Pyruvate, Pi Dikinase in Bundle Sheath Strands as Well as in Mesophyll Cells in Maize Leaves

Aoyagi, Kazuko; Nakamoto, Hitoshi

doi:10.1104/pp.78.3.661

Cited by 51 publications

(41 citation statements)

References 18 publications

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“…For the analysis in this article, nine biologically independent preparations (pairs of BS and M) were used with cross-contamination levels between 5 and 15% but without any significant nonchloroplast contaminations. The cross-contamination of the BS chloroplasts by the M fraction was lower than we calculated, since it was shown that 10% of a light-independent PPDK form can accumulate in BS cells (Aoyagi and Nakamoto, 1985;Sheen andBogorad, 1987a, 1987b). We deliberately did not use other types of BS/M preparations involving long enzymatic digestions of cell walls, likely resulting in unwanted induction of stress proteins.…”

Section: Purification Of Bs and M Chloroplasts From Leaf Tips Of Youncontrasting

confidence: 52%

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

et al. 2005

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Chloroplasts of maize (Zea mays) leaves differentiate into specific bundle sheath (BS) and mesophyll (M) types to accommodate C4 photosynthesis. Consequences for other plastid functions are not well understood but are addressed here through a quantitative comparative proteome analysis of purified M and BS chloroplast stroma. Three independent techniques were used, including cleavable stable isotope coded affinity tags. Enzymes involved in lipid biosynthesis, nitrogen import, and tetrapyrrole and isoprenoid biosynthesis are preferentially located in the M chloroplasts. By contrast, enzymes involved in starch synthesis and sulfur import preferentially accumulate in BS chloroplasts. The different soluble antioxidative systems, in particular peroxiredoxins, accumulate at higher levels in M chloroplasts. We also observed differential accumulation of proteins involved in expression of plastid-encoded proteins (e.g., EF-Tu, EF-G, and mRNA binding proteins) and thylakoid formation (VIPP1), whereas others were equally distributed. Enzymes related to the C4 shuttle, the carboxylation and regeneration phase of the Calvin cycle, and several regulators (e.g., CP12) distributed as expected. However, enzymes involved in triose phosphate reduction and triose phosphate isomerase are primarily located in the M chloroplasts, indicating that the M-localized triose phosphate shuttle should be viewed as part of the BS-localized Calvin cycle, rather than a parallel pathway.

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Section: Purification Of Bs and M Chloroplasts From Leaf Tips Of Youncontrasting

confidence: 52%

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

et al. 2005

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“…Furthermore, in the present study we demonstrated that not only the carboxylases, but also other photosynthetic enzymes, have an atypical intercellular compartmentation compared to C4 plants. Recently, a low amount of PPDK protein was also found in maize (an NADP-ME type monocot) leaf BSC, but it is not certain if the enzyme is active, since an immunoblot method was used to locate PPDK (1). The enzyme distribution of PEPC, PPDK, Rubisco, and NADP-ME contrasts markedly with that found in G. celosioides, another NADP-ME type C4 dicot (31).…”

mentioning

confidence: 99%

Photosynthesis in Flaveria brownii, a C₄-Like Species

Cheng¹,

Moore²,

Edwards³

et al. 1988

Plant Physiol.

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In contrast, activities of ribulose 1,5-bisphosphate carboxylase, other C3 cycle enzymes, and NADP-malHc enzyme showed a reverse gradation, although there were significant activities of these enzymes in mesophyll cells. As indicated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis, the banding pattern of certain polypeptides of the total soluble proteins from the three cell types also supported the distribution pattern obtained by activity assays of these enzymes. Analysis of initial 14C products in whole leaves and extrapolation of pulse-labeling curves to zero time indicated that about 80% of the CO2 is fixed into C4 acids (malate and aspartate), whereas about 20% of the CO2 directly enters the C3 cycle. This is consistent with the high activity of enzymes for C02 rfation by the C4 pathway and the substantial activity of enzymes of the C3 cycle in the mesophyll cells. Therefore, F. brownii appears to have some capacity for C3 photosynthesis in the mesophyll cells and should be considered a C4-like species.A diagnostic feature of C4 photosynthesis is the fixation of atmospheric CO2 into C4 dicarboxylic acids in the leafMC,2 with * 'This work was supported in part by a Washington State University summer research assistantship to S.-H.C. and by National Science Foundation Grant DMB-8506197.

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“…These enzymes are synthesized cytoplasmically in a cell-specific manner and subsequently subcompartmentalized such that MDH and PPdK are found in M cell chloroplasts, PEPCase in M cell cytoplasm, and ME and RuBPCase in BS cell chloroplasts (Edwards and Huber 1979;Broglie et al 1984). PPdK has also been detected in BS cell chloroplasts, but its function in these cells is unknown (Aoyagi and Nakamoto 1985).…”

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Cellular pattern of photosynthetic gene expression in developing maize leaves.

Langdale¹,

Rothermel²,

Nelson³

1988

Genes Dev.

154

116

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Leaf development in C4 plants such as maize involves the differentiation of two photosynthetic cell types [bundle sheath (BS) and mesophyll (M)] to form Kranz-type leaf anatomy. This cellular dimorphism partitions photosynthetic activities so that each enzyme of the C4 pathway accumulates only in the appropriate cell type. We have exploited this property to study BS and M cell interactions in developing maize leaves. Our previous studies showed that C4 proteins appear concurrently with the appearance of Kranz anatomy. To look at earlier events in BS and M cell development we have used three of the corresponding C4 mRNAs as cell-specific markers. We have followed, in situ, the accumulation of malic enzyme (ME), phosphoenolpyruvate carboxylase (PEPCase), and ribulose bisphosphate carboxylase (RuBPCase) mRNAs in developing leaves of both normal and mutant argentia (ar) maize. We have isolated a partial cDNA clone for maize ME to examine ME mRNA expression. We show that throughout the development of light-grown seedlings, all three mRNAs accumulate in a cell-specific fashion in both normal and ar leaves. The pattern of C4 mRNA accumulation longitudinally along the veins, laterally across the leaf, and locally around individual veins reveals the spatial and temporal sequence of BS and M cell development. BS cell-specific mRNAs accumulate around developing veins before Kranz anatomy is evident morphologically. Our analysis of the ar mutant, in which C4 mRNA appearance is delayed relative to the appearance of Kranz anatomy, demonstrates first that BS and M cells develop in clusters across the leaf blade and second that BS cells surrounding any individual vein are activated asynchronously. We discuss our results in relation to models and mechanisms of BS and M cell development.

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Pyruvate, Pi Dikinase in Bundle Sheath Strands as Well as in Mesophyll Cells in Maize Leaves

Cited by 51 publications

References 18 publications

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

Photosynthesis in Flaveria brownii, a C₄-Like Species

Cellular pattern of photosynthetic gene expression in developing maize leaves.

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Pyruvate, Pi Dikinase in Bundle Sheath Strands as Well as in Mesophyll Cells in Maize Leaves

Cited by 51 publications

References 18 publications

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics

Photosynthesis in Flaveria brownii, a C4-Like Species

Cellular pattern of photosynthetic gene expression in developing maize leaves.

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Product

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Photosynthesis in Flaveria brownii, a C₄-Like Species