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. 1998 Oct 27;95(22):13324-9.
doi: 10.1073/pnas.95.22.13324.

Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants

B J Pogson  1 , K K Niyogi, O Björkman, D DellaPenna
Affiliations

Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants

B J Pogson et al. Proc Natl Acad Sci U S A. .

Abstract

Collectively, the xanthophyll class of carotenoids perform a variety of critical roles in light harvesting antenna assembly and function. The xanthophyll composition of higher plant photosystems (lutein, violaxanthin, and neoxanthin) is remarkably conserved, suggesting important functional roles for each. We have taken a molecular genetic approach in Arabidopsis toward defining the respective roles of individual xanthophylls in vivo by using a series of mutant lines that selectively eliminate and substitute a range of xanthophylls. The mutations, lut1 and lut2 (lut = lutein deficient), disrupt lutein biosynthesis. In lut2, lutein is replaced mainly by a stoichiometric increase in violaxanthin and antheraxanthin. A third mutant, aba1, accumulates normal levels of lutein and substitutes zeaxanthin for violaxanthin and neoxanthin. The lut2aba1 double mutant completely lacks lutein, violaxanthin, and neoxanthin and instead accumulates zeaxanthin. All mutants were viable in soil and had chlorophyll a/b ratios ranging from 2.9 to 3.5 and near wild-type rates of photosynthesis. However, mutants accumulating zeaxanthin exhibited a delayed greening virescent phenotype, which was most severe and often lethal when zeaxanthin was the only xanthophyll present. Chlorophyll fluorescence quenching kinetics indicated that both zeaxanthin and lutein contribute to nonphotochemical quenching; specifically, lutein contributes, directly or indirectly, to the rapid rise of nonphotochemical quenching. The results suggest that the normal complement of xanthophylls, while not essential, is required for optimal assembly and function of the light harvesting antenna in higher plants.

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Figures

Figure 1
Figure 1
Carotenoid biosynthetic pathway in higher plant chloroplasts commencing with lycopene (A). lut1, lut2, and aba1 mutations are shown. Carotenoid content of mature green leaves of wild-type and xanthophyll mutant lines are shown in the bar graph (B). Each section of the bar corresponds to a specific carotenoid of the pathway (A). The SDs of the total pool of carotenoids per mole chl a are shown.
Figure 2
Figure 2
Photographs of developing seedlings (A), rate of chlorophyll accumulation in etiolated seedlings (B), and chlorophyll content of mature green leaves (C) of wild-type and mutant lines. (A) Photographs of soil-grown wild-type and xanthophyll mutant seedlings at 7 and 21 days, grown on a 12-h light cycle. The scale for all 7- and 21-day seedlings are shown by bars in the 7- and 21-day lut2aba1 panels, respectively. (B) Rate of total chlorophyll accumulation in seedlings. Wild-type, lut2, aba1, and lut2aba1 etiolated tissue culture-grown seedlings were vernalized, were germinated in the dark for 3 days, and then were transferred to continuous light. At each time point, two replicate extracts of 10 pooled seedlings were analyzed, and the chlorophyll content was expressed on a per plant basis (micrograms per seedling). SDs greater than the size of the symbol are shown. Note that the rate of greening is slower for 12-h-day soil-grown seedlings than for 24-h-day tissue culture-grown seedlings. (C) Chlorophyll ratios and content of mature green leaves. The chl a/b ratio (mol/mol) and total chlorophyll content of green leaves (micrograms per gram fresh weight) with SDs are shown. Values that are significantly different (P < 0.05) from the wild type are marked with an asterisk (∗).
Figure 3
Figure 3
Induction of nonphotochemical quenching (NPQ) in wild-type and xanthophyll mutant lines in the lut2 background (A) and the lut1 background (B). Plants were grown at 140 μmol⋅m−2⋅sec−1 for 12-h cycles and were dark adapted overnight. Fluorescence was measured before, during, and after exposure to actinic light (photosynthetically active radiation of 1,083 μmol⋅m−2⋅sec−1), shown by the white bar above the graphs; the dark bar indicates illumination with a weak, far-red background light. Three replicate plants were analyzed for each line and were averaged. SDs greater than the size of the symbol are shown.
Figure 4
Figure 4
Light response curves of wild-type, lut2, aba1, and lut2aba1 lines were used to calculate the electron transport rate, ETR (A), and photochemical quenching, qP (B). The photosynthetic activity radiation intensities of 0, 132, 304, 499, 794, 1,087, 1,533, and 1,971 μmol⋅m−2⋅sec−1 were applied for 10 min. The fluorescence measurements, Fs and Fm′ values (light), and the Fo′ value (recorded in dark immediately after each step) were used to calculate the ETR and qP.
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