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Adenine nucleotides and the xanthophyll cycle in leaves

II. Comparison of the effects of CO2- and temperature-limited photosynthesis on photosystem II fluorescence quenching, the adenylate energy charge and violaxanthin de-epoxidation in cotton

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Abstract

The relationships among the leaf adenylate energy charge, the xanthophyll-cycle components, and photosystem II (PSII) fluorescence quenching were determined in leaves of cotton (Gossypium hirsutum L. cv. Acala) under different leaf temperatures and different intercellular CO2 concentrations (Ci). Attenuating the rate of photosynthesis by lowering the Ci at a given temperature and photon flux density increased the concentration of high-energy adenylate phosphate bonds (adenylate energy charge) in the cell by restricting ATP consumption (A.M. Gilmore, O. Björkman 1994, Planta 192, 526–536). In this study we show that decreases in photosynthesis and increases in the adenylate energy charge at steady state were both correlated with decreases in PSII photo-chemical efficiency as determined by chlorophyll fluorescence analysis. Attenuating photosynthesis by decreasing Ci also stimulated violaxanthin-de-epoxidation-dependent nonradiative dissipation (NRD) of excess energy in PSII, measured by nonphotochemical fluorescence quenching. However, high NRD levels, which indicate a large trans-thylakoid proton gradient, were not dependent on a high adenylate energy charge, especially at low temperatures. Moreover, dithiothreitol at concentrations sufficient to fully inhibit violaxanthin de-epoxidation and strongly inhibit NRD, affected neither the increased adenylate energy charge nor the decreased PSII photo-chemical efficiency that result from inhibiting photosynthesis. The build-up of a high adenylate energy charge in the light that took place at low Ci and low temperatures was accompanied by a slowing of the relaxation of non-photochemical fluorescence quenching after darkening. This slowly relaxing component of nonphotochemical quenching was also correlated with a sustained high adenylate energy charge in the dark. These results indicate that hydrolysis of ATP that accumulated in the light may acidify the lumen and thus sustain the level of NRD for extended periods after darkening the leaf. Hence, sustained nonphotochemical quenching often observed in leaves subjected to stress, rather than being indicative of photoinhibitory damage, apparently reflects the continued operation of NRD, a photoprotective process.

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Abbreviations

A:

antheraxanthin

adenylate kinase:

(myokinase), ATP:AMPphosphotransferase

Ci :

intercellular CO2 concentration

DPS:

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

DTT:

dithiothreitol

ΔpH:

trans-thylakoid proton gradient

ɛ:

[2ATP+ADP]

F′:

steady-state fluorescence in the presence of NRD

FM :

maximal fluorescence in the absence of NRD

F′M :

maximal fluorescence in the presence of NRD

NRD:

nonradiative energy dissipation

PET:

photosynthetic electron transport rate

PFD:

photon flux density

ΦPSII :

photon yield of PSII photochemistry at the actual reduction state in the light or dark

QA :

the primary electron acceptor of PSII

∑:

[ATP+ADP+AMP]

SVN :

Stern-Volmer nonphotochemical quenching

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.

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Gilmore, A.M., Björkman, O. Adenine nucleotides and the xanthophyll cycle in leaves. Planta 192, 537–544 (1994). https://doi.org/10.1007/BF00203592

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