Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants
Abstract
Crassulacean acid metabolism (CAM) photosynthesis is an important biological innovation enabling plant adaptation to hot and dry environments. CAM plants feature high water-use efficiency, with potential for sustainable crop production under water-limited conditions. A deep understanding of CAM-related gene function and molecular evolution of CAM plants is critical for exploiting the potential of engineering CAM into C3 crops to enhance crop production on semi-arid or marginal agricultural lands. With the newly emerging genomics resources for multiple CAM species, progress has been made in comparative genomics studies on the molecular basis and subsequently on the evolution of CAM. Here, recent advances in CAM comparative genomics research in constitutive and facultative CAM plants are reviewed, with a focus on the analyses of DNA/protein sequences and gene expression to provide new insights into the path and driving force of CAM evolution and to identify candidate genes involved in CAM-related biological processes. Potential applications of new computational and experimental technologies (e.g. CRISPR/Cas-mediated genome-editing technology) to the comparative and evolutionary genomics research on CAM plants are offered.
- Authors:
-
- Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA, The Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, USA
- Department of Genetics, Cell Biology and Development and Center for Precision Plant Genomics, University of Minnesota, Saint Paul, MN, USA
- University of Wyoming, USA
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1576659
- Alternate Identifier(s):
- OSTI ID: 1569384; OSTI ID: 1570521
- Grant/Contract Number:
- SC0008834; AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- Journal of Experimental Botany
- Additional Journal Information:
- Journal Name: Journal of Experimental Botany Journal Volume: 70 Journal Issue: 22; Journal ID: ISSN 0022-0957
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; comparative genomics; crassulacean acid metabolism; drought stress; evolution; gene function; genome editing; photosynthesis
Citation Formats
Yang, Xiaohan, Liu, Degao, Tschaplinski, Timothy J., Tuskan, Gerald A., and Williams, ed., David. Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants. United Kingdom: N. p., 2019.
Web. doi:10.1093/jxb/erz408.
Yang, Xiaohan, Liu, Degao, Tschaplinski, Timothy J., Tuskan, Gerald A., & Williams, ed., David. Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants. United Kingdom. https://doi.org/10.1093/jxb/erz408
Yang, Xiaohan, Liu, Degao, Tschaplinski, Timothy J., Tuskan, Gerald A., and Williams, ed., David. Sat .
"Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants". United Kingdom. https://doi.org/10.1093/jxb/erz408.
@article{osti_1576659,
title = {Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants},
author = {Yang, Xiaohan and Liu, Degao and Tschaplinski, Timothy J. and Tuskan, Gerald A. and Williams, ed., David},
abstractNote = {Crassulacean acid metabolism (CAM) photosynthesis is an important biological innovation enabling plant adaptation to hot and dry environments. CAM plants feature high water-use efficiency, with potential for sustainable crop production under water-limited conditions. A deep understanding of CAM-related gene function and molecular evolution of CAM plants is critical for exploiting the potential of engineering CAM into C3 crops to enhance crop production on semi-arid or marginal agricultural lands. With the newly emerging genomics resources for multiple CAM species, progress has been made in comparative genomics studies on the molecular basis and subsequently on the evolution of CAM. Here, recent advances in CAM comparative genomics research in constitutive and facultative CAM plants are reviewed, with a focus on the analyses of DNA/protein sequences and gene expression to provide new insights into the path and driving force of CAM evolution and to identify candidate genes involved in CAM-related biological processes. Potential applications of new computational and experimental technologies (e.g. CRISPR/Cas-mediated genome-editing technology) to the comparative and evolutionary genomics research on CAM plants are offered.},
doi = {10.1093/jxb/erz408},
journal = {Journal of Experimental Botany},
number = 22,
volume = 70,
place = {United Kingdom},
year = {Sat Sep 07 00:00:00 EDT 2019},
month = {Sat Sep 07 00:00:00 EDT 2019}
}
https://doi.org/10.1093/jxb/erz408
Web of Science
Figures / Tables:
Works referenced in this record:
Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress
journal, February 2019
- Amin, Atia B.; Rathnayake, Kumudu N.; Yim, Won C.
- Frontiers in Plant Science, Vol. 10
Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae
journal, February 2004
- Crayn, D. M.; Winter, K.; Smith, J. A. C.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 10
New technologies accelerate the exploration of non-coding RNAs in horticultural plants
journal, July 2017
- Liu, Degao; Mewalal, Ritesh; Hu, Rongbin
- Horticulture Research, Vol. 4, Issue 1
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants
journal, September 2019
- Liu, Degao; Chen, Mei; Mendoza, Brian
- Journal of Experimental Botany, Vol. 70, Issue 22
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
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
Comparative genomics of Eucalyptus and Corymbia reveals low rates of genome structural rearrangement
journal, May 2017
- Butler, J. B.; Vaillancourt, R. E.; Potts, B. M.
- BMC Genomics, Vol. 18, Issue 1
phot1 and phot2 mediate blue light regulation of stomatal opening
journal, December 2001
- Kinoshita, Toshinori; Doi, Michio; Suetsugu, Noriyuki
- Nature, Vol. 414, Issue 6864
On the Evolutionary Origin of CAM Photosynthesis
journal, April 2017
- Bräutigam, Andrea; Schlüter, Urte; Eisenhut, Marion
- 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
Shared expression of crassulacean acid metabolism (CAM) genes pre-dates the origin of CAM in the genus Yucca
journal, April 2019
- Heyduk, Karolina; Ray, Jeremy N.; Ayyampalayam, Saaravanaraj
- Journal of Experimental Botany, Vol. 70, Issue 22
Comparative Genomics Analysis Provides New Insight Into Molecular Basis of Stomatal Movement in Kalanchoë fedtschenkoi
journal, March 2019
- Moseley, Robert C.; Tuskan, Gerald A.; Yang, Xiaohan
- Frontiers in Plant Science, Vol. 10
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
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
Contingency and determinism in evolution: Replaying life’s tape
journal, November 2018
- Blount, Zachary D.; Lenski, Richard E.; Losos, Jonathan B.
- Science, Vol. 362, Issue 6415
DNA Replicons for Plant Genome Engineering
journal, January 2014
- Baltes, Nicholas J.; Gil-Humanes, Javier; Cermak, Tomas
- The Plant Cell, Vol. 26, 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
Evolutionary trajectories, accessibility and other metaphors: the case of C 4 and CAM photosynthesis
journal, April 2019
- Edwards, Erika J.
- New Phytologist, Vol. 223, Issue 4
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
Partial characterization of guard-cell phosphoenolpyruvate carboxylase: Kinetic datum collection in real time from single-cell activities
journal, July 1990
- Tarczynski, Mitchell C.; Outlaw, William H.
- Archives of Biochemistry and Biophysics, Vol. 280, Issue 1
Divergence of the Dof Gene Families in Poplar, Arabidopsis, and Rice Suggests Multiple Modes of Gene Evolution after Duplication
journal, September 2006
- Yang, Xiaohan; Tuskan, Gerald A.; Cheng, (Max) Zong-Ming
- Plant Physiology, Vol. 142, Issue 3
DROIDS 1.20: A GUI-Based Pipeline for GPU-Accelerated Comparative Protein Dynamics
journal, March 2018
- Babbitt, Gregory A.; Mortensen, Jamie S.; Coppola, Erin E.
- Biophysical Journal, Vol. 114, Issue 5
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
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
Photosynthesis, Reorganized
journal, April 2011
- West-Eberhard, M. J.; Smith, J. A. C.; Winter, K.
- Science, Vol. 332, Issue 6027
CRISPR/Cas9: a promising way to exploit genetic variation in plants
journal, August 2016
- Rani, Reema; Yadav, Prashant; Barbadikar, Kalyani M.
- Biotechnology Letters, Vol. 38, Issue 12
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
Precise gene replacement in rice by RNA transcript-templated homologous recombination
journal, March 2019
- Li, Shaoya; Li, Jingying; He, Yubing
- Nature Biotechnology, Vol. 37, Issue 4
Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia
journal, February 2014
- Barrera Zambrano, V. A.; Lawson, T.; Olmos, E.
- Journal of Experimental Botany, Vol. 65, Issue 13
CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture
journal, April 2019
- Chen, Kunling; Wang, Yanpeng; Zhang, Rui
- Annual Review of Plant Biology, Vol. 70, Issue 1
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
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
Angiosperm Responses to a Low-CO 2 World: CAM and C 4 Photosynthesis as Parallel Evolutionary Trajectories
journal, July 2012
- Edwards, Erika J.; Ogburn, R. Matthew
- International Journal of Plant Sciences, Vol. 173, Issue 6
De novo transcriptome assembly of drought tolerant CAM plants, Agave deserti and Agave tequilana
journal, January 2013
- Gross, Stephen M.; Martin, Jeffrey A.; Simpson, June
- BMC Genomics, Vol. 14, Issue 1
Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album
journal, June 2019
- Wai, Ching Man; Weise, Sean E.; Ozersky, Philip
- PLOS Genetics, Vol. 15, Issue 6
Guard cell photosynthesis and stomatal function
journal, December 2008
- Lawson, Tracy
- New Phytologist, Vol. 181, Issue 1
Expression Profiles of Phosphoenolpyruvate Carboxylase and Phosphoenolpyruvate Carboxylase Kinase Genes in Phalaenopsis, Implications for Regulating the Performance of Crassulacean Acid Metabolism
journal, October 2018
- Ping, Chia-Yun; Chen, Fure-Chyi; Cheng, Teen-Chi
- Frontiers in Plant Science, Vol. 9
Requirements for activation of the signal-transduction network that leads to regulatory phosphorylation of leaf guard-cell phosphoenolpyruvate carboxylase during fusicoccin-stimulated stomatal opening
journal, November 2002
- Outlaw, William H.; Du, Zhirong; Xia Meng, Fan
- Archives of Biochemistry and Biophysics, Vol. 407, Issue 1
The Irreversible C 3 to CAM Shift in Well-watered and Salt-stressed Plants of Mesembryanthemum crystallinum is under Strict Ontogenetic Control
journal, February 1992
- Herppich, W.; Herppich, Margaretha; VON Willert, D. J.
- Botanica Acta, Vol. 105, 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
The genome sequence of the orchid Phalaenopsis equestris
journal, November 2014
- Cai, Jing; Liu, Xin; Vanneste, Kevin
- Nature Genetics, Vol. 47, Issue 1
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
PaperBLAST: Text Mining Papers for Information about Homologs
journal, August 2017
- Price, Morgan N.; Arkin, Adam P.
- mSystems, Vol. 2, Issue 4
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
Choosing the Right Tool for the Job: RNAi, TALEN, or CRISPR
journal, May 2015
- Boettcher, Michael; McManus, Michael T.
- Molecular Cell, Vol. 58, Issue 4
Ecophysiology of constitutive and facultative CAM photosynthesis
journal, February 2019
- Winter, Klaus
- Journal of Experimental Botany, Vol. 70, Issue 22
Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage
journal, April 2016
- Komor, Alexis C.; Kim, Yongjoo B.; Packer, Michael S.
- Nature, Vol. 533, Issue 7603
Engineering Complex Synthetic Transcriptional Programs with CRISPR RNA Scaffolds
journal, January 2015
- Zalatan, Jesse G.; Lee, Michael E.; Almeida, Ricardo
- Cell, Vol. 160, Issue 1-2
The kinome of pineapple: catalog and insights into functions in crassulacean acid metabolism plants
journal, September 2018
- Zhu, Kaikai; Liu, Hui; Chen, Xinlu
- BMC Plant Biology, Vol. 18, Issue 1
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
CRISPR-guided DNA polymerases enable diversification of all nucleotides in a tunable window
journal, August 2018
- Halperin, Shakked O.; Tou, Connor J.; Wong, Eric B.
- Nature, Vol. 560, Issue 7717
On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoe, and Opuntia
journal, June 2007
- Winter, K.; Garcia, M.; Holtum, J. A. M.
- Journal of Experimental Botany, Vol. 59, Issue 7
CRISPR/Cas9-mediated gene targeting in Arabidopsis using sequential transformation
journal, May 2018
- Miki, Daisuke; Zhang, Wenxin; Zeng, Wenjie
- Nature Communications, Vol. 9, Issue 1
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
Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation
journal, November 1993
- Ehleringer, James R.; Monson, Russell K.
- Annual Review of Ecology and Systematics, Vol. 24, Issue 1
Towards a more predictable plant breeding pipeline with CRISPR/Cas-induced allelic series to optimize quantitative and qualitative traits
journal, October 2018
- Scheben, Armin; Edwards, David
- Current Opinion in Plant Biology, Vol. 45
Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)
journal, January 2019
- Heyduk, Karolina; Hwang, Michelle; Albert, Victor
- Frontiers in Plant Science, Vol. 9
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
Adding resolution and dimensionality to comparative genomics: moving from reference genomes to clade genomics
journal, August 2018
- Rogers, Jeffrey
- Genome Biology, Vol. 19, Issue 1
Adaptive Evolution Involving Gene Duplication and Insertion of a Novel Ty1/copia-Like Retrotransposon in Soybean
journal, July 2009
- Kanazawa, Akira; Liu, Baohui; Kong, Fanjiang
- Journal of Molecular Evolution, Vol. 69, Issue 2
Crassulacean Acid Metabolism: A Curiosity in Context
journal, June 1978
- Osmond, C. B.
- Annual Review of Plant Physiology, Vol. 29, Issue 1
Kinetic Properties of Guard-Cell Phosphoenolpyruvate Carboxylase
journal, January 1990
- Outlaw, Jr., William H.
- Biochemie und Physiologie der Pflanzen, Vol. 186, Issue 5-6
Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage
journal, October 2017
- Gaudelli, Nicole M.; Komor, Alexis C.; Rees, Holly A.
- Nature, Vol. 551, Issue 7681
Shared origins of a key enzyme during the evolution of C4 and CAM metabolism
journal, March 2014
- Christin, Pascal-Antoine; Arakaki, Monica; Osborne, Colin P.
- Journal of Experimental Botany, Vol. 65, Issue 13
Light to liquid fuel: theoretical and realized energy conversion efficiency of plants using Crassulacean Acid Metabolism (CAM) in arid conditions
journal, April 2014
- Davis, Sarah C.; LeBauer, David S.; Long, Stephen P.
- Journal of Experimental Botany, Vol. 65, Issue 13
The genetics of convergent evolution: insights from plant photosynthesis
journal, March 2019
- Heyduk, Karolina; Moreno-Villena, Jose J.; Gilman, Ian S.
- Nature Reviews Genetics, Vol. 20, Issue 8
Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems
journal, February 2019
- Papikian, Ashot; Liu, Wanlu; Gallego-Bartolomé, Javier
- Nature Communications, Vol. 10, Issue 1