Trends in Plant Science
ReviewSpecial Issue: Systems BiologyEngineering crassulacean acid metabolism to improve water-use efficiency
Section snippets
Photosynthesis for a parched planet
Earth's population is projected to exceed 9 billion by 2050. The consequent demands on agriculture for food, feed, fiber, and fuels, coupled with decreasing arable land area and increasing nitrogen and phosphate fertilizer requirements for crop production, all point to the need to produce more plant-derived biomass with reduced resource inputs [1]. Approximately 40% of the world's land area is considered arid, semi-arid, or dry sub-humid, with precipitation amounts that are inadequate for most
CAM – a strategic target for synthetic biology
The major plant inorganic CCMs in terrestrial vascular plants are CAM and C4 photosynthesis [22]. CAM arose through multiple independent evolutionary origins in at least 343 genera across 36 plant families representing >6% of higher plant species [23]. CAM resembles C4 photosynthesis in its use of C4 organic acids as storage intermediates during carbon fixation, but exploits a temporal separation of primary and secondary CO2 fixation. Furthermore, CAM maximizes WUE by concentrating CO2 around
Engineering of CAM
The development of bioenergy feedstocks and food crops engineered with the improved WUE of CAM plants complements the direct use of CAM species to supply human needs. CAM and C4 photosynthesis have been described as products of either parallel or convergent evolution of a complex trait with the implication that many, if not all, of the genes and some regulatory elements necessary for these photosynthetic specializations are already present in C3 species 23, 41, 42, 43. Such reasoning also
Probing phylogenetically diverse lineages to enable comparative CAM genomics
A fundamental requirement for engineered CAM is to first understand the minimal set of genes and proteins required for its efficient establishment and operation. Until recently, there has been a paucity of genome or transcriptome information available for CAM species. However, the genomic sequences and transcriptome atlases available from cycling, facultative, or obligate CAM species sampled from diverse phylogenetic origins should rapidly redefine our understanding of the molecular genetics of
Comparative CAM genomics
Comparative transcriptomic and genomic approaches can be used to discern CAM gene function by comparing the expression patterns of known CAM enzymes and transporters among closely related C3 and CAM species within the same genus or family that show C3, weak CAM or strong CAM [23]. Comparative genome and transcriptome sequencing studies of C3 and C4 model species from diverse taxonomic origins do not support the duplication or expansion of C4 pathway genes or the longstanding hypothesis that C4
Coexpression network modeling of CAM
A key challenge for the engineering of CAM into C3 plant species lies in understanding the temporal regulatory events controlling not only the core carboxylation–decarboxylation of C4 acids, but also the coincident metabolic fluxes through glycolysis–gluconeogenesis and storage carbohydrate synthesis and breakdown, as well as stomatal control, over the course of the day–night cycle as illustrated in Figure 3A. A multilayer approach incorporating transcriptional data, functional genomics
Biodesign of CAM modules
Although network-modeling approaches can provide information about new candidate genes by virtue of their association with known genes within a functional module, empirical testing of minimal functional modules, coupled with information from loss-of-function studies of individual enzymes, regulatory proteins, or transcription factors can provide important empirical information about the basic genetic requirements for CAM biodesign. For simplicity, a set of discrete functional modules for
Identifying target host species
Initial CAM biodesign efforts will target the genetic model Arabidopsis, or close relatives, owing to its rapid growth rate and ease of transformation. With regard to bioenergy feedstocks, preferred targets are rapid-cycling C3 crops such as members of the Brassicaceae, particularly oilseed crops, and fast-growing woody plants within the Populus genus, which are used extensively in the timber, pulp, and paper industries and more recently as a bioenergy crop. There are many genetic and genomic
Moving complex traits into target host species
Many biological processes are controlled by gene modules comprising an array of genes 120, 121. Similarly, complex trait engineering, such as the proposed CAM engineering project outlined here, will require the use of multigene stacking technologies. Most plant genetic engineering attempts have been limited to the introduction of one or a few genes at a time [122]. To address this limitation, new methods have been developed recently to assemble multigene plant transformation vectors that
Concluding remarks and future directions
The ability of succulent CAM species, such as Agave and Opuntia, to maintain high biomass productivities with water input of only 20% of that required by C3 or C4 crops has drawn attention to their possible use as feedstocks for biofuel production. Indeed, such CAM species can be grown in areas where precipitation is typically insufficient to support C3 or C4 crops. Thus, exploring the agricultural uses of CAM species should bear fruit as global warming continues to erode finite arable land and
Acknowledgments
This Review is based on work supported by the DOE, Office of Science, Genomic Science Program under Award Number DE-SC0008834. The M. crystallinum transcriptome and mRNA expression data were supported by the National Science Foundation, USA (IOS-084373 awarded to K.A.S. and J.C.C.). The K. fedtschenkoi sequencing and CAM functional genomics project was supported by the Biotechnology and Biological Sciences Research Council, UK (BB/F009313/1 awarded to J.H.). This publication was also made
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