Diffusion of CO<sub>2</sub> across the Mesophyll-Bundle Sheath Cell Interface in a C<sub>4</sub> Plant with Genetically Reduced PEP Carboxylase Activity

Alonso-Cantabrana, Hugo; Danila, Florence R.; Ryan, Timothy A.; Sharwood, Robert E.; Caemmerer, Susanne von; Furbank, Robert T.

doi:10.1104/pp.18.00618

Cited by 28 publications

(43 citation statements)

References 38 publications

(25 reference statements)

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“…In Neurachne and Thyridolepis, MS cells have suberized outer walls and are surrounded by tightly packed PS cells, both of which can enhance resistance to diffusive efflux of CO 2 generated by decarboxylation of Gly or C 4 acids von Caemmerer and Furbank, 2003;Alonso-Cantabrana et al, 2018). In the MS of C 3 species, however, suberized walls and the PS sheath would reduce diffusive CO 2 influx and thus starve chloroplasts of CO 2 .…”

Section: A Model Of C 2 Evolution In the Neurachninaementioning

confidence: 99%

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

et al. 2019

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The Australian grass subtribe Neurachninae contains closely related species that use C 3 , C 4 , and C 2 photosynthesis. To gain insight into the evolution of C 4 photosynthesis in grasses, we examined leaf gas exchange, anatomy and ultrastructure, and tissue localization of Gly decarboxylase subunit P (GLDP) in nine Neurachninae species. We identified previously unrecognized variation in leaf structure and physiology within Neurachne that represents varying degrees of C 3 -C 4 intermediacy in the Neurachninae. These include inverse correlations between the apparent photosynthetic carbon dioxide (CO 2 ) compensation point in the absence of day respiration (C * ) and chloroplast and mitochondrial investment in the mestome sheath (MS), where CO 2 is concentrated in C 2 and C 4 Neurachne species; width of the MS cells; frequency of plasmodesmata in the MS cell walls adjoining the parenchymatous bundle sheath; and the proportion of leaf GLDP invested in the MS tissue. Less than 12% of the leaf GLDP was allocated to the MS of completely C 3 Neurachninae species with C * values of 56-61 mmol mol 21 , whereas twothirds of leaf GLDP was in the MS of Neurachne lanigera, which exhibits a newly-identified, partial C 2 phenotype with C * of 44 mmol mol 21 . Increased investment of GLDP in MS tissue of the C 2 species was attributed to more MS mitochondria and less GLDP in mesophyll mitochondria. These results are consistent with a model where C 4 evolution in Neurachninae initially occurred via an increase in organelle and GLDP content in MS cells, which generated a sink for photorespired CO 2 in MS tissues. 566

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Section: A Model Of C 2 Evolution In the Neurachninaementioning

confidence: 99%

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

et al. 2019

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“…At low intercellular CO 2 (C i ), the assimilation rate is largely limited by the rate of primary CO 2 fixation in mesophyll cells 45 , whilst at high C i , according to the C 4 photosynthesis model 46,47 , assimilation rate is co-limited by the amount and activity of Rubisco, the capacity for regeneration of either PEP or ribulose bisphosphate and the rate of whole leaf electron transport (the sum of electron transport rates of the two cell types). In line with the model, saturating rates of CO 2 assimilation were about 10% higher in plants with about 10% higher Rieske FeS abundance (and hence with higher electron transport rate as discussed above).…”

Section: Photosynthesis Is Co-limited By Electron Transport Capacitymentioning

confidence: 99%

Overexpression of the Rieske FeS protein of the Cytochromeb₆fcomplex increases C₄photosynthesis

Ermakova

Raines

et al. 2019

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C 4 plants contribute 20% to the global primary productivity despite representing only 4% of higher plant species. Their CO 2 concentrating mechanism operating between mesophyll and bundle sheath cells increases CO 2 partial pressure at the site of Rubisco and hence photosynthetic efficiency. Electron transport chains in both cell types supply ATP and NADPH for C 4 photosynthesis. Since Cytochrome b 6 f is a key point of control of electron transport in C 3 plants, we constitutively overexpressed the Rieske FeS subunit in Setaria viridis to study the effects on C 4 photosynthesis. Rieske FeS overexpression resulted in a higher content of Cytochrome b 6 f in both mesophyll and bundle sheath cells without marked changes in abundances of other photosynthetic complexes and Rubisco. Plants with higher Cytochrome b 6 f abundance showed better light conversion efficiency in both Photosystems and could generate higher proton-motive force across the thylakoid membrane. Rieske FeS abundance correlated with CO 2 assimilation rate and plants with a 10% increase in Rieske FeS content showed a 10% increase in CO 2 assimilation rate at ambient and saturating CO 2 and high light. Our results demonstrate that Cytochrome b 6 f controls the rate of electron transport in C 4 plants and that removing electron transport limitations can increase the rate of C 4 photosynthesis.

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“…Although PPC catalyses primary CO2 fixation in CAM and C4 plants, the only reported PPC mutants are for the C4 dicot Amaranthus edulis and the C4 monocot Setaria viridis (Dever et al, 1995;Alonso-Cantabrana et al, 2018). Loss of the C4 PPC isogene in A. edulis caused a severe and lethal growth phenotype in normal air, with the homozygous mutant plants only managing to reach flowering and set seed when grown at highly elevated CO2 (Dever et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

“…Loss of the C4 PPC isogene in A. edulis caused a severe and lethal growth phenotype in normal air, with the homozygous mutant plants only managing to reach flowering and set seed when grown at highly elevated CO2 (Dever et al, 1995). In S. viridis, the C4 PPC was reduced to very low levels using RNAi in transgenic lines (Alonso-Cantabrana et al, 2018). These lines grew very slowly even at 2 % CO2 (normal air is 0.04 %), and developed increased numbers of plasmodesmatal pit fields at the mesophyll-bundle sheath interface (Alonso-Cantabrana et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…In S. viridis, the C4 PPC was reduced to very low levels using RNAi in transgenic lines (Alonso-Cantabrana et al, 2018). These lines grew very slowly even at 2 % CO2 (normal air is 0.04 %), and developed increased numbers of plasmodesmatal pit fields at the mesophyll-bundle sheath interface (Alonso-Cantabrana et al, 2018). By contrast, no CAM mutants lacking PPC have been described, but transgenic lines of Kalanchoë lacking the lightperiod, decarboxylation pathway enzymes mitochondrial NAD-malic enzyme (NAD-ME) and pyruvate orthophosphate dikinase (PPDK) displayed a near complete loss of dark CO2 fixation and failed to turnover significant malate in the light period (Dever et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

Boxall

Kadu

Dever

et al. 2019

Preprint

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Short Title: Silencing PPC1 in an obligate CAM plant One Sentence Summary: Silencing phosphoenolpyruvate carboxylase in an obligate CAM species prevented dark period CO2 fixation and malate accumulation, caused arrhythmia of some components within the central circadian clock and enhanced rhythms of others, and adjusted the temporal regulation and relative abundance of guard cell signalling genes. ABSTRACT Unlike C3 plants, Crassulacean acid metabolism (CAM) plants fix CO2 in the dark using phosphoenolpyruvate carboxylase (PPC; EC 4.1.1.31). PPC combines PEP with CO2(as HCO3 -), forming oxaloacetate that is rapidly converted to malate, leading to vacuolar malic acid accumulation that peaks phased to dawn. In the light period, malate decarboxylation concentrates CO2 around RuBisCO for secondary fixation.CAM mutants lacking PPC have not been described. Here, RNAi was employed totranscripts, PPC activity, dark period CO2 fixation, and nocturnal malate accumulation.Light period stomatal closure was also perturbed, and the plants displayed reduced but detectable dark period stomatal conductance, and arrhythmia of the CAM CO2 fixation circadian rhythm under constant light and temperature (LL) free-running conditions. By contrast, the rhythm of delayed fluorescence was enhanced in plants lacking PPC1. Furthermore, a subset of gene transcripts within the central circadian oscillator were up-regulated and oscillated robustly. The regulation guard cell genes involved controlling stomatal movements was also altered in rPPC1-B. This provided direct evidence that altered regulatory patterns of key guard cell signaling genes are linked with the characteristic inverse pattern of stomatal opening and closing during CAM. RESULTS Initial Screening and Characterisation of PPC1 RNAi Lines of K. laxifloraAs K. laxiflora is relatively slow to grow, flower and set seed, taking around 9-months seed-to-seed (Hartwell et al., 2016), data are presented for independent primary transformants that were propagated clonally via leaf margin plantlets and/ or stem cuttings. Primary transformants were screened initially using high-throughput leaf disc tests for starch and acidity at dawn and dusk (Cushman et al., 2008; Dever et al., 2015). Independent transgenic lines that acidified less during the dark period were screened for the steady-state abundance of PPC1 transcripts using RT-qPCR. Line rPPC1-B displayed a complete loss of PPC1 transcripts, whereas rPPC1-A had an intermediate level of PPC1 transcripts ( Figure 1A). The other plant-type PPC genes (PPC2, PPC3 and PPC4) were up-regulated relative to the wild type, with their peak

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Diffusion of CO₂ across the Mesophyll-Bundle Sheath Cell Interface in a C₄ Plant with Genetically Reduced PEP Carboxylase Activity

Abstract: One-sentence summary: 15 RNAi reduction of PEP carboxylase activity in Setaria viridis results in low CO 2 assimilation 16 rates and increased plasmodesmata density at the mesophyll-bundle sheath interface.

Cited by 28 publications

References 38 publications

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

Overexpression of the Rieske FeS protein of the Cytochromeb₆fcomplex increases C₄photosynthesis

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

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Diffusion of CO2 across the Mesophyll-Bundle Sheath Cell Interface in a C4 Plant with Genetically Reduced PEP Carboxylase Activity

Abstract: One-sentence summary: 15 RNAi reduction of PEP carboxylase activity in Setaria viridis results in low CO 2 assimilation 16 rates and increased plasmodesmata density at the mesophyll-bundle sheath interface.

Cited by 28 publications

References 38 publications

The Evolutionary Origin of C4 Photosynthesis in the Grass Subtribe Neurachninae

The Evolutionary Origin of C4 Photosynthesis in the Grass Subtribe Neurachninae

Overexpression of the Rieske FeS protein of the Cytochromeb6fcomplex increases C4photosynthesis

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C3-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

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Diffusion of CO₂ across the Mesophyll-Bundle Sheath Cell Interface in a C₄ Plant with Genetically Reduced PEP Carboxylase Activity

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

The Evolutionary Origin of C₄ Photosynthesis in the Grass Subtribe Neurachninae

Overexpression of the Rieske FeS protein of the Cytochromeb₆fcomplex increases C₄photosynthesis

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes