Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism

Ceusters, Johan; Borland, Anne M.; Taybi, Tahar; Frans, Mario; Godts, Christof; Proft, M.P. De

doi:10.1093/jxb/eru185

Cited by 38 publications

(34 citation statements)

References 60 publications

(72 reference statements)

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“…Refinement of CAM may take the form of improving secondary metabolic processes or genomic characteristics that allow for strong and constitutive CAM to exist. For example, fine tuning of carbohydrate turnover is necessary for CAM function (Borland et al, 2016; Ceusters et al, 2014). Experiments placing Mesembryanthemum crystallinum in CO 2 -free air at night resulted in a dampened CAM cycle (Dodd et al, 2003) and comparative RNA-seq in facultative CAM and C 3 /CAM comparisons has shown increased reliance on carbohydrate breakdown as CAM function increases (Brilhaus et al, 2016; Heyduk et al, 2018a).…”

Section: Discussionmentioning

confidence: 99%

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Heyduk¹,

Hwang²,

Silvera

et al. 2018

Preprint

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Crassulacean acid metabolism (CAM) photosynthesis is a modification of the core C3 photosynthetic pathway that improves the ability of plants to assimilate carbon in water-limited environments. CAM plants fix CO2 mostly at night, when transpiration rates are low. All of the CAM pathway genes exist in ancestral C3 species, but the timing and magnitude of expression are greatly altered between C3 and CAM species. Understanding these regulatory changes is key to elucidating the mechanism by which CAM evolved from C3. Here we use two closely related species in the Orchidaceae, Erycina pusilla (CAM) and Erycina crista-galli (C3), to conduct comparative transcriptomic analyses across multiple time points. Clustering of genes with expression variation across the diel cycle revealed some canonical CAM pathway genes similarly expressed in both species, regardless of photosynthetic pathway. However, gene network construction indicated that 149 gene families had significant differences in network connectivity and were further explored for these functional enrichments. Genes involved in light sensing and ABA signaling were some of the most differently connected genes between the C3 and CAM Erycina species, in agreement with the contrasting diel patterns of stomatal conductance in C3 and CAM plants. Our results suggest changes to transcriptional cascades are important for the transition from C3 to CAM photosynthesis in Erycina.

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Section: Discussionmentioning

confidence: 99%

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Heyduk¹,

Hwang²,

Silvera

et al. 2018

Preprint

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“…Various stimuli can lead to stomatal closure, but stomatal opening is predominately evoked by means of wavelength-responsive mechanisms 27 . The regulatory mechanism of stomatal opening by blue light has been well studied in a number of C 3 plants 28,29 , but its role is less clear in CAM plants 30 light-induced switch from C 3 to CAM in Clusia minor 31 . In the present study, we observed a light-induced gene expression profile for a blue/UV-A light-absorbing cryptochrome 2 (CRY2) (Aam348626) that has been implicated in inhibition of hypocotyl elongation, regulation of flowering time and entrainment of the circadian clock 32 .…”

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confidence: 99%

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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“…PEPC activity can be regulated according to a circadian clock and modulated according to environmental stresses [58,59]. The regulatory gene expression can be influenced by several environmental parameters, including the level of salinity, the light intensity at the different wave bands [60], and the temperature. As a results of the specific features of PEPCs, CAM plants are very plastic organisms, as they finely regulate the amplitude of malic acid change and the amount of day versus night CO 2 fixation in relation to the peculiar combination of internal conditions and environmental factors [46].…”

Section: Discussionmentioning

confidence: 99%

Colonization of a Deglaciated Moraine: Contrasting Patterns of Carbon Uptake and Release from C3 and CAM Plants

Elisa¹,

Zanotelli²,

Montagnani³

et al. 2016

PLoS ONE

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IntroductionCurrent glacier retreat makes vast mountain ranges available for vegetation establishment and growth. As a result, carbon (C) is accumulated in the soil, in a negative feedback to climate change. Little is known about the effective C budget of these new ecosystems and how the presence of different vegetation communities influences CO2 fluxes.MethodsOn the Matsch glacier forefield (Alps, Italy) we measured over two growing seasons the Net Ecosystem Exchange (NEE) of a typical grassland, dominated by the C3 Festuca halleri All., and a community dominated by the CAM rosettes Sempervivum montanum L. Using transparent and opaque chambers, with air temperature as the driver, we partitioned NEE to calculate Ecosystem Respiration (Reco) and Gross Ecosystem Exchange (GEE). In addition, soil and vegetation samples were collected from the same sites to estimate the Net Ecosystem Carbon Balance (NECB).ResultsThe two communities showed contrasting GEE but similar Reco patterns, and as a result they were significantly different in NEE during the period measured. The grassland acted as a C sink, with a total cumulated value of -46.4±35.5 g C m-2 NEE, while the plots dominated by the CAM rosettes acted as a source, with 31.9±22.4 g C m-2. In spite of the different NEE, soil analysis did not reveal significant differences in carbon accumulation of the two plant communities (1770±130 for F. halleri and 2080±230 g C m-2 for S. montanum), suggesting that processes often neglected, like lateral flows and winter respiration, can have a similar relevance as NEE in the determination of the Net Ecosystem Carbon Balance.

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Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism

Abstract: SummaryBesides the acknowledged roles of red light, blue light is a key determinant for synchronizing the metabolic and physiological components of CAM over the day/night cycle.

Cited by 38 publications

References 60 publications

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

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

Colonization of a Deglaciated Moraine: Contrasting Patterns of Carbon Uptake and Release from C3 and CAM Plants

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Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism

Abstract: SummaryBesides the acknowledged roles of red light, blue light is a key determinant for synchronizing the metabolic and physiological components of CAM over the day/night cycle.

Cited by 38 publications

References 60 publications

Altered Gene Regulatory Networks are Associated with the Transition from C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Altered Gene Regulatory Networks are Associated with the Transition from C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

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

Colonization of a Deglaciated Moraine: Contrasting Patterns of Carbon Uptake and Release from C3 and CAM Plants

Contact Info

Product

Resources

About

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)