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Reduced-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana

II. Study of the mechanisms which regulate photosynthate partitioning

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Abstract

(i) We have studied the influence of reduced phosphoglucose-isomerase (PGI) activity on photosynthetic carbon metabolism in mutants of Clarkia xantiana Gray (Onagraceae). The mutants had reduced plastid (75% or 50% of wildtype) or reduced cytosolic (64%, 36% or 18% of wildtype) PGI activity. (ii) Reduced plastid PGI had no significant effect on metabolism in low light. In high light, starch synthesis decreased by 50%. There was no corresponding increase of sucrose synthesis. Instead glycerate-3-phosphate, ribulose-1,5-bisphosphate, reduction of QA (the acceptor for photosystem II) and energy-dependent chlorophyll-fluorescence quenching increased, and O2 evolution was inhibited by 25%. (iii) Decreased cytosolic PGI led to lower rates of sucrose synthesis, increased fructose-2,6-bisphosphate, glycerate-3-phosphate and ribulose-1,5-bisphosphate, and a stimulation of starch synthesis, but without a significant inhibition of O2 evolution. Partitioning was most affected in low light, while the metabolite levels changed more at saturating irradiances. (iv) These results provide decisive evidence that fructose-2,6-bisphosphate can mediate a feedback inhibition of sucrose synthesis in response to accumulating hexose phosphates. They also provide evidence that the ensuing stimulation of starch synthesis is due to activation of ADP-glucose pyrophosphorylase by a rising glycerate-3-phosphate: inorganic phosphate ratio, and that this can occur without any loss of photosynthetic rate. However the effectiveness of these mechanisms varies, depending on the conditions. (v) These results are analysed using the approach of Kacser and Burns (1973, Trends Biochem. Sci. 7, 1149–1161) to provide estimates for the elasticities and flux-control coefficient of the cytosolic fructose-1,6-bisphosphatase, and to estimate the gain in the fructose-2,6-bisphosphate regulator cycle during feedback inhibition of sucrose synthesis.

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Abbreviations

Chl:

chlorophyll

Fru6P:

fructose-6-phosphate

Frul,6bisP:

fructose-1,6-bisphosphate

Fru-1,6Pase:

fructose-1,6-bisphosphatase

Fru2,6bisP:

fructose-2,6-bisphosphate

Fru2,6Pase:

fructose-2,6-bisphosphatase

Glc6P:

glucose-6-phosphate

PGI:

phosphoglucose isomerase

Pi:

inorganic phosphate

QA :

acceptor for photosystem II

Ru1,5bisP:

ributose-1,5-bisphosphate

SPS:

sucrose-phosphate synthase

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Authors and Affiliations

  1. Lehrstuhl für Pflanzenphysiologie, Universität Bayreuth, Postfach 10 12 51, D-8580, Bayreuth, Federal Republic of Germany

    H. Ekkehard Neuhaus, Regina Feil & Mark Stitt

  2. Department of Genetics, University of California, 95616, Davis, CA, USA

    Arthur L. Kruckeberg

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  1. H. Ekkehard Neuhaus
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  2. Arthur L. Kruckeberg
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  3. Regina Feil
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  4. Mark Stitt
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Neuhaus, H.E., Kruckeberg, A.L., Feil, R. et al. Reduced-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana . Planta 178, 110–122 (1989). https://doi.org/10.1007/BF00392534

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