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Adenine nucleotides and the xanthophyll cycle in leaves

I. Effects of CO2- and temperature-limited photosynthesis on adenylate energy charge and violaxanthin de-epoxidation

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Abstract

The effects of varying the steady-state rate of non-cyclic photosynthetic electron transport on the leaf adenylate energy charge and the epoxidation state of the xanthophyll-cycle pigments were determined in leaves of cotton (Gossypium hirsutum L.) and the mangrove (Aegialitis annulata R.Br.). Different photosynthetic rates were obtained by varying the intercellular CO2 concentration and/or the leaf temperature, and in some cases, by changing the leaf conductance to CO2 diffusion. Also determined were the effects of these treatments on the changes in the adenylate energy charge and the epoxidation state of the xanthophyll-cycle pigments that occur after darkening of the leaves. The leaf adenylate pool remained close to equilibrium with the adenylate kinase both in the light at steady state and during dark relaxation. The adenylate energy charge increased as the photosynthetic rate decreased and maximal levels were obtained when CO2 assimilation and, therefore, non-cyclic electron flow were maximally inhibited. This implies that, in nature, photophosphorylation may provide energy needed for ion-pumping and biosynthetic and repair processes, even under stress conditions that severely restrict or prevent photosynthetic gas exchange. High levels of de-epoxidized violaxanthin in the light did not necessarily indicate or depend on a high adenylate energy charge. Dithiothreitol, an inhibitor of the violaxanthin de-epoxidase a nd ascorbate peroxidase, did not inhibit the adenylate energy charge in the light. Thus we conclude that coupled electron transport during inhibited CO2 fixation was not driven by a dithiothreitol-sensitive Mehler ascorbate-peroxidase reaction. The changes in the adenylate energy charge and xanthophyll re-epoxidation that follow when leaves were darkened are strongly affected by the preceding photosynthetic rate. Postillumination fluctuations in adenylate energy charge, both at 15 ° and 27 °C, were most pronounced when the preceding photosynthetic rate was minimal and least pronounced when this rate was maximal. Temperature had a considerably greater influence in the dark on xanthophyll re-epoxidation than on the pattern of adenylate relaxation.

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Abbreviations

A:

antheraxanthin

adenylate kinase:

(myokinase), ATP: AMP phosphotransferase

Ci :

intercellular CO2 concentration

DPS:

de-epoxidation state of violaxanthin, ([Z + A]/[V + A + Z])

ΔpH:

trans-thylakoid proton gradient

ε:

[2ATP+ADP]

PET:

photosynthetic electron transportrate

PFD:

photon flux density

∑:

[ATP+ADP+AMP]

V:

violaxanthin

Z:

zeaxanthin

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Authors and Affiliations

  1. Department of Plant Biology, Carnegie Institution of Washington, 290 Panama Street, 94305, Stanford, CA, USA

    Adam M. Gilmore & Olle Björkman

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  1. Adam M. Gilmore
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  2. Olle Björkman
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Additional information

We thank Connie Shih for skillful assistance in growing plants and for conducting HPLC analyses. A Carnegie Institution Fellowship to A.G. is also gratefully acknowledged. This manuscript is C.I.W.-D.PB. Publication No. 1183.

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Gilmore, A.M., Björkman, O. Adenine nucleotides and the xanthophyll cycle in leaves. Planta 192, 526–536 (1994). https://doi.org/10.1007/BF00203591

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