CRISPR/Cas9-mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants
Abstract
Crassulacean acid metabolism (CAM) is an important photosynthetic pathway in diverse lineages of plants featuring high water-use efficiency and drought tolerance. A big challenge facing the CAM research community is to understand the function of the annotated genes in CAM plant genomes. Recently, a new genome editing technology using CRISPR/Cas9 has become a more precise and powerful tool than traditional approaches for functional genomics research in C3 and C4 plants. In this study, we seek to realize the potential of CRISPR/Cas9 to characterize the function of CAM-related genes in the model CAM species Kalanchoë fedtschenkoi. We demonstrate that CRISPR/Cas9 is effective to create biallelic indel mutagenesis to reveal previously unknown roles of blue light receptor phototropin 2 (KfePHOT2) in the CAM pathway. Knocking-out of the KfePHOT2 reduced stomatal conductance and CO2 fixation in the late afternoon and increased stomatal conductance and CO2 fixation in the early evening, indicating that blue light signaling plays an important role in the CAM pathway. Lastly, we provide a genome-wide gRNA database targeting 45,183 protein-coding genes annotated in the K. fedtschenkoi genome.
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-Center for Bioenergy Innovation (CBI)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Southwest Univ. of Science and Technology, Mianyang, Sichuan (China). School of Life Science and Engineering
- Univ. of Tennessee, Knoxville, TN (United States). Dept.t of Chemical and Biomolecular Engineering
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-Center for Bioenergy Innovation (CBI); Univ. of Tennessee, Knoxville, TN (United States). Dept.t of Chemical and Biomolecular Engineering
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1569393
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Experimental Botany
- Additional Journal Information:
- Journal Volume: 70; Journal Issue: 22; Journal ID: ISSN 0022-0957
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; CRISPR/Cas9; crassulacean acid metabolism; phototropin 2; functional genomics; genome-editing
Citation Formats
Liu, Degao, Chen, Mei, Mendoza, Brian, Cheng, Hua, Hu, Rongbin, Li, Linling, Trinh, Cong T., Tuskan, Gerald A., and Yang, Xiaohan. CRISPR/Cas9-mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants. United States: N. p., 2019.
Web. doi:10.1093/jxb/erz415.
Liu, Degao, Chen, Mei, Mendoza, Brian, Cheng, Hua, Hu, Rongbin, Li, Linling, Trinh, Cong T., Tuskan, Gerald A., & Yang, Xiaohan. CRISPR/Cas9-mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants. United States. doi:10.1093/jxb/erz415.
Liu, Degao, Chen, Mei, Mendoza, Brian, Cheng, Hua, Hu, Rongbin, Li, Linling, Trinh, Cong T., Tuskan, Gerald A., and Yang, Xiaohan. Sat .
"CRISPR/Cas9-mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants". United States. doi:10.1093/jxb/erz415. https://www.osti.gov/servlets/purl/1569393.
@article{osti_1569393,
title = {CRISPR/Cas9-mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants},
author = {Liu, Degao and Chen, Mei and Mendoza, Brian and Cheng, Hua and Hu, Rongbin and Li, Linling and Trinh, Cong T. and Tuskan, Gerald A. and Yang, Xiaohan},
abstractNote = {Crassulacean acid metabolism (CAM) is an important photosynthetic pathway in diverse lineages of plants featuring high water-use efficiency and drought tolerance. A big challenge facing the CAM research community is to understand the function of the annotated genes in CAM plant genomes. Recently, a new genome editing technology using CRISPR/Cas9 has become a more precise and powerful tool than traditional approaches for functional genomics research in C3 and C4 plants. In this study, we seek to realize the potential of CRISPR/Cas9 to characterize the function of CAM-related genes in the model CAM species Kalanchoë fedtschenkoi. We demonstrate that CRISPR/Cas9 is effective to create biallelic indel mutagenesis to reveal previously unknown roles of blue light receptor phototropin 2 (KfePHOT2) in the CAM pathway. Knocking-out of the KfePHOT2 reduced stomatal conductance and CO2 fixation in the late afternoon and increased stomatal conductance and CO2 fixation in the early evening, indicating that blue light signaling plays an important role in the CAM pathway. Lastly, we provide a genome-wide gRNA database targeting 45,183 protein-coding genes annotated in the K. fedtschenkoi genome.},
doi = {10.1093/jxb/erz415},
journal = {Journal of Experimental Botany},
number = 22,
volume = 70,
place = {United States},
year = {2019},
month = {9}
}
Web of Science
Figures / Tables:

Works referenced in this record:
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Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize
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Orchestration of carbohydrate processing for crassulacean acid metabolism
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Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits
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Perspectives on the basic and applied aspects of crassulacean acid metabolism (CAM) research
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Stomatal Biology of CAM Plants
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Stomatal response to blue light in crassulacean acid metabolism plants Kalanchoe pinnata and Kalanchoe daigremontiana
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Transcript, protein and metabolite temporal dynamics in the CAM plant Agave
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Phototropin-related NPL1 controls chloroplast relocation induced by blue light
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Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato
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Stomatal responses to light in the facultative Crassulacean acid metabolism species, Portulacaria afra
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sgRNAcas9: A Software Package for Designing CRISPR sgRNA and Evaluating Potential Off-Target Cleavage Sites
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CRISPR/Cas9 Platforms for Genome Editing in Plants: Developments and Applications
journal, July 2016
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Induction of CAM in Mesembryanthemum crystallinum Abolishes the Stomatal Response to Blue Light and Light-Dependent Zeaxanthin Formation in Guard Cell Chloroplasts
journal, January 1997
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Editing plant genomes with CRISPR/Cas9
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Targeted genome modification of crop plants using a CRISPR-Cas system
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Growth-mediated plant movements: hidden in plain sight
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Engineering crassulacean acid metabolism to improve water-use efficiency
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Computational Estimation and Experimental Verification of Off-Target Silencing during Posttranscriptional Gene Silencing in Plants
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A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world
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Phototropins maintain robust circadian oscillation of PSII operating efficiency under blue light
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Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism
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- Ceusters, J.; Borland, A. M.; Taybi, T.
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High-efficiency genome editing using a dmc1 promoter-controlled CRISPR/Cas9 system in maize
journal, April 2018
- Feng, Chao; Su, Handong; Bai, Han
- Plant Biotechnology Journal, Vol. 16, Issue 11
Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system
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- Xie, Kabin; Minkenberg, Bastian; Yang, Yinong
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism
journal, March 2008
- Cushman, John C.; Agarie, Sakae; Albion, Rebecca L.
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Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research
journal, April 2016
- Liu, Degao; Hu, Rongbin; Palla, Kaitlin J.
- Current Opinion in Plant Biology, Vol. 30
Ecophysiology of constitutive and facultative CAM photosynthesis
journal, February 2019
- Winter, Klaus
- Journal of Experimental Botany, Vol. 70, Issue 22
Phosphorylation of Phospho enol pyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO 2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi
journal, September 2017
- Boxall, Susanna F.; Dever, Louisa V.; Kneřová, Jana
- The Plant Cell, Vol. 29, Issue 10
Applying CRISPR/Cas for genome engineering in plants: the best is yet to come
journal, April 2017
- Puchta, Holger
- Current Opinion in Plant Biology, Vol. 36
An Agrobacterium -delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize
journal, September 2016
- Char, Si Nian; Neelakandan, Anjanasree K.; Nahampun, Hartinio
- Plant Biotechnology Journal, Vol. 15, Issue 2
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening
journal, February 2016
- Horrer, Daniel; Flütsch, Sabrina; Pazmino, Diana
- Current Biology, Vol. 26, Issue 3
Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana
journal, October 2006
- Galen, Candace; Rabenold, Jessica J.; Liscum, Emmanuel
- New Phytologist, Vol. 173, Issue 1
Efficient genome editing in plants using a CRISPR/Cas system
journal, August 2013
- Feng, Zhengyan; Zhang, Botao; Ding, Wona
- Cell Research, Vol. 23, Issue 10
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth
journal, November 2014
- Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana
- Plant Physiology, Vol. 167, Issue 1
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017
- Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu
- Nature Communications, Vol. 8, Issue 1
Tissue-Autonomous Promotion of Palisade Cell Development by Phototropin 2 in Arabidopsis
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Precision genome engineering through adenine base editing in plants
journal, June 2018
- Kang, Beum-Chang; Yun, Jae-Young; Kim, Sang-Tae
- Nature Plants, Vol. 4, Issue 7
Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion
journal, March 2017
- Shimatani, Zenpei; Kashojiya, Sachiko; Takayama, Mariko
- Nature Biotechnology, Vol. 35, Issue 5
A CRISPR/Cas9 toolkit for multiplex genome editing in plants
journal, November 2014
- Xing, Hui-Li; Dong, Li; Wang, Zhi-Ping
- BMC Plant Biology, Vol. 14, Issue 1
Works referencing / citing this record:
Phosphorylation of Phospho enol pyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO 2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi
journal, September 2017
- Boxall, Susanna F.; Dever, Louisa V.; Kneřová, Jana
- The Plant Cell, Vol. 29, Issue 10
Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system
journal, March 2015
- Xie, Kabin; Minkenberg, Bastian; Yang, Yinong
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth
journal, November 2014
- Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana
- Plant Physiology, Vol. 167, Issue 1
High-efficiency genome editing using a dmc1 promoter-controlled CRISPR/Cas9 system in maize
journal, April 2018
- Feng, Chao; Su, Handong; Bai, Han
- Plant Biotechnology Journal, Vol. 16, Issue 11
Targeted genome modification of crop plants using a CRISPR-Cas system
journal, August 2013
- Shan, Qiwei; Wang, Yanpeng; Li, Jun
- Nature Biotechnology, Vol. 31, Issue 8
Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana
journal, October 2006
- Galen, Candace; Rabenold, Jessica J.; Liscum, Emmanuel
- New Phytologist, Vol. 173, Issue 1
Tissue-Autonomous Promotion of Palisade Cell Development by Phototropin 2 in Arabidopsis
journal, October 2011
- Kozuka, Toshiaki; Kong, Sam-Geun; Doi, Michio
- The Plant Cell, Vol. 23, Issue 10
Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism
journal, May 2014
- Ceusters, J.; Borland, A. M.; Taybi, T.
- Journal of Experimental Botany, Vol. 65, Issue 13
A CRISPR/Cas9 toolkit for multiplex genome editing in plants
journal, November 2014
- Xing, Hui-Li; Dong, Li; Wang, Zhi-Ping
- BMC Plant Biology, Vol. 14, Issue 1
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening
journal, February 2016
- Horrer, Daniel; Flütsch, Sabrina; Pazmino, Diana
- Current Biology, Vol. 26, Issue 3
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
sgRNAcas9: A Software Package for Designing CRISPR sgRNA and Evaluating Potential Off-Target Cleavage Sites
journal, June 2014
- Xie, Shengsong; Shen, Bin; Zhang, Chaobao
- PLoS ONE, Vol. 9, Issue 6
Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism
journal, March 2008
- Cushman, John C.; Agarie, Sakae; Albion, Rebecca L.
- Plant Physiology, Vol. 147, Issue 1
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research
journal, April 2016
- Liu, Degao; Hu, Rongbin; Palla, Kaitlin J.
- Current Opinion in Plant Biology, Vol. 30
Growth-mediated plant movements: hidden in plain sight
journal, February 2018
- Harmer, Stacey L.; Brooks, Christopher J.
- Current Opinion in Plant Biology, Vol. 41
Precision genome engineering through adenine base editing in plants
journal, June 2018
- Kang, Beum-Chang; Yun, Jae-Young; Kim, Sang-Tae
- Nature Plants, Vol. 4, Issue 7
CRISPR/Cas9 Platforms for Genome Editing in Plants: Developments and Applications
journal, July 2016
- Ma, Xingliang; Zhu, Qinlong; Chen, Yuanling
- Molecular Plant, Vol. 9, Issue 7
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017
- Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu
- Nature Communications, Vol. 8, Issue 1
Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits
journal, August 2013
- Kadomura-Ishikawa, Yasuko; Miyawaki, Katsuyuki; Noji, Sumihare
- Journal of Plant Research, Vol. 126, Issue 6
Enhanced guide-RNA design and targeting analysis for precise CRISPR genome editing of single and consortia of industrially relevant and non-model organisms
journal, September 2017
- Mendoza, Brian J.; Trinh, Cong T.
- Bioinformatics, Vol. 34, Issue 1
Stomatal response to blue light in crassulacean acid metabolism plants Kalanchoe pinnata and Kalanchoe daigremontiana
journal, December 2018
- Gotoh, Eiji; Oiwamoto, Kohei; Inoue, Shin-ichiro
- Journal of Experimental Botany, Vol. 70, Issue 4
Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato
journal, December 2013
- Liu, Degao; He, Shaozhen; Zhai, Hong
- Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 117, Issue 1
Applying CRISPR/Cas for genome engineering in plants: the best is yet to come
journal, April 2017
- Puchta, Holger
- Current Opinion in Plant Biology, Vol. 36
Efficient genome editing in plants using a CRISPR/Cas system
journal, August 2013
- Feng, Zhengyan; Zhang, Botao; Ding, Wona
- Cell Research, Vol. 23, Issue 10
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world
journal, July 2015
- Yang, Xiaohan; Cushman, John C.; Borland, Anne M.
- New Phytologist, Vol. 207, Issue 3
Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014
- Borland, Anne M.; Hartwell, James; Weston, David J.
- Trends in Plant Science, Vol. 19, Issue 5
Stomatal Biology of CAM Plants
journal, February 2017
- Males, Jamie; Griffiths, Howard
- Plant Physiology, Vol. 174, Issue 2
Transcript, protein and metabolite temporal dynamics in the CAM plant Agave
journal, November 2016
- Abraham, Paul E.; Yin, Hengfu; Borland, Anne M.
- Nature Plants, Vol. 2, Issue 12
Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize
journal, October 2018
- Salesse-Smith, Coralie E.; Sharwood, Robert E.; Busch, Florian A.
- Nature Plants, Vol. 4, Issue 10
Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion
journal, March 2017
- Shimatani, Zenpei; Kashojiya, Sachiko; Takayama, Mariko
- Nature Biotechnology, Vol. 35, Issue 5
Orchestration of carbohydrate processing for crassulacean acid metabolism
journal, June 2016
- Borland, Anne M.; Guo, Hao-Bo; Yang, Xiaohan
- Current Opinion in Plant Biology, Vol. 31
An Agrobacterium -delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize
journal, September 2016
- Char, Si Nian; Neelakandan, Anjanasree K.; Nahampun, Hartinio
- Plant Biotechnology Journal, Vol. 15, Issue 2
Phototropin-related NPL1 controls chloroplast relocation induced by blue light
journal, April 2001
- Jarillo, Jose A.; Gabrys, Halina; Capel, Juan
- Nature, Vol. 410, Issue 6831
Ecophysiology of constitutive and facultative CAM photosynthesis
journal, February 2019
- Winter, Klaus
- Journal of Experimental Botany, Vol. 70, Issue 22
Phototropins maintain robust circadian oscillation of PSII operating efficiency under blue light
journal, August 2015
- Litthauer, Suzanne; Battle, Martin W.; Lawson, Tracy
- The Plant Journal, Vol. 83, Issue 6
Computational Estimation and Experimental Verification of Off-Target Silencing during Posttranscriptional Gene Silencing in Plants
journal, August 2006
- Xu, Ping; Zhang, Yuanji; Kang, Li
- Plant Physiology, Vol. 142, Issue 2
Stomatal responses to light in the facultative Crassulacean acid metabolism species, Portulacaria afra
journal, May 1992
- Lee, David M.; Assmann, Sarah M.
- Physiologia Plantarum, Vol. 85, Issue 1
Induction of CAM in Mesembryanthemum crystallinum Abolishes the Stomatal Response to Blue Light and Light-Dependent Zeaxanthin Formation in Guard Cell Chloroplasts
journal, January 1997
- Tallman, G.; Zhu, J.; Mawson, B. T.
- Plant and Cell Physiology, Vol. 38, Issue 3
Editing plant genomes with CRISPR/Cas9
journal, April 2015
- Belhaj, Khaoula; Chaparro-Garcia, Angela; Kamoun, Sophien
- Current Opinion in Biotechnology, Vol. 32
Perspectives on the basic and applied aspects of crassulacean acid metabolism (CAM) research
journal, September 2018
- Liu, Degao; Palla, Kaitlin J.; Hu, Rongbin
- Plant Science, Vol. 274
Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants
journal, September 2019
- Yang, Xiaohan; Liu, Degao; Tschaplinski, Timothy J.
- Journal of Experimental Botany, Vol. 70, Issue 22
Figures / Tables found in this record: