Acclimation of Arabidopsis thaliana to the light environment: regulation of photosystem stoichiometry

Robin G. Walters, Peter Horton

Robert Hill Institute, Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, UK

Evidence is growing that that variations in chloroplast composition in response to environmental change depend on signals from photosynthetic metabolism such the levels of ATP and NADPH in the stroma and/or cytoplasm, or the redox state of components of the photosynthetic apparatus (e.g. plastoquinone), but the nature of such signals remains unknown (Melis et al. 1985; Chow et al. 1990a; Maxwell et al. 1994, 1995). Based on experiments in which the spectral quality of growth lights have been manipulated so as to preferentially excite either PSI or PSII, it has been suggested that photosystem stoichiometry is regulated by the redox state of electron transport components between the two photosystems, a signal known to be important in cyanobacteria (Fujita et al. 1987); an imbalance between the two in the rates of excitation would thus generate a signal which feeds back, leading to the correction of that imbalance (Kim et al. 1993).

Contrary to this hypothesis, work by ourselves and Chow et al. (1990b) has showed that growth with and without high levels of supplementary far-red light does not lead to changes in photosystem stoichiometry, despite the marked effect on the redox state of the electron transport chain. Furthermore, Arabidopsis grown in red light enriched in far-red and depleted in blue wavelengths (preferentially absorbed by PSI) has a PSII/PSI ratio similar to that of white light-grown plants. These data indicate that photosystem levels are not regulated by metabolic control alone. Supplementing red growth lights with low irradiance blue light had a marked effect on PSII levels, suggesting a direct role for blue light in the regulation of photosystem stoichiometry. Assaying PSII in plants grown in background red illumination with varying irradiances of supplementary blue light did not reveal a correlation between blue irradiance and PSII content.

However, further analysis of the data suggests that both red and blue have a regulatory role. The figure shows data for PSII content plotted as a function of the blue irradiance relative to that of the background red light, together with PSI and PSII levels for plants grown under other light regimes. A relationship between the spectral characteristics of the growth light regime and photosystem stoichiometry is now apparent: the presence of very low supplementary blue light leads to a 50% increase in the level of PSII per unit Chl; as blue light increases further relative to the background red light, PSII content falls again, eventually returning to the level observed in plants grown in red light alone. The relatively minor changes in PSI levels which are observed as the proportion of blue light increases mirror the changes in PSII.

Such two-phase responses to blue light have previously been observed in pea seedlings, for epicotyl elongation and Lhcb mRNA levels (Warpeha et al. 1989; Warpeha and Kaufman 1990a, 1990b; Marrs and Kaufman 1991), and have been interpreted as indicating the involvement of two separate blue light responses: low-fluence-responses which inhibited epicotyl elongation and stimulated mRNA accumulation; and high-fluence responses which had the reverse effects. These observations are highly reminiscent of the response of PSII levels to blue light, and we suggest that two blue light reponses are involved in the regulation of photosystem stoichiometry: an inductive low-fluence-response, which activates acclimation; and a regulatory high-fluence response which is attenuated by red light. We interpret this effect of red light as being consistent with existing hypotheses that chloroplast composition is regulated by photosynthetic metabolism. The behaviour of a hy4 mutant, which exhibits altered acclimation behaviour (see Figure), supports this hypothesis; the hy4 mutation affects the inhibition of hypocotyl elongation, a blue high-fluence-response (Ahmad and Cashmore 1993).

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