A molecular pathway for CO2 response in Arabidopsis guard cells

Wang, Tian; Hou, Cheng; Ren, Zhijie; Pan, Ya‐Jun; Jia, Jinjin; Zhang, Haiwen; Bai, Fenglin; Zhang, Peng; Zhu, Huifen; He, Yulong; Luo, Shenglian; Li, Legong; Luan, Sheng

doi:10.1038/ncomms7057

Cited by 139 publications

(201 citation statements)

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“…Protective Role of Photorespiration TEMPERATURE 1 (HT1), and OPEN STOMATA 1 (OST1), and leads to stomatal closing if external CO 2 levels are raised and to stomatal opening if external CO 2 levels are lowered (Tian et al, 2015). Analyses of transcriptome data and transpiration rates both indicate that Arabidopsis CO 2 sensing returns to a new set point after about 5 days, at which time the ABA signal and the CO 2 signal are integrated in a way that prevents a drought response in leaves.…”

Section: Discussionmentioning

confidence: 99%

“…Work on stomatal opening and closing mechanisms (Hu et al, 2010;Xue et al, 2011;Tian et al, 2015) predicted stomatal opening upon reduced external CO 2 concentration. Using the apparent transpiration rates as a proxy for stomatal aperture, WT and hpr1 plants indeed showed the expected short-term response, i.e., stomatal opening.…”

Section: General Transcriptional Lc Response Overlaps Significantly Wmentioning

confidence: 99%

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Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

et al. 2017

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The photorespiratory pathway or photorespiration is an essential process in oxygenic photosynthetic organisms, which can reduce the efficiency of photosynthetic carbon assimilation and is hence frequently considered as a wasteful process. By comparing the response of the wild-type plants and mutants impaired in photorespiration to a shift in ambient CO 2 concentrations, we demonstrate that photorespiration also plays a beneficial role during short-term acclimation to reduced CO 2 availability. The wild-type plants responded with few differentially expressed genes, mostly involved in drought stress, which is likely a consequence of enhanced opening of stomata and concomitant water loss upon a shift toward low CO 2 . In contrast, mutants with impaired activity of photorespiratory enzymes were highly stressed and not able to adjust stomatal conductance to reduced external CO 2 availability. The transcriptional response of mutant plants was congruent, indicating a general reprogramming to deal with the consequences of reduced CO 2 availability, signaled by enhanced oxygenation of ribulose-1,5-bisphosphate and amplified by the artificially impaired photorespiratory metabolism. Central in this reprogramming was the pronounced reallocation of resources from growth processes to stress responses. Taken together, our results indicate that unrestricted photorespiratory metabolism is a prerequisite for rapid physiological acclimation to a reduction in CO 2 availability.

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Section: Discussionmentioning

confidence: 99%

Section: General Transcriptional Lc Response Overlaps Significantly Wmentioning

confidence: 99%

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

et al. 2017

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“…Moreover, this increase could be even faster by assuming an even larger CA activity at the membrane. One prediction of the above model, assuming that HCO 3 2 is the intracellular signal that transmits the CO 2 response (Xue et al, 2011;Tian et al, 2015), is that longer exposures to elevated CO 2 should enable stomata of ca1ca4 mutant plants to close to similar levels as wild-type plants but at a slowed rate. Because the rate of stomatal closing was found previously to be slowed in ca1ca4 mutant plants (Hu et al, 2010), we conducted experiments in which prolonged elevated CO 2 concentrations were applied.…”

Section: Reaction-diffusion Model Of Co 2 Influx Into Guard Cells Canmentioning

confidence: 99%

“…A current molecular genetic and physiological model of this pathway was proposed: elevated CO 2 accelerates the conversion by bCA1 and bCA4 into bicarbonate; elevated bicarbonate together with CO 2 act as an intracellular messenger to activate S-type anion channels through OST1, thus triggering closure of stomata (Xue et al, 2011). Recently, the RESISTANT TO HIGH CARBON DIOXIDE1 (RHC1) MULTIDRUG AND TOXIC COMPOUND EXTRUSION (MATE) transmembrane protein was reported to function as an HCO 3 2 sensing protein, interact with HT1, and release OST1 to phosphorylate SLAC1 channels (Tian et al, 2015). Beyond the function of bCA1 and bCA4 in CO 2 control of stomatal movements, bCA1 and bCA4 were also identified as functioning in CO 2 regulation of stomatal development together with the secreted EPIDERMAL PATTERNING FACTOR2 (EPF2) signaling peptide and a secreted protease CARBON DIOXIDE RESPONSE SECRETED PROTEASE (CRSP) in a distinct OST1-independent pathway (Engineer et al, 2014).…”

mentioning

confidence: 99%

Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

Rappel

Occhipinti

et al. 2015

Plant Physiol.

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ORCID IDs: 0000-0003-0538-6646 (H.H.); 0000-0001-6675-273X (M.B.).Elevated carbon dioxide (CO 2 ) in leaves closes stomatal apertures. Research has shown key functions of the b-carbonic anhydrases (bCA1 and bCA4) in rapid CO 2 -induced stomatal movements by catalytic transmission of the CO 2 signal in guard cells. However, the underlying mechanisms remain unclear, because initial studies indicate that these Arabidopsis (Arabidopsis thaliana) bCAs are targeted to distinct intracellular compartments upon expression in tobacco (Nicotiana benthamiana) cells. Which cellular location of these enzymes plays a key role in native guard cells in CO 2 -regulated stomatal movements remains unknown. Here, we express fluorescently tagged CAs in guard cells of ca1ca4 double-mutant plants and show that the specific locations of bCA4 at the plasma membrane and bCA1 in native guard cell chloroplasts each can mediate rapid CO 2 control of stomatal movements. Localization and complementation analyses using a mammalian aCAII-yellow fluorescent protein in guard cells further show that cytoplasmic localization is also sufficient to restore CO 2 regulation of stomatal conductance. Mathematical modeling of cellular CO 2 catalysis suggests that the dynamics of the intracellular HCO 3 2 concentration change in guard cells can be driven by plasma membrane and cytoplasmic localizations of CAs but not as clearly by chloroplast targeting. Moreover, modeling supports the notion that the intracellular HCO 3 2 concentration dynamics in guard cells are a key mechanism in mediating CO 2 -regulated stomatal movements but that an additional chloroplast role of CAs exists that has yet to be identified.

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“…3c). CO 2 and ABA-induced perception and signalling are interdependent and open stomata 1 (OST)/SNF-related protein kinase 2.6 (Aam349853), which is a downstream target of HT1 35 and a convergence point for ABA and CO 2 signalling pathways, also exhibited rescheduled expression in Agave compared to Arabidopsis (Fig. 3c).…”

mentioning

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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A molecular pathway for CO2 response in Arabidopsis guard cells

Cited by 139 publications

References 58 publications

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

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

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