The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana

Grasses, Thomas; Pesaresi, Paolo; Schiavon, Fabio; Varotto, Claudio; Salamini, F.; Jahns, Peter; Leister, Dario

doi:10.1016/s0981-9428(01)01346-8

Cited by 69 publications

(58 citation statements)

References 31 publications

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“…In addition, in none of the mutants tested in this study was overall photosynthetic electron flow affected severely, as indicated by the fact that parameters such as maximum and effective quantum yield, and photochemical quenching, were unchanged. Several other mutant studies (Haldrup et al, 1999;Naver et al, 1999;Jensen et al, 2000;Li et al, 2000;Gra␤es et al, 2002) have also shown that under optimal conditions, Arabidopsis can tolerate the loss of single polypeptides of the photosynthetic apparatus and their associated functions; for example, energy dissipation by ⌬pH-dependent quenching (Li et al, 2000;Gra␤es et al, 2002), or photosynthetic state transitions (Lunde et al, 2000; unpublished data in our lab) without obvious consequences for photoautotrophic growth. However, even if growth under growth chamber conditions appears to be unaffected in such mutants, there is increasing evidence that fitness in natural environments, particularly under rapidly changing illumination conditions, is reduced by such mutations (Gra␤es et al, 2002;S.…”

Section: A Role Of Psi-k In State Transitionsmentioning

confidence: 66%

Single and Double Knockouts of the Genes for Photosystem I Subunits G, K, and H of Arabidopsis. Effects on Photosystem I Composition, Photosynthetic Electron Flow, and State Transitions

Varotto¹,

Pesaresi²,

Jahns

et al. 2002

Plant Physiology

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Zentrum zur Identifikation von Genfunktionen durch Insertionsmutagenese bei Arabidopsis thaliana (C.V., P.P., A.L., D.L.), and Abteilung fü r Pflanzenzü chtung und Ertragsphysiologie, Max-Planck-Institut fü r Zü chtungsforschung, Carl-von-Linné Weg 10, 50829 Kö ln, Germany (M.T., F.Sc., F.Sa., D.L.); and Institut fü r Biochemie der Pflanzen, Heinrich-Heine-Universität Dü sseldorf, Universitätsstra␤e 1, 40225 Dü sseldorf, Germany (P.J.)Photosystem I (PSI) of higher plants contains 18 subunits. Using Arabidopsis En insertion lines, we have isolated knockout alleles of the genes psaG, psaH2, and psaK, which code for PSI-G, -H, and -K. In the mutants psak-1 and psag-1.4, complete loss of PSI-K and -G, respectively, was confirmed, whereas the residual H level in psah2-1.4 is due to a second gene encoding PSI-H, psaH1. Double mutants, lacking PSI-G, and also -K, or a fraction of -H, together with the three single mutants were characterized for their growth phenotypes and PSI polypeptide composition. In general, the loss of each subunit has secondary, in some cases additive, effects on the abundance of other PSI polypeptides, such as D, E, H, L, N, and the light-harvesting complex I proteins Lhca2 and 3. In the G-less mutant psag-1.4, the variation in PSI composition suggests that PSI-G stabilizes the PSI-core. Levels of light-harvesting complex I proteins in plants, which lack simultaneously PSI-G and -K, indicate that PSI subunits other than G and K can also bind Lhca2 and 3. In the same single and double mutants, psag-1. 4, psak-1, psah2-1.4, psag-1.4/psah2-1.4, and psag-1.4/psak-1 photosynthetic electron flow and excitation energy quenching were analyzed to address the roles of the various subunits in P700 reduction (mediated by PSI-F and -N) and oxidation (PSI-E), and state transitions (PSI-H). Based on the results, we also suggest for PSI-K a role in state transitions.PSI mediates light-driven electron transport from plastocyanin to ferredoxin across the thylakoid membrane. The PSI complexes in plants and cyanobacteria are basically similar, but there are some notable differences (Scheller et al., 1997): The plant PSI is slightly larger (Kitmitto et al., 1997), trimer formation has been observed only in cyanobacteria (Chitnis and Chitnis, 1993), and the plant PSI core is associated with the light-harvesting complex I (LHCI), which is made up of the four different chlorophyll (Chl)/carotenoidbinding polypeptides Lhca1-4 (Jansson, 1999). In addition, among the 14 subunits that form the core of PSI in flowering plants (PSI-A through -O; Scheller et al., 1997Scheller et al., , 2001; H.V. Scheller, personal communication), four subunits (PSI-G, -H, -N, and -O; Okkels et al., 1989Okkels et al., , 1992 Knoetzel and Simpson, 1993; H.V. Scheller, personal communication) are not present in cyanobacteria. Conversely, no homolog of the cyanobacterial PSI-M has been found yet in higher plants.Most essential for PSI function are the three subunits PSI-A, -B, and -C, which bind the electron acceptors. These acceptor-bi...

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Section: A Role Of Psi-k In State Transitionsmentioning

confidence: 66%

Single and Double Knockouts of the Genes for Photosystem I Subunits G, K, and H of Arabidopsis. Effects on Photosystem I Composition, Photosynthetic Electron Flow, and State Transitions

Varotto¹,

Pesaresi²,

Jahns

et al. 2002

Plant Physiology

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“…Mutant lines from the Salk collection 9 were identified by searching the SiGNAL database (http://signal.salk.edu/ tabout.html). Methods for plant propagation have been described elsewhere [25][26][27] . Chlorophyll fluorescence and pigment analysis.…”

Section: Methodsmentioning

confidence: 99%

“…Chlorophyll fluorescence and pigment analysis. Photosynthetic electron transport, state transitions and leaf pigment composition were measured as described [25][26][27] (see Supplementary Information for details). Analysis of LHCII phosphorylation in vivo and in vitro.…”

Section: Methodsmentioning

confidence: 99%

Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases

Bonardi

Pesaresi

Becker

et al. 2005

Nature

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411

496

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Illumination changes elicit modifications of thylakoid proteins and reorganization of the photosynthetic machinery. This involves, in the short term, phosphorylation of photosystem II (PSII) and light-harvesting (LHCII) proteins. PSII phosphorylation is thought to be relevant for PSII turnover 1,2 , whereas LHCII phosphorylation is associated with the relocation of LHCII and the redistribution of excitation energy (state transitions) between photosystems 3,4 . In the long term, imbalances in energy distribution between photosystems are counteracted by adjusting photosystem stoichiometry 5,6 . In the green alga Chlamydomonas and the plant Arabidopsis, state transitions require the orthologous protein kinases STT7 and STN7, respectively 7,8 . Here we show that in Arabidopsis a second protein kinase, STN8, is required for the quantitative phosphorylation of PSII core proteins. However, PSII activity under high-intensity light is affected only slightly in stn8 mutants, and D1 turnover is indistinguishable from the wild type, implying that reversible protein phosphorylation is not essential for PSII repair. Acclimation to changes in light quality is defective in stn7 but not in stn8 mutants, indicating that short-term and long-term photosynthetic adaptations are coupled. Therefore the phosphorylation of LHCII, or of an unknown substrate of STN7, is also crucial for the control of photosynthetic gene expression.STT7 and STN7 are orthologous protein kinases required for LHCII phosphorylation and for state transitions in Chlamydomonas and Arabidopsis, respectively 7,8 . In Arabidopsis, another STT7/STN7-like protein (STN8) exists that is not required for state transitions 8 . STN8 is located in the chloroplast, as shown by in vivo subcellular localization of its amino-terminal region fused to the dsRED protein and by the import of, and transit peptide removal from, STN8 translated in vitro (Fig. 1a, b). Chloroplast subfractionation after import revealed that the protein is associated, like STT7 and STN7, with thylakoids ( Fig. 1c) (refs 7, 8).Insertion mutants for STN8 and STN7 were obtained from the Salk collection 9 , and for each gene two independent mutant alleles lacking the respective transcript were identified (Supplementary Fig. S1). The stn7 stn8 double mutant was generated by crossing stn7 and stn8 single knockouts and screening the resulting F 2 generation for homozygous double mutants. All mutants were indistinguishable from the wild type with regard to the timing of seed germination and growth rate in the greenhouse ( Supplementary Fig. S1). In stn7 and stn7 stn8 mutants, a slight decrease in the levels of neoxanthin, lutein and total chlorophyll was found (Supplementary Table S1). These subtle changes can be attributed to a minor decrease in LHCII content, not detectable by polyacrylamide-gel electrophoresis (PAGE) analysis ( Supplementary Fig. S2).Photosynthetic electron flow, measured on the basis of chlorophyll fluorescence, was not altered in the mutants (Supplementary Table S2). State transitions w...

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“…The following mutants were used: npq1 and npq2 (Niyogi et al, 1998), pgr1 (Munekage et al, 2001), and psbs-1.3 (Grasses et al, 2002). For the latter mutant, which is allelic to the PsbS-deficient npq4 mutant (Li et al, 2000), the more common name npq4 is used throughout the article.…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

“…The following mutants were used: (1) the npq1 mutant (Niyogi et al, 1998), which is affected in the violaxanthin (Vx) de-epoxidase and is unable to form Zx upon illumination; (2) the npq2 mutant (Niyogi et al, 1998), which is affected in the Zx epoxidase and accumulates high levels of Zx under all conditions; (3) the pgr1 mutant (Munekage et al, 2001), which carries a single point mutation in the Rieske subunit of the cytochrome b 6 /f complex (this mutant is limited in lumen acidification due to an altered pH dependence of linear electron transport and ferredoxin-dependent cyclic electron transport [Okegawa et al, 2005]); and (4) the psbs-1.3 mutant (Grasses et al, 2002), which is affected in the PsbS protein of PSII and thus unable to generate qE. For the latter mutant, which is allelic to the PsbS-deficient npq4 mutant (Li et al, 2000), the more common name npq4 will be used throughout the article.…”

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confidence: 99%

The Transiently Generated Nonphotochemical Quenching of Excitation Energy in Arabidopsis Leaves Is Modulated by Zeaxanthin

2007

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Upon the transition of dark-adapted plants to low light, the energy-dependent quenching (qE) of excitation energy is only transiently induced due to the only transient generation of the transthylakoid pH gradient. We investigated the transient qE (qE TR ) in different Arabidopsis (Arabidopsis thaliana) mutants. In dark-adapted plants, qE TR was absent in the npq4 mutant (deficient in the PsbS protein) and the pgr1 mutant (restricted in lumen acidification). In comparison with wild-type plants, qE TR was reduced in the zeaxanthin (Zx)-deficient npq1 mutant and increased in the Zx-accumulating npq2 mutant. After preillumination of plants (to allow the synthesis of large amounts of Zx), the formation and relaxation of qE TR was accelerated in all plants (except for npq4) in comparison with the respective dark-adapted plants. The extent of qE TR , however, was unchanged in npq1 and npq4, decreased in npq2, but increased in wild-type and pgr1 plants. Even in presence of high levels of Zx, qE TR in pgr1 mutants was still lower than that in wild-type plants. In the presence of the uncoupler nigericin, qE TR was completely abolished in all genotypes. Thus, the transient qE TR shows essentially the same characteristics as the steady-state qE; it is strictly dependent on the PsbS protein and a low lumen pH, but the extent of qE TR is largely modulated by Zx. These results indicate that qE TR does not represent a different quenching mechanism in comparison with the steady-state qE, but simply reflects the response of qE to the dynamics of the lumen pH during light activation of photosynthesis.

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The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana

Cited by 69 publications

References 31 publications

Single and Double Knockouts of the Genes for Photosystem I Subunits G, K, and H of Arabidopsis. Effects on Photosystem I Composition, Photosynthetic Electron Flow, and State Transitions

Single and Double Knockouts of the Genes for Photosystem I Subunits G, K, and H of Arabidopsis. Effects on Photosystem I Composition, Photosynthetic Electron Flow, and State Transitions

Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases

The Transiently Generated Nonphotochemical Quenching of Excitation Energy in Arabidopsis Leaves Is Modulated by Zeaxanthin

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