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Maltose is the major form of carbon exported from the chloroplast at night

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Abstract

Transitory starch is formed in chloroplasts during the day and broken down at night. We investigated carbon export from chloroplasts resulting from transitory-starch breakdown. Starch-filled chloroplasts from spinach (Spinacia oleracea L. cv. Nordic IV) were isolated 1 h after the beginning of the dark period and incubated for 2.5 h, followed by centrifugation through silicone oil. Exported products were measured in the incubation medium to avoid measuring compounds retained inside the chloroplasts. Maltose and glucose made up 85% of the total exported products and were exported at rates of 626 and 309 nmol C mg−1 chlorophyll h−1, respectively. Net export of phosphorylated products was less than 5% and higher maltodextrins were not detected. Maltose levels in leaves of bean (Phaseolus vulgaris L. cv. Linden), spinach, and Arabidopsis thaliana (L.) Heynh. were low in the light and high in the dark. Maltose levels remained low and unchanged during the light/dark cycle in two starch-deficient Arabidopsis mutants, stf1, deficient in plastid phosphoglucomutase, and pgi, deficient in plastid phosphoglucoisomerase. Through the use of nonaqueous fractionation, we determined that maltose was distributed equally between the chloroplast and cytosolic fractions during darkness. In the light there was approximately 24% more maltose in the cytosol than the chloroplast. Taken together these data indicate that maltose is the major form of carbon exported from the chloroplast at night as a result of starch breakdown. We hypothesize that the hydrolytic pathway for transitory-starch degradation is the primary pathway used when starch is being converted to sucrose and that the phosphorolytic pathway provides carbon for other purposes.

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Abbreviations

CAM:

crassulacean acid metabolism

Chl:

chlorophyll

DHAP:

dihydroxyacetone phosphate

FBPase:

fructose bisphosphatase

GAP:

glyceraldehyde-3-phosphate

G6P:

glucose 6-phosphate

PGA:

3-phosphoglycerate

TPT:

triose phosphate translocator

WT:

wild type

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Acknowledgements

This research was supported by the US Department of Energy under grant DE-FG02-99ER 20345. S.E.W. was supported in part by the Wisconsin Center for Space Automation and Robotics of UW-Madison. We thank Peter Vanderveer for help in starting this project.

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  1. Andreas P. M. Weber

    Present address: Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA

Authors and Affiliations

  1. Department of Botany, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI 53706, USA

    Sean E. Weise & Thomas D. Sharkey

  2. Department of Botany II, University of Cologne, Gyhofstrasse 15, 50931, Cologne, Germany

    Andreas P. M. Weber

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  1. Sean E. Weise
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  2. Andreas P. M. Weber
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Correspondence to Thomas D. Sharkey.

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Weise, S.E., Weber, A.P.M. & Sharkey, T.D. Maltose is the major form of carbon exported from the chloroplast at night. Planta 218, 474–482 (2004). https://doi.org/10.1007/s00425-003-1128-y

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