Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Kubicki, Andreas; Funk, Edgar; Westhoff, Peter; Steinmüller, Klaus

doi:10.1007/bf00196569

Cited by 102 publications

(66 citation statements)

References 38 publications

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“…2 a and b). In contrast, in NADP-ME species, the ratio of NDH-H contents in mesophyll to bundle-sheath preparations was only 0.27 (Z. mays) and 0.61 (P. grandiflora), which is consistent with previous reports that NDH complex is greatly accumulated in bundle-sheath cells of the NADP-ME-type Sorgum bicolor and Z. mays (25,26). These results indicate that NDH-H is highly accumulated in cells that require a high level of ATP synthesis; i.e., mesophyll-sheath cells of NAD-ME species and bundlesheath cells of NADP-ME species.…”

Section: Resultssupporting

confidence: 92%

Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Takabayashi

Kishine

Asada

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

142

114

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Whereas linear electron flow (LEF) in photosynthesis produces both ATP and NADPH, the cyclic electron flow (CEF) around photosystem I has been shown to produce only ATP. Two alternative routes have been shown for CEF; NAD(P)H dehydrogenase (NDH)-and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flows, but their physiological relevance has not been elucidated in detail. Meanwhile, because C 4 photosynthesis requires more ATP than does C3 photosynthesis to concentrate CO2, it has not been clear how the extra ATP is produced. In this study, to elucidate whether CEF contributes to the additional ATP needed in C4 photosynthesis, we estimated the amounts of PGR5, which participates in FQR-dependent flow, and NDH-H, a subunit of NDH, in four C 4 species. Although the expression profiles of PGR5 did not correlate well with the additional ATP requirement, NDH was greatly expressed in mesophyll cells in the NAD-malic enzyme (ME) species, and in bundle-sheath cells in NADP-ME species, where there is a strong need for ATP in the respective cells. Our results indicate that CEF via NDH plays a central role in driving the CO2-concentrating mechanism in C4 photosynthesis.ATP synthesis ͉ ferredoxin:plastoquinone oxidoreductase ͉ NAD(P)H dehydrogenase ͉ PGR5 ͉ plant D uring plant photosynthesis, both ATP and NADPH are produced by the linear electron flow (LEF) using both photosystem (PS)I and PSII. Alternatively, ATP can also be produced by cyclic electron flow (CEF) without production of NADPH. Because the ratio of ATP͞NADPH required for CO 2 fixation changes, depending on activities of photorespiration or nitrate assimilation to glutamate, balancing between CEF and LEF is important to perform C 3 photosynthesis effectively (1-4).There are two known pathways of CEF around PSI; chloroplastic NAD(P)H dehydrogenase (NDH)-dependent flow and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flow. NDH complex was identified on the basis of high homology with respiratory complex I in bacteria and mitochondria, when plastid genomes of tobacco (5) and liverwort (6) were completely sequenced. To elucidate the function of NDH complex, several laboratories inactivated the tobacco ndh genes by the plastid transformation technique. Although NDH-inactivated tobacco plants showed normal growth under standard conditions (7-10), environmental stress, such as heat, high light, or decreased air humidity, causes retarded growth, suggesting that the absence of the ATP produced by NDH-dependent CEF makes it more difficult to adapt to changing environmental conditions (9,11,12).On the contrary, the molecular identity of FQR had not been revealed. However, a mutant analysis of Arabidopsis identified the protein PGR5, which is essential for FQR-mediated CEF, although PGR5 itself has no known redox motif (13).Involvement of PGR5 in FQR-mediated CEF is supported by the report that ssr2016 in Synechocystis sp. PCC 6803, homologue of Arabidopsis pgr5, is also required for FQR activity (14). Double mutants defective in both NDH-and FQR-depende...

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Section: Resultssupporting

confidence: 92%

Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Takabayashi

Kishine

Asada

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

142

114

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“…In C 3 plants, the NDH complex is of much lower abundance than the four major photosynthetic complexes (estimated at 0.2% of total thylakoid protein (66)). The plastid genome encodes for 11 putative NDH subunits (A-K), and several have been identified in both C 3 (67) and C 4 (15,18,68) plants. Recently five nucleus-encoded Ndh subunits (M, N, and O and CRR3 and -7) were identified in Arabidopsis (69 -71).…”

Section: Purification Of M and Bs Chloroplast Membranes Frommentioning

confidence: 99%

Consequences of C4 Differentiation for Chloroplast Membrane Proteomes in Maize Mesophyll and Bundle Sheath Cells

Majeran

Zybailov

Ytterberg

et al. 2008

Molecular & Cellular Proteomics

192

205

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Chloroplasts of maize leaves differentiate into specific bundle sheath (BS) and mesophyll (M) types to accommodate C 4 photosynthesis. Chloroplasts contain thylakoid and envelope membranes that contain the photosynthetic machineries and transporters but also proteins involved in e.g. protein homeostasis. These chloroplast membranes must be specialized within each cell type to accommodate C 4 photosynthesis and regulate metabolic fluxes and activities. This quantitative study determined the differentiated state of BS and M chloroplast thylakoid and envelope membrane proteomes and their oligomeric states using innovative gel-based and mass spectrometry-based protein quantifications. This included native gels, iTRAQ, and label-free quantification using an LTQ-Orbitrap. Subunits of Photosystems I and II, the cytochrome b 6 f, and ATP synthase complexes showed average BS/M accumulation ratios of 1.6, 0.45, 1.0, and 1.33, respectively, whereas ratios for the light-harvesting complex I and II families were 1.72 and 0.68, respectively. A 1000-kDa BS-specific NAD(P)H dehydrogenase complex with associated proteins of unknown function containing more than 15 proteins was observed; we speculate that this novel complex possibly functions in inorganic carbon concentration when carboxylation rates by ribulose-bisphosphate carboxylase/oxygenase are lower than decarboxylation rates by malic enzyme. In leaves of C 4 grasses such as maize (Zea mays), photosynthetic activities are partitioned between two morphologically and biochemically distinct bundle sheath (BS) 1 and mesophyll (M) cells. A single ring of BS cells surrounds the vascular bundle followed by a concentric ring of specialized M cells, creating the classical Kranz anatomy. C 4 differentiation occurs along a developmental gradient with proplastids at the leaf base and fully differentiated C 4 M and BS chloroplasts at the leaf tip. Genetic screens for mutants affected in BS differentiation identified various mutants (1-4). However, the molecular basis for C 4 differentiation is still poorly understood but includes transcriptional regulation through DNA regulatory elements, transcription factors, and likely also metabolic signals (5, 6). Differential accumulation of thylakoid proteases (Egy andDegP

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“…In C 4 plants, subunits of the Ndh complex have been reported to be much more strongly expressed in bundle sheath chloroplasts than in mesophyll chloroplasts (49). In bundle sheath chloroplasts, only low levels of PS II are detected.…”

Section: Measurement Of a Ps Ii-mediated Electron Flow To At-ptox In mentioning

confidence: 99%

Involvement of a Plastid Terminal Oxidase in Plastoquinone Oxidation as Evidenced by Expression of the Arabidopsis thaliana Enzyme in Tobacco

Joët¹,

Genty²,

Josse³

et al. 2002

Journal of Biological Chemistry

151

156

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Chlororespiration has been defined as a respiratory electron transport chain in interaction with photosynthetic electron transport involving both non-photochemical reduction and oxidation of plastoquinones. Different enzymatic activities, including a plastidencoded NADH dehydrogenase complex, have been reported to be involved in the non-photochemical reduction of plastoquinones. However, the enzyme responsible for plasquinol oxidation has not yet been clearly identified. In order to determine whether the newly discovered plastid oxidase (PTOX) involved in carotenoid biosynthesis acts as a plastoquinol oxidase in higher plant chloroplasts, the Arabidopsis thaliana PTOX gene (At-PTOX) was expressed in tobacco under the control of a strong constitutive promoter. We showed that At-PTOX is functional in tobacco chloroplasts and strongly accelerates the non-photochemical reoxidation of plastoquinols; this effect was inhibited by propyl gallate, a known inhibitor of PTOX. During the dark to light induction phase of photosynthesis at low irradiances, At-PTOX drives significant electron flow to O 2 , thus avoiding over-reduction of plastoquinones, when photosynthetic CO 2 assimilation was not fully induced. We proposed that PTOX, by modulating the redox state of intersystem electron carriers, may participate in the regulation of cyclic electron flow around photosystem I.

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Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Cited by 102 publications

References 38 publications

Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Consequences of C4 Differentiation for Chloroplast Membrane Proteomes in Maize Mesophyll and Bundle Sheath Cells

Involvement of a Plastid Terminal Oxidase in Plastoquinone Oxidation as Evidenced by Expression of the Arabidopsis thaliana Enzyme in Tobacco

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Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Cited by 102 publications

References 38 publications

Differential use of two cyclic electron flows around photosystem I for driving CO 2 -concentration mechanism in C 4 photosynthesis

Differential use of two cyclic electron flows around photosystem I for driving CO 2 -concentration mechanism in C 4 photosynthesis

Consequences of C4 Differentiation for Chloroplast Membrane Proteomes in Maize Mesophyll and Bundle Sheath Cells

Involvement of a Plastid Terminal Oxidase in Plastoquinone Oxidation as Evidenced by Expression of the Arabidopsis thaliana Enzyme in Tobacco

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Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis