Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress
Abstract
This perspective paper explores the utilization of abiotic stress-responsive transcription factors (TFs) from crassulacean acid metabolism (CAM) plants to improve abiotic stress tolerance in crop plants. CAM is a specialized type of photosynthetic adaptation that enhances water-use efficiency (WUE) by shifting CO2 uptake to all or part of the nighttime when evaporative water losses are minimal. Recent studies have shown that TF-based genetic engineering could be a useful approach for improving plant abiotic stress tolerance because of the role of TFs as master regulators of clusters of stress-responsive genes. Here, we explore the use of abiotic stress-responsive TFs from CAM plants to improve abiotic stress tolerance and WUE in crops by controlling the expression of gene cohorts that mediate drought-responsive adaptations. Recent research has revealed several TF families including AP2/ERF, MYB, WRKY, NAC, NF-Y, and bZIP that might regulate water-deficit stress responses and CAM in the inducible CAM plant Mesembryanthemum crystallinum under water-deficit stress-induced CAM and in the obligate CAM plant Kalanchoe fedtschenkoi. Overexpression of genes from these families in Arabidopsis thaliana can improve abiotic stress tolerance in A. thaliana in some instances. Therefore, we propose that TF-based genetic engineering with a small number of CAM abiotic stress-responsive TFs willmore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Nevada, Reno, NV (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1495739
- Alternate Identifier(s):
- OSTI ID: 1611162
- Grant/Contract Number:
- SC0008834
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Name: Frontiers in Plant Science Journal Volume: 10; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Plant Sciences; abiotic stress response; crassulacean acid metabolism; drought tolerance; extremophytes; genetic engineering; transcription factor
Citation Formats
Amin, Atia B., Rathnayake, Kumudu N., Yim, Won C., Garcia, Travis M., Wone, Beate, Cushman, John C., and Wone, Bernard W. M. Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress. Switzerland: N. p., 2019.
Web. doi:10.3389/fpls.2019.00129.
Amin, Atia B., Rathnayake, Kumudu N., Yim, Won C., Garcia, Travis M., Wone, Beate, Cushman, John C., & Wone, Bernard W. M. Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress. Switzerland. https://doi.org/10.3389/fpls.2019.00129
Amin, Atia B., Rathnayake, Kumudu N., Yim, Won C., Garcia, Travis M., Wone, Beate, Cushman, John C., and Wone, Bernard W. M. Fri .
"Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress". Switzerland. https://doi.org/10.3389/fpls.2019.00129.
@article{osti_1495739,
title = {Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress},
author = {Amin, Atia B. and Rathnayake, Kumudu N. and Yim, Won C. and Garcia, Travis M. and Wone, Beate and Cushman, John C. and Wone, Bernard W. M.},
abstractNote = {This perspective paper explores the utilization of abiotic stress-responsive transcription factors (TFs) from crassulacean acid metabolism (CAM) plants to improve abiotic stress tolerance in crop plants. CAM is a specialized type of photosynthetic adaptation that enhances water-use efficiency (WUE) by shifting CO2 uptake to all or part of the nighttime when evaporative water losses are minimal. Recent studies have shown that TF-based genetic engineering could be a useful approach for improving plant abiotic stress tolerance because of the role of TFs as master regulators of clusters of stress-responsive genes. Here, we explore the use of abiotic stress-responsive TFs from CAM plants to improve abiotic stress tolerance and WUE in crops by controlling the expression of gene cohorts that mediate drought-responsive adaptations. Recent research has revealed several TF families including AP2/ERF, MYB, WRKY, NAC, NF-Y, and bZIP that might regulate water-deficit stress responses and CAM in the inducible CAM plant Mesembryanthemum crystallinum under water-deficit stress-induced CAM and in the obligate CAM plant Kalanchoe fedtschenkoi. Overexpression of genes from these families in Arabidopsis thaliana can improve abiotic stress tolerance in A. thaliana in some instances. Therefore, we propose that TF-based genetic engineering with a small number of CAM abiotic stress-responsive TFs will be a promising strategy for improving abiotic stress tolerance and WUE in crop plants in a projected hotter and drier landscape in the 21st-century and beyond.},
doi = {10.3389/fpls.2019.00129},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {Switzerland},
year = {Fri Feb 22 00:00:00 EST 2019},
month = {Fri Feb 22 00:00:00 EST 2019}
}
https://doi.org/10.3389/fpls.2019.00129
Web of Science
Works referenced in this record:
The Potential of Transcription Factor-Based Genetic Engineering in Improving Crop Tolerance to Drought
journal, October 2014
- Rabara, Roel C.; Tripathi, Prateek; Rushton, Paul J.
- OMICS: A Journal of Integrative Biology, Vol. 18, Issue 10
Analysis of expression and evolutionary relationships of phosphoenol-pyruvate carboxylase genes in Flaveria trinervia (C4) and F. pringlei (C3)
journal, December 1990
- Hermans, J�rgen; Westhoff, Peter
- MGG Molecular & General Genetics, Vol. 224, Issue 3
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
Abscisic acid signaling and protein synthesis requirements for phosphoenolpyruvate carboxylase transcript induction in the common ice plant
journal, January 2002
- Taybi, Tahar; Cushman, John C.
- Journal of Plant Physiology, Vol. 159, Issue 11
Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice
journal, July 2014
- Cai, Ronghao; Zhao, Yang; Wang, Yufu
- Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 119, Issue 3
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands
journal, April 2009
- Borland, A. M.; Griffiths, H.; Hartwell, J.
- Journal of Experimental Botany, Vol. 60, Issue 10
Induction of Crassulacean acid metabolism by water limitation
journal, February 2002
- Cushman, J. C.; Borland, A. M.
- Plant, Cell and Environment, Vol. 25, Issue 2
Crassulacean acid metabolism biology
journal, November 2014
- Garcia, Travis M.; Heyduk, Karolina; Kuzmick, Emily
- New Phytologist, Vol. 204, Issue 4
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
Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants
journal, August 2008
- Liao, Yong; Zou, Hong-Feng; Wang, Hui-Wen
- Cell Research, Vol. 18, Issue 10
Transcription Factors and Plants Response to Drought Stress: Current Understanding and Future Directions
journal, July 2016
- Joshi, Rohit; Wani, Shabir H.; Singh, Balwant
- Frontiers in Plant Science, Vol. 7
Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia
journal, November 2016
- Rodrigues, Maria Aurineide; Hamachi, Leonardo; Mioto, Paulo Tamaso
- Plant Physiology and Biochemistry, Vol. 108
Embracing new-generation ‘omics’ tools to improve drought tolerance in cereal and food-legume crops
journal, April 2015
- Singh, B.; Bohra, A.; Mishra, S.
- Biologia Plantarum, Vol. 59, Issue 3
Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species
journal, February 2011
- Zhang, Xia; Wang, Lei; Meng, Hui
- Plant Molecular Biology, Vol. 75, Issue 4-5
Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
journal, August 2018
- Yin, Hengfu; Guo, Hao-Bo; Weston, David J.
- BMC Genomics, Vol. 19, Issue 1
Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings
journal, August 2016
- Chiang, Chih-Pin; Yim, Won C.; Sun, Ying-Hsuan
- Frontiers in Plant Science, Vol. 7
Engineering Cold Stress Tolerance in Crop Plants
journal, March 2011
- S. Sanghera, Gulzar; H. Wani, Shabir; Hussain, Wasim
- Current Genomics, Vol. 12, Issue 1
Conservation and Diversification of Circadian Rhythmicity Between a Model Crassulacean Acid Metabolism Plant Kalanchoë fedtschenkoi and a Model C3 Photosynthesis Plant Arabidopsis thaliana
journal, November 2018
- Moseley, Robert C.; Mewalal, Ritesh; Motta, Francis
- Frontiers in Plant Science, Vol. 9
Stress Tolerance and Glucose Insensitive Phenotypes in Arabidopsis Overexpressing the CpMYB10 Transcription Factor Gene
journal, April 2004
- Villalobos, Miguel Angel; Bartels, Dorothea; Iturriaga, Gabriel
- Plant Physiology, Vol. 135, Issue 1
Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network
journal, April 2011
- Golldack, Dortje; Lüking, Ines; Yang, Oksoon
- Plant Cell Reports, Vol. 30, Issue 8
The multifaceted roles of NUCLEAR FACTOR-Y in Arabidopsis thaliana development and stress responses
journal, May 2017
- Swain, Swadhin; Myers, Zachary A.; Siriwardana, Chamindika L.
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1860, Issue 5
The NAC Family Transcription Factor OsNAP Confers Abiotic Stress Response Through the ABA Pathway
journal, February 2014
- Chen, Xu; Wang, Yaofeng; Lv, Bo
- Plant and Cell Physiology, Vol. 55, Issue 3
Salt Cress. A Halophyte and Cryophyte Arabidopsis Relative Model System and Its Applicability to Molecular Genetic Analyses of Growth and Development of Extremophiles
journal, July 2004
- Inan, Günsu; Zhang, Quan; Li, Pinghua
- Plant Physiology, Vol. 135, Issue 3
TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis
journal, February 2012
- Mao, Xinguo; Zhang, Hongying; Qian, Xueya
- Journal of Experimental Botany, Vol. 63, Issue 8
Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis
journal, January 2009
- Qiu, Y.; Yu, D.
- Environmental and Experimental Botany, Vol. 65, Issue 1
Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare
journal, November 2015
- Brilhaus, Dominik; Bräutigam, Andrea; Mettler-Altmann, Tabea
- Plant Physiology, Vol. 170, Issue 1
Responses of some North American CAM plants to freezing temperatures and doubled CO2concentrations: implications of global climate change for extending cultivation
journal, October 1996
- Nobel, Park S.
- Journal of Arid Environments, Vol. 34, Issue 2
Global warming and 21st century drying
journal, March 2014
- Cook, Benjamin I.; Smerdon, Jason E.; Seager, Richard
- Climate Dynamics, Vol. 43, Issue 9-10
Crop Production under Drought and Heat Stress: Plant Responses and Management Options
journal, June 2017
- Fahad, Shah; Bajwa, Ali A.; Nazir, Usman
- Frontiers in Plant Science, Vol. 8
The pineapple genome and the evolution of CAM photosynthesis
journal, November 2015
- Ming, Ray; VanBuren, Robert; Wai, Ching Man
- Nature Genetics, Vol. 47, Issue 12
Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future
journal, April 2006
- Umezawa, Taishi; Fujita, Miki; Fujita, Yasunari
- Current Opinion in Biotechnology, Vol. 17, Issue 2
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
Crassulacean acid metabolism under global climate change: Meetings
journal, February 2009
- Reyes-García, Casandra; Andrade, José Luis
- New Phytologist, Vol. 181, Issue 4
Temporal and spatial transcriptomic and micro RNA dynamics of CAM photosynthesis in pineapple
journal, August 2017
- Wai, Ching M.; VanBuren, Robert; Zhang, Jisen
- The Plant Journal, Vol. 92, Issue 1
Recent Advances in Utilizing Transcription Factors to Improve Plant Abiotic Stress Tolerance by Transgenic Technology
journal, February 2016
- Wang, Hongyan; Wang, Honglei; Shao, Hongbo
- Frontiers in Plant Science, Vol. 7
Climate-resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy: CAM engineering in trees
journal, December 2014
- Borland, Anne M.; Wullschleger, Stan D.; Weston, David J.
- Plant, Cell & Environment, Vol. 38, Issue 9
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
Global Synthesis of Drought Effects on Maize and Wheat Production
journal, May 2016
- Daryanto, Stefani; Wang, Lixin; Jacinthe, Pierre-André
- PLOS ONE, Vol. 11, Issue 5
Transcriptomic Analysis of a Tertiary Relict Plant, Extreme Xerophyte Reaumuria soongorica to Identify Genes Related to Drought Adaptation
journal, May 2013
- Shi, Yong; Yan, Xia; Zhao, Pengshan
- PLoS ONE, Vol. 8, Issue 5
Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis
journal, March 2014
- Winter, K.; Holtum, J. A. M.
- Journal of Experimental Botany, Vol. 65, Issue 13
Functional and Transcriptome Analysis Reveals an Acclimatization Strategy for Abiotic Stress Tolerance Mediated by Arabidopsis NF-YA Family Members
journal, October 2012
- Leyva-González, Marco Antonio; Ibarra-Laclette, Enrique; Cruz-Ramírez, Alfredo
- PLoS ONE, Vol. 7, Issue 10
Plant NF-Y transcription factors: Key players in plant-microbe interactions, root development and adaptation to stress
journal, May 2017
- Zanetti, María Eugenia; Rípodas, Carolina; Niebel, Andreas
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1860, Issue 5
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
Phosphoenolpyruvate carboxylase genes in C 3 , crassulacean acid metabolism (CAM) and C 3 /CAM intermediate species of the genus Clusia: rapid reversible C 3 /CAM switches are based on the C 3 housekeeping gene
journal, December 2006
- Vaasen, Anja; Begerow, Dominik; Hampp, RÜDiger
- Plant, Cell and Environment, Vol. 29, Issue 12
Transcription factors as tools to engineer enhanced drought stress tolerance in plants
journal, February 2011
- Hussain, Syed Sarfraz; Kayani, Mahmood Akhtar; Amjad, Muhammad
- Biotechnology Progress, Vol. 27, Issue 2
Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments
journal, December 2001
- Cushman, John C.
- Plant Physiology, Vol. 127, Issue 4
A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice
journal, February 2012
- Yang, An; Dai, Xiaoyan; Zhang, Wen-Hao
- Journal of Experimental Botany, Vol. 63, Issue 7
Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome
journal, January 2016
- Roy, Sujit
- Plant Signaling & Behavior, Vol. 11, Issue 1
Induction of Crassulacean Acid Metabolism in the Facultative Halophyte Mesembryanthemum crystallinum by Abscisic Acid
journal, July 1990
- Chu, Chun; Dai, Ziyu; Ku, Maurice S. B.
- Plant Physiology, Vol. 93, Issue 3
Pineapple Genome: A Reference for Monocots and CAM Photosynthesis
journal, November 2016
- Ming, Ray; Wai, Ching Man; Guyot, Romain
- Trends in Genetics, Vol. 32, Issue 11
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism
journal, June 2016
- Hartwell, James; Dever, Louisa V.; Boxall, Susanna F.
- Current Opinion in Plant Biology, Vol. 31
NAC transcription factors in plant abiotic stress responses
journal, February 2012
- Nakashima, Kazuo; Takasaki, Hironori; Mizoi, Junya
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2
Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism
journal, February 2018
- Heyduk, Karolina; Ray, Jeremy N.; Ayyampalayam, Saravanaraj
- American Journal of Botany, Vol. 105, Issue 3
Climate Trends and Global Crop Production Since 1980
journal, May 2011
- Lobell, D. B.; Schlenker, W.; Costa-Roberts, J.
- Science, Vol. 333, Issue 6042
Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach
journal, January 2010
- Tran, Lam-Son Phan; Nishiyama, Rie; Yamaguchi-Shinozaki, Kazuko
- GM Crops, Vol. 1, Issue 1
Expression, purification, and initial characterization of a recombinant form of plant PEP-carboxylase kinase from CAM-induced Mesembryanthemum crystallinum with enhanced solubility in Escherichia coli
journal, May 2003
- Ermolova, Natalia V.; Ann Cushman, Mary; Taybi, Tahar
- Protein Expression and Purification, Vol. 29, Issue 1
Evolution along the crassulacean acid metabolism continuum
journal, January 2010
- Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark
- Functional Plant Biology, Vol. 37, Issue 11
Systems biology: A new CAM era
journal, November 2016
- Fernie, Alisdair R.
- Nature Plants, Vol. 2, Issue 12
Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation
journal, March 2015
- Shrivastava, Pooja; Kumar, Rajesh
- Saudi Journal of Biological Sciences, Vol. 22, Issue 2
Development and use of bioenergy feedstocks for semi-arid and arid lands
journal, April 2015
- Cushman, John C.; Davis, Sarah C.; Yang, Xiaohan
- Journal of Experimental Botany, Vol. 66, Issue 14
A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield
journal, April 2018
- Lim, Sung Don; Yim, Won Choel; Liu, Degao
- Plant Biotechnology Journal, Vol. 16, Issue 9
Plant Life in Extreme Environments: How Do You Improve Drought Tolerance?
journal, May 2018
- Bechtold, Ulrike
- Frontiers in Plant Science, Vol. 9
Differential Effects of Abscisic Acid on Phosphoenolpyruvate Carboxylase and CAM Operation in Kalanchoë blossfeldiana
journal, June 1995
- Taybi, T.; Sotta, B.; Gehrig, H.
- Botanica Acta, Vol. 108, Issue 3
Temperature extremes: Effect on plant growth and development
journal, December 2015
- Hatfield, Jerry L.; Prueger, John H.
- Weather and Climate Extremes, Vol. 10
Transcriptome Comparison Reveals Distinct Selection Patterns in Domesticated and Wild Agave Species, the Important CAM Plants
journal, November 2018
- Huang, Xing; Wang, Bo; Xi, Jingen
- International Journal of Genomics, Vol. 2018
Transcriptional Regulatory Networks in Cellular Responses and Tolerance to Dehydration and cold Stresses
journal, June 2006
- Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo
- Annual Review of Plant Biology, Vol. 57, Issue 1
Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice
journal, August 2006
- Hu, H.; Dai, M.; Yao, J.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 35
Sorghum phosphoenolpyruvate carboxylase gene family: structure, function and molecular evolution
journal, February 1993
- Lepiniec, Lo�c; Keryer, Eliane; Philippe, Herve
- Plant Molecular Biology, Vol. 21, Issue 3
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
A meta-analysis of crop yield under climate change and adaptation
journal, March 2014
- Challinor, A. J.; Watson, J.; Lobell, D. B.
- Nature Climate Change, Vol. 4, Issue 4
World population stabilization unlikely this century
journal, September 2014
- Gerland, P.; Raftery, A. E.; ev ikova, H.
- Science, Vol. 346, Issue 6206
Influence of extreme weather disasters on global crop production
journal, January 2016
- Lesk, Corey; Rowhani, Pedram; Ramankutty, Navin
- Nature, Vol. 529, Issue 7584
Achievable productivities of certain CAM plants: basis for high values compared with C3 and C4 plants
journal, October 1991
- Nobel, Park S.
- New Phytologist, Vol. 119, Issue 2
Overexpression of a NAC transcription factor enhances rice drought and salt tolerance
journal, February 2009
- Zheng, Xingnan; Chen, Bo; Lu, Guojun
- Biochemical and Biophysical Research Communications, Vol. 379, Issue 4
Food Security: The Challenge of Feeding 9 Billion People
journal, January 2010
- Godfray, H. C. J.; Beddington, J. R.; Crute, I. R.
- Science, Vol. 327, Issue 5967
A transcription factor hierarchy defines an environmental stress response network
journal, November 2016
- Song, L.; Huang, S. -s. C.; Wise, A.
- Science, Vol. 354, Issue 6312
Signaling Events Leading to Crassulacean Acid Metabolism Induction in the Common Ice Plant
journal, October 1999
- Taybi, Tahar; Cushman, John C.
- Plant Physiology, Vol. 121, Issue 2