Differential biogenesis of photosystem‐II in mesophyll and bundle‐sheath cells of ‘malic’ enzyme NADP<sup>+</sup>‐type C<sub>4</sub> plants

Oswald, Angela; Streubel, Monika; Ljungberg, Ulf; Hermans, J.; Eskins, Kenneth; Westhoff, Peter

doi:10.1111/j.1432-1033.1990.tb15563.x

Cited by 50 publications

(43 citation statements)

References 43 publications

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“…2 a and d), consistent with previous results (23). Because the intersystem electron carrier cytochrome b 6 ͞f complex participates in both LEF and CEF, its contents should not be affected by PSI͞PSII and show good correlation with PSI (24).…”

Section: Resultssupporting

confidence: 80%

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.

143

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: 80%

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.

143

114

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“…These large PSII complexes likely represent the active PSII complexes. We also note that accumulation of oxygen-evolving complex proteins was more strongly reduced to about 15% (12,14). Based on some of the older literature (see the Introduction), one could have expected that the observed PSII protein levels in BS thylakoids would be even more reduced than observed here.…”

Section: Purification Of M and Bs Chloroplast Membranes Frommentioning

confidence: 61%

“…As a consequence, BS thylakoids mostly carry out cyclic electron flow and have low rates of linear electron flow (9 -11). After several conflicting reports on protein levels of PSII and light-harvesting complex (LHC) II (11)(12)(13), a subsequent study partially clarified both activity and protein accumulation levels of PSI and PSII complexes in BS and M thylakoids (14). However, a more comprehensive overview of accumulation levels and assembly state of the thylakoidbound photosynthetic apparatus remains to be determined.…”

mentioning

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

196

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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“…After a final Qurification by SDS-gel electrophoresis and elution of the desired band, the fusion protein was used to elicit antibodies in rabbits according to standard procedures (Harlow and Lane 1988). The antibodies against DI (PSII-A), CP47 (PSII-B) and PSI-A from spinach are described in Oswald et al (1990).…”

Section: S Berger Et A!: Studies On the Expression Of Noh-hmentioning

confidence: 99%

Studies on the expression of NDH-H, a subunit of the NAD(P)H-plastoquinone-oxidoreductase of higher-plant chloroplasts

Berger

Ellersiek

Westhoff

et al. 1993

Planta

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Abstract. The plastid genomes of higher plants contain eleven reading frames (ndhA-K) that are homologous to genes encoding subunits of the mitochondrial NADHubiquinone-oxidoreductase (complex I). The carboxyterminal end of the NDH-H subunit from rice (Oryza sativa L.) was expressed as a fusion protein in Escherichia coli and antibodies against the fusion protein were generated in rabbits. The antibody was used to study the expression of NDH-H, and the following results were obtained: (i) NDH-H is expressed in mono-and dicotyledonous plants, (ii) NDH-H is localized on the stroma lamellae of the thylakoid membrane and (iii) NDH-H is expressed in etioplasts. Together with the finding that two other ndh genes (ndhI and ndhK) are expressed in plastids, these results point to the existence of an NAD(P)H-plastoquinone-oxidoreductase on the thylakoid membrane. The possible function of the enzyme in plastids is discussed and it is suggested that it works in balancing the ATP/ADP and the NADPH/NADP ratios during changing external (i.e. light) or internal (i.e. ATP and NADPH demands of biosynthetic pathways of the plastid) conditions.

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Differential biogenesis of photosystem‐II in mesophyll and bundle‐sheath cells of ‘malic’ enzyme NADP⁺‐type C₄ plants

Cited by 50 publications

References 43 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

Studies on the expression of NDH-H, a subunit of the NAD(P)H-plastoquinone-oxidoreductase of higher-plant chloroplasts

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Differential biogenesis of photosystem‐II in mesophyll and bundle‐sheath cells of ‘malic’ enzyme NADP+‐type C4 plants

Cited by 50 publications

References 43 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

Studies on the expression of NDH-H, a subunit of the NAD(P)H-plastoquinone-oxidoreductase of higher-plant chloroplasts

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Differential biogenesis of photosystem‐II in mesophyll and bundle‐sheath cells of ‘malic’ enzyme NADP⁺‐type C₄ plants

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