Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification

Christopher, Jack; Holtum, Joseph A. M.

doi:10.1104/pp.112.1.393

Cited by 89 publications

(60 citation statements)

References 25 publications

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“…By comparing Agave and Arabidopsis leaves under comparable growth conditions, we were able to examine rescheduled components of C 3 -and CAM-specific gene expression controlling other processes. Comparison of sucrose abundance at different times of day lends further support to the premise that this carbon source is broken down in Agave at the end of the light period to release glucose and fructose, which supply the PEP for nocturnal carbon fixation, as in other Agave species 45 . Overall, the nocturnal increases in malic acid, fumaric acid and NADP + in Agave are consistent with the reportedly high mitochondrial fluxes of carbon and electron transport that occur in CAM plants at night.…”

Section: Discussionmentioning

confidence: 59%

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

et al. 2016

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Already a proven mechanism for drought resilience, crassulacean acid metabolism (CAM) is a specialized type of photosynthesis that maximizes water-use efficiency by means of an inverse (compared to C 3 and C 4 photosynthesis) day/ night pattern of stomatal closure/opening to shift CO 2 uptake to the night, when evapotranspiration rates are low. A systems-level understanding of temporal molecular and metabolic controls is needed to define the cellular behaviour underpinning CAM. Here, we report high-resolution temporal behaviours of transcript, protein and metabolite abundances across a CAM diel cycle and, where applicable, compare the observations to the well-established C 3 model plant Arabidopsis. A mechanistic finding that emerged is that CAM operates with a diel redox poise that is shifted relative to that in Arabidopsis. Moreover, we identify widespread rescheduled expression of genes associated with signal transduction mechanisms that regulate stomatal opening/closing. Controlled production and degradation of transcripts and proteins represents a timing mechanism by which to regulate cellular function, yet knowledge of how this molecular timekeeping regulates CAM is unknown. Here, we provide new insights into complex post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets provide a resource to inform efforts to engineer more efficient CAM traits into economically valuable C 3 crops.T he water-use efficiency of Agave spp. hinges on crassulacean acid metabolism (CAM), a specialized mode of photosynthesis that evolved from ancestral C 3 photosynthesis in response to water and CO 2 limitation 1 and is found in ∼6.5% of higher plants. Whereas C 3 photosynthesis produces a three-carbon (3-C) molecule for carbon fixation during the day, CAM generates a four-carbon organic acid from carbon fixation at night. In CAM, this nocturnal carboxylation reaction is catalysed by phosphoenolpyruvate carboxylase (PEPC), and the 3-C substrate phosphoenolpyruvate (PEP) is supplied by the glycolytic breakdown of carbohydrate formed during the previous day. The nocturnally accumulated malic acid is stored overnight in a central vacuole, and during the subsequent day malate is decarboxylated to release CO 2 at an elevated concentration for Rubisco in the chloroplast. The diel separation of carboxylases in CAM is accompanied by an inverse (compared with C 3 and C 4 photosynthesis-performing species) day/night pattern of stomatal closure/ opening that results in improved water-use efficiency (CO 2 fixed per unit water lost) that is up to sixfold higher than that of C 3 photosynthesis plants and up to threefold higher than that of C 4 photosynthesis plants under comparable conditions 2 .The frequent emergence of CAM from C 3 photosynthesis throughout evolutionary history implies that all of the enzymes required for CAM are homologues of ancestral forms found in C 3 species 1,3 . As such, the CAM pathway has been identified as a target for synthetic biology because it offers the potential to engin...

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Section: Discussionmentioning

confidence: 59%

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

et al. 2016

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“…This decarboxylation can lead to generation of internal leaf CO 2 partial pressures greater than 100 times atmospheric levels (Cockburn et al 1979;Spalding et al 1979), reduction in stomatal opening and transpiration and sometimes even release of CO 2 from the leaf despite low stomatal conductance (Frimert et al 1986). Decarboxylation is catalysed by either cytosolic PEP carboxykinase (PEPCK) or cytosolic NADP + -and/or mitochondrial NAD + -malic enzymes (ME) (Smith and Bryce 1992;Christopher and Holtum 1996;Holtum et al 2005). This CO 2 -concentrating mechanism or 'CO 2 pump' effectively suppresses photorespiration during this phase.…”

Section: Phases Of Cammentioning

confidence: 99%

“…sucrose, glucose, fructose) and polysaccharides (e.g. fructan, galactomannan) in extra-chloroplastic compartments, while other species store both plastidic starch and cytoplasmic glucose (Christopher and Holtum 1996). Detailed studies have revealed at least eight distinct combinations of malate decarboxylation and carbohydrate storage strategies in CAM plants (Christopher and Holtum 1996).…”

Section: Molecular Markers For Studying Cam Evolutionmentioning

confidence: 99%

Evolution along the crassulacean acid metabolism continuum

Silvera

Neubig

Whitten

et al. 2010

Functional Plant Biol.

197

199

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Abstract. Crassulacean acid metabolism (CAM) is a specialised mode of photosynthesis that improves atmospheric CO 2 assimilation in water-limited terrestrial and epiphytic habitats and in CO 2 -limited aquatic environments. In contrast with C 3 and C 4 plants, CAM plants take up CO 2 from the atmosphere partially or predominantly at night. CAM is taxonomically widespread among vascular plants and is present in many succulent species that occupy semiarid regions, as well as in tropical epiphytes and in some aquatic macrophytes. This water-conserving photosynthetic pathway has evolved multiple times and is found in close to 6% of vascular plant species from at least 35 families. Although many aspects of CAM molecular biology, biochemistry and ecophysiology are well understood, relatively little is known about the evolutionary origins of CAM. This review focuses on five main topics: (1) the permutations and plasticity of CAM, (2) the requirements for CAM evolution, (3) the drivers of CAM evolution, (4) the prevalence and taxonomic distribution of CAM among vascular plants with emphasis on the Orchidaceae and (5) the molecular underpinnings of CAM evolution including circadian clock regulation of gene expression.

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“…It is not known whether the TR-δ 13 C relationship differs between terrestrial leaf and stem succulents and epiphytic CAM species or between groupings of CAM species based on other criteria such as growth altitude, taxonomic affiliation or CAM metabolic variant (Christopher and Holtum 1996). For example, in C 4 species TR differed significantly between 9 NAD-ME and 9 NADP-ME species when plants were water-stressed but not when well watered (Ghannoum et al 2002).…”

Section: Correlations Between Tr δ 13 C and Nocturnal Co 2 Gainmentioning

confidence: 99%

Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism

Winter

Aranda

Holtum

2005

Functional Plant Biol.

117

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Abstract.The relationship between water-use efficiency, measured as the transpiration ratio (g H 2 O transpired g −1 above-plus below-ground dry mass accumulated), and 13 C / 12 C ratio (expressed as δ 13 C value) of bulk biomass carbon was compared in 15 plant species growing under tropical conditions at two field sites in the Republic of Panama. The species included five constitutive crassulacean acid metabolism (CAM) species [Aloe vera (L.) Webb & Berth., Ananas comosus (L.) Merr., Euphorbia tirucalli L., Kalanchoë daigremontiana Hamet et Perr., Kalanchoë pinnata (Lam.) Pers.], two species of tropical C 3 trees (Tectona grandis Linn. f. and Swietenia macrophylla King), one C 4 species (Zea mays L.), and seven arborescent species of the neotropical genus Clusia, of which two exhibited pronounced CAM. The transpiration ratios of the C 3 and CAM species, which ranged between 496 g H 2 O g −1 dry mass in the C 3 -CAM species Clusia pratensis Seeman to 54 g H 2 O g −1 dry mass in the constitutive CAM species Aloe vera, correlated strongly with δ 13 C values and nocturnal CO 2 gain suggesting that δ 13 C value can be used to estimate both water-use efficiency and the proportion of CO 2 gained by CAM species during the light and the dark integrated over the lifetime of the tissues.

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Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification

Cited by 89 publications

References 25 publications

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

Evolution along the crassulacean acid metabolism continuum

Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism

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