, Julie E.; Aach, John Nature Biotechnology, Vol. 31, Issue 8 https://doi.org/10.1038/nbt.2654	journal	August 2013
Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library Koike-Yusa, Hiroko; Li, Yilong; Tan, E-Pien Nature Biotechnology, Vol. 32, Issue 3 https://doi.org/10.1038/nbt.2800	journal	December 2013
CRISPR-Cas systems for editing, regulating and targeting genomes Sander, Jeffry D.; Joung, J. Keith Nature Biotechnology, Vol. 32, Issue 4 https://doi.org/10.1038/nbt.2842	journal	March 2014
Generation of mouse models of myeloid malignancy with combinatorial genetic lesions using CRISPR-Cas9 genome editing Heckl, Dirk; Kowalczyk, Monika S.; Yudovich, David Nature Biotechnology, Vol. 32, Issue 9 https://doi.org/10.1038/nbt.2951	journal	June 2014
Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew Wang, Yanpeng; Cheng, Xi; Shan, Qiwei Nature Biotechnology, Vol. 32, Issue 9 https://doi.org/10.1038/nbt.2969	journal	July 2014
A split-Cas9 architecture for inducible genome editing and transcription modulation Zetsche, Bernd; Volz, Sara E.; Zhang, Feng Nature Biotechnology, Vol. 33, Issue 2 https://doi.org/10.1038/nbt.3149	journal	February 2015
Inducible in vivo genome editing with CRISPR-Cas9 Dow, Lukas E.; Fisher, Jonathan; O'Rourke, Kevin P. Nature Biotechnology, Vol. 33, Issue 4 https://doi.org/10.1038/nbt.3155	journal	February 2015
Photoactivatable CRISPR-Cas9 for optogenetic genome editing Nihongaki, Yuta; Kawano, Fuun; Nakajima, Takahiro Nature Biotechnology, Vol. 33, Issue 7 https://doi.org/10.1038/nbt.3245	journal	June 2015
DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins Woo, Je Wook; Kim, Jungeun; Kwon, Soon Il Nature Biotechnology, Vol. 33, Issue 11 https://doi.org/10.1038/nbt.3389	journal	October 2015
Modular construction of mammalian gene circuits using TALE transcriptional repressors Li, Yinqing; Jiang, Yun; Chen, He Nature Chemical Biology, Vol. 11, Issue 3 https://doi.org/10.1038/nchembio.1736	journal	February 2015
A light-inducible CRISPR-Cas9 system for control of endogenous gene activation Polstein, Lauren R.; Gersbach, Charles A. Nature Chemical Biology, Vol. 11, Issue 3 https://doi.org/10.1038/nchembio.1753	journal	February 2015
Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display Shechner, David M.; Hacisuleyman, Ezgi; Younger, Scott T. Nature Methods, Vol. 12, Issue 7 https://doi.org/10.1038/nmeth.3433	journal	June 2015
High-throughput functional genomics using CRISPR–Cas9 Shalem, Ophir; Sanjana, Neville E.; Zhang, Feng Nature Reviews Genetics, Vol. 16, Issue 5 https://doi.org/10.1038/nrg3899	journal	April 2015
Efficient CRISPR/Cas9-mediated Targeted Mutagenesis in Populus in the First Generation Fan, Di; Liu, Tingting; Li, Chaofeng Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep12217	journal	July 2015
An innovative platform for quick and flexible joining of assorted DNA fragments De Paoli, Henrique Cestari; Tuskan, Gerald A.; Yang, Xiaohan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19278	journal	January 2016
A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens Takken, Frank L. W.; Luderer, Rianne; Gabriels, Suzan H. E. J. The Plant Journal, Vol. 24, Issue 2 https://doi.org/10.1046/j.1365-313x.2000.00866.x	journal	October 2000
Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system Xie, Kabin; Minkenberg, Bastian; Yang, Yinong Proceedings of the National Academy of Sciences, Vol. 112, Issue 11 https://doi.org/10.1073/pnas.1420294112	journal	March 2015
CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells Deng, Wulan; Shi, Xinghua; Tjian, Robert Proceedings of the National Academy of Sciences, Vol. 112, Issue 38 https://doi.org/10.1073/pnas.1515692112	journal	August 2015
Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides) Hu, W. -J.; Kawaoka, A.; Tsai, C. -J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 9 https://doi.org/10.1073/pnas.95.9.5407	journal	April 1998
Accelerating the domestication of a bioenergy crop: identifying and modelling morphological targets for sustainable yield increase in Miscanthus Robson, Paul; Jensen, Elaine; Hawkins, Sarah Journal of Experimental Botany, Vol. 64, Issue 14 https://doi.org/10.1093/jxb/ert225	journal	September 2013
Functional modules by relating protein interaction networks and gene expression Tornow, S. Nucleic Acids Research, Vol. 31, Issue 21 https://doi.org/10.1093/nar/gkg838	journal	November 2003
Obligate Ligation-Gated Recombination (ObLiGaRe): Custom-designed nuclease-mediated targeted integration through nonhomologous end joining Maresca, M.; Lin, V. G.; Guo, N. Genome Research, Vol. 23, Issue 3 https://doi.org/10.1101/gr.145441.112	journal	November 2012
Differential Substrate Inhibition Couples Kinetically Distinct 4-Coumarate:Coenzyme A Ligases with Spatially Distinct Metabolic Roles in Quaking Aspen Harding, Scott A.; Leshkevich, Jacqueline; Chiang, Vincent L. Plant Physiology, Vol. 128, Issue 2 https://doi.org/10.1104/pp.010603	journal	February 2002
Computational Estimation and Experimental Verification of Off-Target Silencing during Posttranscriptional Gene Silencing in Plants Xu, Ping; Zhang, Yuanji; Kang, Li Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.083295	journal	August 2006
Activation Tagging in Arabidopsis Weigel, Detlef; Ahn, Ji Hoon; Blázquez, Miguel A. Plant Physiology, Vol. 122, Issue 4 https://doi.org/10.1104/pp.122.4.1003	journal	April 2000
A CRISPR/Cas9 Toolbox for Multiplexed Plant Genome Editing and Transcriptional Regulation Lowder, Levi G.; Zhang, Dengwei; Baltes, Nicholas J. Plant Physiology, Vol. 169, Issue 2 https://doi.org/10.1104/pp.15.00636	journal	August 2015
DNA Replicons for Plant Genome Engineering Baltes, Nicholas J.; Gil-Humanes, Javier; Cermak, Tomas The Plant Cell, Vol. 26, Issue 1 https://doi.org/10.1105/tpc.113.119792	journal	January 2014
Marker-free site-specific gene integration in rice based on the use of two recombination systems: Marker-free precise transgene integration Nandy, Soumen; Srivastava, Vibha Plant Biotechnology Journal, Vol. 10, Issue 8 https://doi.org/10.1111/j.1467-7652.2012.00715.x	journal	June 2012
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world Yang, Xiaohan; Cushman, John C.; Borland, Anne M. New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13393	journal	July 2015
Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy Zhou, Xiaohong; Jacobs, Thomas B.; Xue, Liang-Jiao New Phytologist, Vol. 208, Issue 2 https://doi.org/10.1111/nph.13470	journal	May 2015
Targeted molecular trait stacking in cotton through targeted double‐strand break induction D'Halluin, Kathleen; Vanderstraeten, Chantal; Hulle, Jolien Plant Biotechnology Journal, Vol. 11, Issue 8 https://doi.org/10.1111/pbi.12085	journal	June 2013
Trait stacking via targeted genome editing Ainley, William M.; Sastry-Dent, Lakshmi; Welter, Mary E. Plant Biotechnology Journal, Vol. 11, Issue 9 https://doi.org/10.1111/pbi.12107	journal	August 2013
RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors Piatek, Agnieszka; Ali, Zahir; Baazim, Hatoon Plant Biotechnology Journal, Vol. 13, Issue 4 https://doi.org/10.1111/pbi.12284	journal	November 2014
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 Schiml, Simon; Fauser, Friedrich; Puchta, Holger The Plant Journal, Vol. 80, Issue 6 https://doi.org/10.1111/tpj.12704	journal	November 2014
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Tuskan, G. A.; DiFazio, S.; Jansson, S. Science, Vol. 313, Issue 5793, p. 1596-1604 https://doi.org/10.1126/science.1128691	journal	September 2006
A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity Jinek, M.; Chylinski, K.; Fonfara, I. Science, Vol. 337, Issue 6096, p. 816-821 https://doi.org/10.1126/science.1225829	journal	June 2012
Lignin Valorization: Improving Lignin Processing in the Biorefinery Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J. Science, Vol. 344, Issue 6185, p. 1246843-1246843 https://doi.org/10.1126/science.1246843	journal	May 2014
Genetic Screens in Human Cells Using the CRISPR-Cas9 System Wang, Tim; Wei, Jenny J.; Sabatini, David M. Science, Vol. 343, Issue 6166 https://doi.org/10.1126/science.1246981	journal	December 2013
Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system Belhaj, Khaoula; Chaparro-Garcia, Angela; Kamoun, Sophien Plant Methods, Vol. 9, Issue 1 https://doi.org/10.1186/1746-4811-9-39	journal	January 2013
A CRISPR/Cas9 toolkit for multiplex genome editing in plants Xing, Hui-Li; Dong, Li; Wang, Zhi-Ping BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870-014-0327-y	journal	November 2014
High-frequency, precise modification of the tomato genome Čermák, Tomáš; Baltes, Nicholas J.; Čegan, Radim Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0796-9	journal	November 2015
Phytosequestration: Carbon Biosequestration by Plants and the Prospects of Genetic Engineering Jansson, Christer; Wullschleger, Stan D.; Kalluri, Udaya C. BioScience, Vol. 60, Issue 9 https://doi.org/10.1525/bio.2010.60.9.6	journal	October 2010
Community and Ecosystem Genetics: a Consequence of the Extended Phenotype Whitham, Thomas G.; Young, William P.; Martinsen, Gregory D. Ecology, Vol. 84, Issue 3 https://doi.org/10.1890/0012-9658(2003)084[0559:CAEGAC]2.0.CO;2	journal	March 2003
Genotype variation in bark texture drives lichen community assembly across multiple environments Lamit, L. J.; Lau, M. K.; Næsborg, R. Reese Ecology, Vol. 96, Issue 4 https://doi.org/10.1890/14-1007.1	journal	April 2015
Function genomics of abiotic stress tolerance in plants: a CRISPR approach Jain, Mukesh Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00375	journal	May 2015

Cited By (24)

The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01491-7	journal	December 2017
Unwinding JAZ7 – enigma to harmony Shyu, Christine Journal of Experimental Botany, Vol. 67, Issue 11 https://doi.org/10.1093/jxb/erw191	journal	May 2016
Untapping root system architecture for crop improvement Hochholdinger, Frank Journal of Experimental Botany, Vol. 67, Issue 15 https://doi.org/10.1093/jxb/erw262	journal	August 2016
Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants Yang, Xiaohan; Liu, Degao; Tschaplinski, Timothy J. Journal of Experimental Botany, Vol. 70, Issue 22 https://doi.org/10.1093/jxb/erz408	journal	September 2019
Generation of targeted mutant rice using a CRISPR-Cpf1 system Xu, Rongfang; Qin, Ruiying; Li, Hao Plant Biotechnology Journal, Vol. 15, Issue 6 https://doi.org/10.1111/pbi.12669	journal	February 2017
Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum Li, Rui; Li, Ran; Li, Xindi Plant Biotechnology Journal, Vol. 16, Issue 2 https://doi.org/10.1111/pbi.12781	journal	August 2017
Corrigendum: Building a Genetic Manipulation Tool Box for Orchid Biology: Identification of Constitutive Promoters and Application of CRISPR/Cas9 in the Orchid, Dendrobium officinale Kui, Ling Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00664	journal	January 2017
White Lupin: A Model System for Understanding Plant Adaptation to Low Phosphorus Availability Uhde-Stone, Claudia Legume Nitrogen Fixation in Soils with Low Phosphorus Availability https://doi.org/10.1007/978-3-319-55729-8_13	book	January 2017
Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications Nianiou-Obeidat, Irini; Madesis, Panagiotis; Kissoudis, Christos Plant Cell Reports, Vol. 36, Issue 6 https://doi.org/10.1007/s00299-017-2139-7	journal	April 2017
CRISPR/Cas9-mediated efficient targeted mutagenesis has the potential to accelerate the domestication of Coffea canephora Breitler, Jean-Christophe; Dechamp, Eveline; Campa, Claudine Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 134, Issue 3 https://doi.org/10.1007/s11240-018-1429-2	journal	May 2018
New technologies accelerate the exploration of non-coding RNAs in horticultural plants Liu, Degao; Mewalal, Ritesh; Hu, Rongbin Horticulture Research, Vol. 4, Issue 1 https://doi.org/10.1038/hortres.2017.31	journal	July 2017
CRISPR/Cas9-Mediated Immunity to Geminiviruses: Differential Interference and Evasion Ali, Zahir; Ali, Shakila; Tashkandi, Manal Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26912	journal	May 2016
Base editors: modular tools for the introduction of point mutations in living cells Evanoff, Mallory; Komor, Alexis C. Emerging Topics in Life Sciences, Vol. 3, Issue 5 https://doi.org/10.1042/etls20190088	journal	September 2019
Improvements in algal lipid production: a systems biology and gene editing approach Banerjee, Avik; Banerjee, Chiranjib; Negi, Sangeeta Critical Reviews in Biotechnology, Vol. 38, Issue 3 https://doi.org/10.1080/07388551.2017.1356803	journal	August 2017
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants Liu, Degao; Chen, Mei; Mendoza, Brian Journal of Experimental Botany, Vol. 70, Issue 22 https://doi.org/10.1093/jxb/erz415	journal	September 2019
Standing genomic variation within coding and regulatory regions contributes to the adaptive capacity to climate in a foundation tree species Ahrens, Collin W.; Byrne, Margaret; Rymer, Paul D. Molecular Ecology, Vol. 28, Issue 10 https://doi.org/10.1111/mec.15092	journal	May 2019
SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant development Liu, Kunpeng; Yu, Yu; Dong, Aiwu New Phytologist, Vol. 215, Issue 2 https://doi.org/10.1111/nph.14596	journal	May 2017
Elucidating the role of highly homologous Nicotiana benthamiana ubiquitin E2 gene family members in plant immunity through an improved virus-induced gene silencing approach Zhou, Bangjun; Zeng, Lirong Plant Methods, Vol. 13, Issue 1 https://doi.org/10.1186/s13007-017-0210-6	journal	July 2017
Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees Beckers, Bram; Op De Beeck, Michiel; Weyens, Nele Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0241-2	journal	February 2017
Efficient and heritable transformation of Phalaenopsis orchids Hsing, Hong-Xian; Lin, Yi-Jyun; Tong, Chii-Gong Botanical Studies, Vol. 57, Issue 1 https://doi.org/10.1186/s40529-016-0146-6	journal	October 2016
Overexpression of a pine Dof transcription factor in hybrid poplars: A comparative study in trees growing under controlled and natural conditions Rueda-López, Marina; Pascual, María Belén; Pallero, Mercedes PLOS ONE, Vol. 12, Issue 4 https://doi.org/10.1371/journal.pone.0174748	journal	April 2017
Defining the genetic components of callus formation: A GWAS approach Tuskan, Gerald A.; Mewalal, Ritesh; Gunter, Lee E. PLOS ONE, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pone.0202519	journal	August 2018
Genetic improvement of horticultural crops mediated by CRISPR/Cas: a new horizon of possibilities Koltun, Alessandra; Erpen-Dalla Corte, Lígia; Mertz-Henning, Liliane Marcia Horticultura Brasileira, Vol. 36, Issue 3 https://doi.org/10.1590/s0102-053620180302	journal	September 2018
Sustaining the Future of Plant Breeding: The Critical Role of the USDA‐ARS National Plant Germplasm System Byrne, Patrick F.; Volk, Gayle M.; Gardner, Candice Crop Science, Vol. 58, Issue 2 https://doi.org/10.2135/cropsci2017.05.0303	journal	March 2018

Similar Records

Multiallelic, Targeted Mutagenesis of Magnesium Chelatase With CRISPR/Cas9 Provides a Rapidly Scorable Phenotype in Highly Polyploid Sugarcane

Journal Article · Thu Apr 29 00:00:00 EDT 2021 · Frontiers in Genome Editing · OSTI ID:1780543

Use of anti-CRISPR protein AcrIIA4 as a capture ligand for CRISPR/Cas9 detection

Journal Article · Sun Sep 15 00:00:00 EDT 2019 · Biosensors and Bioelectronics · OSTI ID:1559508

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research

Citation Formats

References (71)

Cited By (24)

Similar Records

Related Subjects