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Plant Physiol. (1999) 120: 727-738 Xanthophyll Cycle Pigment Localization and Dynamics during Exposure to Low Temperatures and Light Stress in Vinca major1
Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, Colorado 80309-0334 (A.S.V., W.W.A., B.D.-A.); and Universita di Verona, Facolta di Scienze Matematiche, Fisiche e Naturali, Biotecnologie Vegetali, Strada Le Grazie, 37134 Verona, Italy (R.C., R.B.)
The distribution of xanthophyll cycle pigments (violaxanthin plus antheraxanthin plus zeaxanthin [VAZ]) among photosynthetic pigment-protein complexes was examined in Vinca major before, during, and subsequent to a photoinhibitory treatment at low temperature. Four pigment-protein complexes were isolated: the core of photosystem (PS) II, the major light-harvesting complex (LHC) protein of PSII (LHCII), the minor light-harvesting proteins (CPs) of PSII (CP29, CP26, and CP24), and PSI with its LHC proteins (PSI-LHCI). In isolated thylakoids 80% of VAZ was bound to protein independently of the de-epoxidation state and was found in all complexes. Plants grown outside in natural sunlight had higher levels of VAZ (expressed per chlorophyll), compared with plants grown in low light in the laboratory, and the additional VAZ was mainly bound to the major LHCII complex, apparently in an acid-labile site. The extent of de-epoxidation of VAZ in high light and the rate of reconversion of Z plus A to V following 2.5 h of recovery were greatest in the free-pigment fraction and varied among the pigment-protein complexes. Photoinhibition caused increases in VAZ, particularly in low-light-acclimated leaves. The data suggest that the photoinhibitory treatment caused an enrichment in VAZ bound to the minor CPs caused by de novo synthesis of the pigments and/or a redistribution of VAZ from the major LHCII complex.
Photoinhibition refers to a condition in which a persistent
decrease in the efficiency of photosynthetic energy conversion in
leaves is observed. Photoinhibition occurs in the field in plants
exposed to conditions of high light in combination with environmental
stress, such as cold temperatures, but can also be induced by exposure
of shade-acclimated leaves to high light (Krause, 1994 Under various photoinhibitory conditions large quantities of the
xanthophyll cycle pigments Z and A have been found to be retained in
leaves for extended periods after darkening (Demmig et al., 1988 To influence Chl fluorescence yield xanthophylls must be localized in
close proximity to the pigment-protein complexes of the thylakoid
membrane, and knowledge of their precise organization is important to
understand the mechanism of (Z plus A)-dependent energy dissipation.
Several studies have demonstrated that the xanthophyll cycle pigments
(VAZ) are associated with all light-harvesting components, including
LHCI (Thayer and Björkman, 1992 Although several studies have been conducted to examine the
distribution of the xanthophyll cycle pigments among pigment-protein complexes isolated from unstressed leaves, very little is know about
their distribution under photoinhibitory conditions when the rate of Z
epoxidation is severely slowed following leaf darkening. The major goal
of this study was to assess whether changes occur in the levels or
distribution of VAZ in the pigment-protein complexes when plants are
treated with such photoinhibitory high light, as well as whether
differences exist in the rate at which Z and A are reconverted to V on
the different pigment-proteins during the slow recovery from
photoinhibition.
Plant Material and Photoinhibitory Treatments
Thylakoid Isolation Thylakoid membranes were isolated as described previously by Bassi et al. (1988) except the grinding buffer consisted of 0.1 M
Tricine, pH 7.8, 0.4 M sorbitol, 0.5% nonfat dried milk,
0.2 mM PMSF, 5 mM
 -amino-n-caproic acid, and 1 mM
benzamidine; the washing buffer consisted of 25 mM Hepes/KOH, pH 7.5, and 10 mM EDTA; and the resuspension buffer consisted of
10 mM Hepes/KOH, pH 7.5, 1 mM EDTA, and 50% (v/v) glycerol.
Chl Fluorescence Fluorescence measurements were performed on intact leaves under the respective growth PPFD conditions with a portable fluorometer (PAM-2000, Walz, Effeltrich, Germany). Fluorescence measurements and calculations were performed as described previously (Demmig-Adams and Adams, 1996; Demmig-Adams et al., 1996).
Solubilization and Fractionation of Thylakoids and Identification of Pigment-Protein Complexes Thylakoids were resuspended in 2 mg Chl/mL and solubilized by adding an equal volume of 2.8% dodecyl maltoside in water. The sample was then vortexed for 20 s and put on ice for 1 min. The solubilized sample was spun for 2 min at 15,000g and 4°C and rapidly loaded onto a 0.1 to 1 M Suc gradient containing 10 mM Hepes, pH 7.6, and 0.06% dodecyl maltoside. The gradient was spun in a Beckman SW41 rotor at 39,000 rpm for 27 h at 4°C. Individual green fractions were harvested with a syringe. Pigment-protein complexes were identified using analytical SDS-PAGE, spectroscopy, and pigment analysis, as described previously for several different species (Di Paolo et al., 1990; Santini et al., 1994; Kilian et al., 1997).
Electrophoresis and Immunoblotting Analytical SDS-PAGE was performed with gradient gels (10%-16% acrylamide) using the Tris/Tricine buffer system of Schägger and von Jagow (1987). Alternatively, a Tris-sulfate buffer system was used
(Bassi et al., 1985a). Preparative IEF was performed as previously
described (Dainese et al., 1990). Nondenaturing green gel
electrophoresis was done according to the method of Knoetzel and
Simpson (1991). For immunoblot assays, samples were separated by the
Tris-sulfate gel system and transferred to a nitrocellulose filter
(Millipore). The filters were incubated with antibodies and detected
with alkaline phosphatase coupled to anti-rabbit IgG (Sigma).
Analysis of Pigments Total pigments were extracted with 80% acetone. Analysis of the extracts by HPLC was as described previously (Gilmore and Yamamoto, 1991). In this study the determination of the Chl-to-carotenoid ratio
in pigment proteins was of crucial importance. The results of HPLC
analysis were therefore verified by fitting the absorption spectra of
ethanolic extracts of pigment proteins with the spectra of pure
pigments in ethanol (Connelly et al., 1997). Spectra (350-750 nm) were
recorded using a DW2000 spectrophotometer in the split-beam mode
(Aminco, Silver Spring, MD). Individual pigments were purified by HPLC,
dried under a vacuum, and resuspended in 96% ethanol. Curve fitting
was obtained by using a nonlinear least-squares fitting code
(Origin, MicroCal Software, Northampton, MA).
Verification of Specificity of Pigment Binding To verify the specificity of xanthophyll binding to the different pigment-protein complexes, an experiment was undertaken in which excess xanthophylls were added to solubilized thylakoids before their fractionation. No change in pigment composition of the protein complexes was observed after fractionation, suggesting that no nonspecific binding of the xanthophylls was caused by the solubilization conditions.DEAE Chromatography of the PSII Core The Suc-gradient fraction containing the PSII core was purified using DEAE chromatography as described previously (Giuffra et al., 1996).
Characterization of Pigment Content and Distribution prior to Photoinhibitory Treatment The pigment content of V. major var variegata Loud. was examined in control conditions from both isolated thylakoids and whole-leaf extracts (Table I). In control conditions the differences in carotenoid levels, relative to Chl a, from plants grown in the GC relative to those grown OD involved predominantly the fraction of VAZ (Table I). In both isolated thylakoids and leaf extracts from plants grown OD, the content of V and VAZ was approximately twice that of the plants grown in GCs. A comparison of the pigment composition of whole-leaf extracts versus isolated thylakoids demonstrates that the ratios of total carotenoid and of VAZ to Chl were not significantly changed following thylakoid isolation.
Distribution of VAZ among Pigment Proteins In a first approach to examining the location of pigments within the protein complexes, thylakoid membranes were solubilized with dodecyl maltoside, and Suc-gradient fractionation was performed, followed by analysis of the pigment and protein content of the fractions (Fig. 1; Tables II and III). Five major fractions were obtained.
Effect of Photoinhibitory Treatment V. major plants were subjected to treatments of continuous light (48 or 122 h for plants grown in GCs and OD, respectively) and chilling temperatures (15°C and 10°C for plants grown in GCs and OD, respectively) to induce photoinhibition, after which plants were allowed to recover at room temperature in darkness for 2.5 h. Plants were monitored during the treatment to ensure that photoinhibitory conditions (i.e. persistent reductions in Fv/Fm) were achieved. The different treatment conditions reflect different requirements necessary to photoinhibit the plants, with the plants acclimated to the lower-light environment becoming photoinhibited much more rapidly than the plants grown in full sunlight.
Suc-Gradient Fractionation of Thylakoid Membranes upon Stress and
Recovery
Analysis of the PSII Core-Containing Fraction Immunoblot analysis of the PSII core-containing fraction, isolated from the plants grown OD, indicated that LHCII was the principal contaminant and that minor CPs or PSI-LHCI were not present. To quantify the level of contamination high amounts of the core fraction (protein equivalent to 10 µg of Chl) in addition to known amounts of pure LHCII trimer were subjected to SDS-PAGE. Densitometric analysis of the Coomassie Blue-stained gels revealed the level of contamination at a maximum of 7% LHCII. Calculations of expected pigment content (moles per 100 moles of Chl a) assuming pure PSII core and 7% contamination with LHCII were compared with the actual data in Table V. Although LHCII contamination accounted for all of the Chl b, neoxanthin, and lutein present, there was a greater concentration of VAZ in the core than could be accounted for by LHCII contamination, suggesting that some VAZ may be bound to the PSII core.
Flat-Bed IEF Fractionation of the LHCII Monomer and Minor CP-Containing Fraction from High-LightAcclimated Leaves The Suc-gradient fraction from the high-light OD samples containing LHCII monomer and the minor Chl proteins was subjected to flat-bed IEF. Fractions from IEF were applied to glycerol gradients (15%-40% glycerol) and ultracentrifuged, and two bands were collected in each case. Bands were analyzed by SDS-PAGE, and pigment analysis was performed (Fig. 2; Table VI). Although fully purified minor CPs were not obtained, the minor CPs were separated from LHCII, except for some contamination of the minor CPs by LHCII in the control sample (Fig. 2).
Nondenaturing Green Gel of the Minor CP-Containing Fraction IEF fractions containing the minor CPs were solubilized with 1.9% dodecyl maltoside and run on a nondenaturing green gel. Each of the fractions resulted in two green bands, which were excised, eluted from the gel, and analyzed. Although pure CPs were not obtained, SDS-PAGE analysis indicated that there was significant enrichment in CP26 or CP29 in two of the bands excised from both the stress samples and the recovery samples. Results of the densitometric analysis of the Coomassie Blue-stained gels, indicating the relative quantities of the proteins, in addition to the xanthophyll cycle pigment content for each fraction, is presented in Figure 3. A relative enrichment in V correlated with CP29, whereas enrichment with Z correlated with CP26. This suggests that the conversion state of the xanthophyll cycle was not uniform among the minor CPs and that the pigments bound to CP29 de-epoxidized to a lesser extent compared with either CP26 or the LHCIIs.
The results of this study demonstrate that at least 80% of the
xanthophyll cycle pigments (VAZ) that were present in isolated thylakoids were bound to protein independently of the de-epoxidation state (Table II). These data are consistent with those of Thayer and
Björkman (1992)
LHCII In leaves acclimated to different environmental conditions, the fraction containing LHCII exhibited an altered VAZ content. In Table VII the xanthophyll content per LHCII polypeptide was computed assuming 12 Chl a+b bound (Dainese and Bassi, 1991; Kühlbrandt et al., 1994) and
using the data from Table III and VI. Thus, VAZ per polypeptide was
greater in plants grown OD versus V. major grown in GCs. The
additional VAZ found in the plants grown OD was mostly loosely bound,
because it was removed upon IEF. In addition, there were 2 luteins and
0.8 neoxanthin per LHCII polypeptide, both of which were not altered by
growth conditions or stress treatment (Tables II, VI, and VII). These
data therefore indicate approximately 3.5 carotenoids per LHCII monomer
in the bands from Suc gradients (Table II) and close to 3 carotenoids
per LHCII following IEF (Tables VI and VII), which is in agreement with
the value of 3 xanthophylls per LHCII polypeptide consistently found for highly purified LHCII (Bassi et al., 1993; Ruban et al., 1994). We
propose that LHCII possesses an additional xanthophyll-binding site (in
addition to the three usually found) that binds additional VAZ in
leaves acclimated to high light. Since loosely bound VAZ was found to
be associated with the LHCII complex, it could be hypothesized that the
VAZ found in the free-pigment fraction actually derives from LHCII,
which would account for 0.2 mol VAZ per mol LHCII in the case of the
sample from the plants grown OD. With this complement each LHCII would
bind 3.7 xanthophyll molecules of which approximately 1 would bind to
the new binding site postulated above.
Minor Chl Proteins
PSII Core Suc-gradient fractionation yielded PSII core fractions with a maximum of 7% contamination by LHCII. Assuming 56 Chls per PSII core, between 1 and 1.8 xanthophylls per PSII core were detected in samples from GC plants and 0.8 to 1.3 xanthophylls per PSII core were detected in samples from plants grown OD in full sunlight. The LHCII contamination accounted for less than 0.1 xanthophyll molecule per PSII core (Table V), suggesting that 1 to 2 VAZ molecules may be bound to the PSII core. This was not previously recognized in a study of maize leaves (Bassi et al., 1993) in which a multistep purification procedure
was used, which would remove any loosely bound pigment. A loose binding
site for VAZ in the PSII core is suggested by the results of
ion-exchange chromatography; when the complex was bound to the column
and the column was washed extensively, the xanthophyll content
decreased to 0.17 per PSII core. The presence of VAZ in PSII core
fractions has also been reported in barley (Lee and Thornber, 1995) and
lettuce (Phillip and Young, 1995).
PSI-LHCI We confirm the presence of VAZ in PSI-LHCI (Thayer and Björkman, 1992; Lee and Thornber, 1995; Zhu et al., 1997).
However, the VAZ bound to PSI-LHCI was de-epoxidized to a lesser extent upon photoinhibitory treatment than that bound to the PSII complexes, and the extent of reconversion following 2.5 h recovery was also lower in PSI-LHCI. The presence of photoconvertible VAZ in PSI-LHCI raises the question of whether thermal energy-dissipation mechanisms similar to those observed in PSII take place in PSI. This seemed unlikely previously, since PSI was believed to be a deep trap, which
would make energy dissipation in LHCI inefficient (in decreasing Chl
a excited state concentrations at the level of the PSI
reaction center). More recently, however, it was recognized that PSI,
like PSII, is a shallow trap and that, therefore, PSI and its antenna are essentially equilibrated (Croce et al., 1996b), implying that thermal dissipation in the LHCI antenna could be an efficient regulatory mechanism for Chl a excitation in PSI. This could
provide protection from the adverse effects of excess excitation on PSI as well (Terashima et al., 1994; Tjus et al., 1998).
In this study we have shown that xanthophyll cycle pigments undergo dynamic changes not only in their epoxidation state but also in their association with CPs. Upon acclimation to growth OD in full sunlight, the V content of control thylakoids was greatly increased. This additional V was bound to the major LHCII fraction. Following photoinhibitory treatment, the VAZ content of the LHCII fraction decreased and the minor CP fraction of PSII (CP29, CP26, and CP24), and to a lesser extent the PSII core complex fraction, bound increased amounts of Z plus A. This is interpreted in terms of the presence of an additional, low-affinity V-binding site in LHCII, in equilibrium with V free in the lipid phase, and of an additional high-affinity Z-binding site in the minor CPs. The higher degree of de-epoxidation in the free-pigment fraction suggests that the preferred substrate for V de-epoxidase is the pigment free in the lipid phase, which, upon conversion, becomes bound to minor CPs and PSII core CPs.
2 Present address: University of St. Thomas, Department of Biology, 2115 Summit Avenue, St. Paul, MN 55105-1096. * Corresponding author; e-mail verhoeve{at}hawaii.edu; fax (Hawaii) 1-808-956-3542; fax (Minnesota) 1-651-962-5209. Received December 15, 1998;
accepted March 22, 1999.
Abbreviations: A, antheraxanthin. Chl, chlorophyll. CP, Chl-binding protein. ELIP, early-light-inducible protein. Fv/Fm, ratio of variable to maximal Chl fluorescence. GC, growth chamber. LHCI or II, light-harvesting complex I or II. OD, outdoors. V, violaxanthin. VAZ, V plus A plus Z. Z, zeaxanthin.
We gratefully acknowledge Paolo Pesaresi for his assistance in performing some of the experimental techniques.
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K. Humbeck and K. Krupinska The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light J. Exp. Bot., January 2, 2003; 54(381): 375 - 383. [Abstract] [Full Text] [PDF]
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A. V. Ruban, A. Pascal, P. J. Lee, B. Robert, and P. Horton Molecular Configuration of Xanthophyll Cycle Carotenoids in Photosystem II Antenna Complexes J. Biol. Chem., November 1, 2002; 277(45): 42937 - 42942. [Abstract] [Full Text] [PDF]
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T. Morosinotto, R. Baronio, and R. Bassi Dynamics of Chromophore Binding to Lhc Proteins in Vivo and in Vitro during Operation of the Xanthophyll Cycle J. Biol. Chem., September 27, 2002; 277(40): 36913 - 36920. [Abstract] [Full Text] [PDF]
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D. Elrad, K. K. Niyogi, and A. R. Grossman A Major Light-Harvesting Polypeptide of Photosystem II Functions in Thermal Dissipation PLANT CELL, August 1, 2002; 14(8): 1801 - 1816. [Abstract] [Full Text] [PDF]
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C. Lu, Q. Lu, J. Zhang, and T. Kuang Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field J. Exp. Bot., September 1, 2001; 52(362): 1805 - 1810. [Abstract] [Full Text] [PDF]
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J. E. W. Polle, K. K. Niyogi, and A. Melis Absence of Lutein, Violaxanthin and Neoxanthin Affects the Functional Chlorophyll Antenna Size of Photosystem-II but not that of Photosystem-I in the Green Alga Chlamydomonas reinhardtii Plant Cell Physiol., May 1, 2001; 42(5): 482 - 491. [Abstract] [Full Text] [PDF]
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P. Jahns, A. Wehner, H. Paulsen, and S. Hobe De-epoxidation of Violaxanthin after Reconstitution into Different Carotenoid Binding Sites of Light-harvesting Complex II J. Biol. Chem., June 15, 2001; 276(25): 22154 - 22159. [Abstract] [Full Text] [PDF]
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A. V. Ruban, A. A. Pascal, B. Robert, and P. Horton Configuration and Dynamics of Xanthophylls in Light-harvesting Antennae of Higher Plants. SPECTROSCOPIC ANALYSIS OF ISOLATED LIGHT-HARVESTING COMPLEX OF PHOTOSYSTEM II AND THYLAKOID MEMBRANES J. Biol. Chem., June 29, 2001; 276(27): 24862 - 24870. [Abstract] [Full Text] [PDF]
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S. Caffarri, R. Croce, J. Breton, and R. Bassi The Major Antenna Complex of Photosystem II Has a Xanthophyll Binding Site Not Involved in Light Harvesting J. Biol. Chem., September 14, 2001; 276(38): 35924 - 35933. [Abstract] [Full Text] [PDF]
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Abstract
Introduction
2
s
-carotene for which the leaf data are not available. See
``
F]/Fm
[Z plus A]/[VAZ] of 
