Role of the Reversible Xanthophyll Cycle in the Photosystem II Damage and Repair Cycle in Dunaliella salina  

Abstract

The Dunaliella salina photosynthetic apparatus organization and function was investigated in wild type (WT) and a mutant (zea1) lacking all ␤,␤-epoxycarotenoids derived from zeaxanthin (Z). The zea1 mutant lacked antheraxanthin, violaxanthin, and neoxanthin from its thylakoid membranes but constitutively accumulated Z instead. It also lacked the so-called xanthophyll cycle, which, upon irradiance stress, reversibly converts violaxanthin to Z via a de-epoxidation reaction. Despite the pronounced difference observed in the composition of ␤,␤-epoxycarotenoids between WT and zea1, no discernible difference could be observed between the two strains in terms of growth, photosynthesis, organization of the photosynthetic apparatus, photo-acclimation, sensitivity to photodamage, or recovery from photo-inhibition. WT and zea1 were probed for the above parameters over a broad range of growth irradiance and upon light shift experiments (low light to high light shift and vice versa). A constitutive accumulation of Z in the zea1 strain did not affect the acclimation of the photosynthetic apparatus to irradiance, as evidenced by indistinguishable irradiance-dependent adjustments in the chlorophyll antenna size and photosystem content of WT and zea1 strain. In addition, a constitutive accumulation of Z in the zea1 strain did not affect rates of photodamage or the recovery of the photosynthetic apparatus from photo-inhibition. However, Z in the WT accumulated in parallel with the accumulation of photodamaged PSII centers in the chloroplast thylakoids and decayed in tandem with a chloroplast recovery from photo-inhibition. These results suggest a role for Z in the protection of photodamaged and disassembled PSII reaction centers, apparently needed while PSII is in the process of degradation and replacement of the D1/32-kD reaction center protein.Organisms of oxygenic photosynthesis convert the energy of sunlight into chemical energy, which supports most life on earth. In photosynthetic membranes of green algae and plants, incident irradiance is absorbed by chlorophyll (Chl)-binding lightharvesting antenna complexes (LHCs) associated with the reaction centers of PSII and PSI. However, when the photosynthetic apparatus absorbs irradiance in excess of that required for the saturation of photosynthesis, singlet oxygen is generated, and PSII is subject to an irreversible photooxidative damage (Vass et al., 1992; Telfer et al., 1994; Melis, 1999). This photodamage selectively impairs the function of the D1/32-kD reaction center protein of PSII and has the potential to lower rates of photosynthesis and diminish plant growth and productivity (Powles and Critchley, 1980; Powles, 1984). The probability of photooxidative damage in chloroplasts depends on the oxidation reduction state of the primary electron-accepting plastoquinone of PSII (Q A ), which is the parameter that controls photodamage under a variety of physiological and environmental conditions. When Q A is oxidized under continuous illumination, photochemical electron transport...

Differential Expression and Localization of Early Light-Induced Proteins in Arabidopsis

“…Both the outer population of LHCII and damaged PSII migrate from the grana stacks to the stroma lamellae of the thylakoid membrane and this is in agreement with the location of Elips in nonappressed regions of thylakoid membranes (Adamska and Kloppstech, 1991). It was proposed that Cbr in Dunaliella may participate in PSII repair process and may by critical for the protection of PSII during the process of degrading and replacing nonfunctional D1 reaction center protein (Jin et al, 2001(Jin et al, , 2003. This hypothesis is also consistent with the accumulation pattern of Elip1 and Elip2 in Arabidopsis that amounts correlated with the degree of photoinactivation and photodamage of PSII reaction center.…”

“…4), red, and yellow leaves (Table I), the comparable amounts of Elip2 were induced only when approximately 40% of PSII reaction centers were damaged. Thus, the expression pattern of Elip1 resembles that reported for its Cbr homolog in Dunaliella, where the induction of Cbr followed the accumulation of (%) 100 6 0 5 8 6 6 100 6 0 9 3 6 2 100 6 0 7 2 6 2 Amount of D1 (%) 100 6 0 5 5 6 10 100 6 0 9 3 6 7 100 6 0 8 0 6 11 Amount of Elip1 (%) 0 6 0 100 6 0 0 6 0 7 0 6 9 0 6 0 9 0 6 5 Amount of Elip2 (%) 0 6 0 100 6 0 0 6 0 7 6 5 0 6 0 1 5 6 5 photodamaged D1 protein in 160 kD complex (Jin et al, 2001(Jin et al, , 2003. We expect that the physiological role of Elip2 is required under light stress conditions, where the accumulation of Elip1 alone did not offer a sufficient protection and an additional protection from Elip2 might ensure an adequate light stress defense.…”

“…It was reported that the accumulation of the carotenoid biosynthesis-related (Cbr) protein, a homolog of Elip in the green alga Dunaliella salina, occurs in parallel with the accumulation of photodamaged PSII reaction centers (Jin et al, 2001(Jin et al, , 2003. To test whether the accumulation of Elip1 and Elip2 in Arabidopsis correlates with the photoinactivation and photodamage of PSII we exposed leaves to increasing light intensities and measured the PSII activity by the assay of chl fluorescence (Fig.…”

Light- and pH-dependent structural changes in the PsbS subunit of photosystem II

“…It is worth recalling that zeaxanthin, forming at low luminal pH and found either free in the lipid phase (40) or bound to Lhcb proteins (41,42), does not bind to PsbS in vitro in a pHdependent manner (18). However, constitutive accumulation of zeaxanthin in a Dunaiella salina mutant does not bring about permanent quenching nor affect photosynthesis or sensitivity to irradiance stress, and it has been proposed that zeaxanthin is involved in photoprotection after PSII photodamage (43). A recent hypothesis envisions dynamic translocation of pigments and different domain localization for violaxanthin and zeaxanthin during the reversible xantophyll cycle (43).…”

Pigment Shuffling in Antenna Systems Achieved by Expressing Prokaryotic Chlorophyllide a Oxygenase in Arabidopsis

“…The second possible mechanism to explain the damage to PSII includes the inhibition of the D1 repair cycle. Under high light conditions, rapid D1 turnover is required because the D1 protein is damaged under high light conditions (52). In transgenic plants, Chl b interferes with the assembly of Chl a with D1 proteins during the repair cycle because the distribution of Chl b is not controlled.…”