A Chromodomain Protein Encoded by the Arabidopsis CAO Gene Is a Plant-Specific Component of the Chloroplast Signal Recognition Particle Pathway That Is Involved in LHCP Targeting

Klimyuk, Victor; Cartieaux, Fabienne; Havaux, Michel; Contard-David, Pascale; Schünemann, Danja; Meiherhoff, Karin; Gouet, Patrice; Jones, Jonathan D. G.; Hoffman, Neil E.; Nussaume, Laurent

doi:10.2307/3870840

Cited by 34 publications

(64 citation statements)

References 32 publications

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“…1B) in the leaves. The same treatment was imposed on the chaos mutant that lacks cpSRP43, a subunit of the cpSRP complex (16,17). This mutant has a pale-green phenotype because of a substantial reduction of the LHC level (16,18).…”

Section: Resultsmentioning

confidence: 99%

“…An obstacle in the analysis of the ELIP function in vivo is the multigenicity of these proteins. In this study, we have circumvented this difficulty by using chaos, an Arabidopsis mutant of the chloroplast signal recognition particle (cpSRP) system that is involved in the rapid targeting of LHC-type proteins, including ELIPs, to thylakoid membranes (16)(17)(18). The results presented in this study demonstrate that ELIPs protect plant leaves from photooxidation and suggest that this photoprotective function involves the maintenance of a low level of free chlorophyll under high-light stress conditions.…”

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confidence: 89%

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Early light-induced proteins protect Arabidopsis from photooxidative stress

Hutin

Nussaume

Moise

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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The early light-induced proteins (ELIPs) belong to the multigenic family of light-harvesting complexes, which bind chlorophyll and absorb solar energy in green plants. ELIPs accumulate transiently in plants exposed to high light intensities. By using an Arabidopsis thaliana mutant (chaos) affected in the posttranslational targeting of light-harvesting complex-type proteins to the thylakoids, we succeeded in suppressing the rapid accumulation of ELIPs during high-light stress, resulting in leaf bleaching and extensive photooxidative damage. Constitutive expression of ELIP genes in chaos before light stress resulted in ELIP accumulation and restored the phototolerance of the plants to the wild-type level. Free chlorophyll, a generator of singlet oxygen in the light, was detected by chlorophyll fluorescence lifetime measurements in chaos leaves before the symptoms of oxidative stress appeared. Our findings indicate that ELIPs fulfill a photoprotective function that could involve either the binding of chlorophylls released during turnover of pigment-binding proteins or the stabilization of the proper assembly of those proteins during high-light stress.L ight is essential for plants through photosynthetic carbon assimilation. However, when absorbed light exceeds the photosynthetic capacities, reactive O 2 species are generated in the chloroplasts, causing oxidative damage to proteins, lipids, and photosynthetic pigments (1, 2). This effect is amplified by environmental stresses such as low temperature or drought, for example, that inhibit the photosynthetic activity, leading to strong yield reduction in crops. In green plants, solar energy is collected by chlorophyll-and carotenoid-binding lightharvesting complexes (LHCs), which are encoded by a multigene family of LHC genes. The expression of these genes is tightly regulated by light (2-4). High light intensities inhibit transcription of LHC genes and activate synthesis of the early lightinduced proteins (ELIPs), a class of proteins structurally related to the LHCs (5). The ELIPs are predicted to have three transmembrane helices, and they have sequence similarity to the LHCs in the central pair of helices (6, 7). The similarity is not only at the sequence level, however, because both LHCs and ELIPs bind chlorophyll and carotenoids (8). The ELIPs differ from the LHCs by their transient expression under high-light stress (5). Recently, a number of ELIP-type polypeptides, containing LHC motifs and inducible by high light, have been discovered in vascular plants: the one-helix high-light-induced proteins (9) and the two-helix stress-enhanced proteins (10).The physiological role of the ELIPs in vascular plants has not yet been elucidated, although there have been several suggestions (11)(12)(13)(14). The induction of ELIPs by high light intensities suggests a role in the acclimation to light stress rather than a light-harvesting function, but this has not yet been demonstrated. ELIP antisense transgenic tobacco plants did not exhibit any phenotype of sensitivity to high ...

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Section: Resultsmentioning

confidence: 99%

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confidence: 89%

Early light-induced proteins protect Arabidopsis from photooxidative stress

Hutin

Nussaume

Moise

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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296

250

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“…The fact that the antisense plants have a novel phenotype suggests that ClpC1 and ClpC2 act synergistically or that they might be functionally redundant, but only in part. In this context, it might be relevant that the yellow-heart phenotype is reminiscent of mutants blocked in the import of nuclear-encoded proteins into the chloroplast, e.g., ppi1, chaos, or ffc1 (27)(28)(29)(30). Because ClpC-type Hsp100 chaperones are associated with the chloroplast import apparatus (31), we speculate that ClpC1 might be involved in import, whereas ClpC2 is not.…”

Section: Isolation and Map-based Cloning Of A Var2 Second-site Supprementioning

confidence: 99%

Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis

Park

Rodermel

2004

Proc. Natl. Acad. Sci. U.S.A.

101

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The Arabidopsis var2 variegation mutant defines a nuclear gene for a chloroplast FtsH metalloprotease. Leaf variegation is expressed only in homozygous recessive plants. The cells in the green leaf sectors of this mutant contain morphologically normal chloroplasts, whereas cells in the white sectors contain abnormal plastids lacking organized lamellar structures. var2 mutants are hypersusceptible to photoinhibition, and VAR2 degrades unassembled polypeptides and is involved in the D1 repair cycle of photosystem II, likely by affecting turnover of the photodamaged D1 polypeptide. A second-site suppressor screen of var2 yielded a normalappearing, nonvariegated line. Map-based cloning revealed that the suppression of variegation in this line is due to a splice site mutation in ClpC2, a chloroplast Hsp100 chaperone, that results in sharply reduced ClpC2 protein accumulation. Isolation of clpC2 single mutants showed that clpC2 is epistatic to var2, and that a lack of ClpC2 does not markedly alter the composition of the thylakoid membrane. Suppression by clpC2 is not allele-specific. Our results suggest that clpC2 is a suppressor of thylakoid biogenesis and maintenance and that ClpC2 might act by accelerating photooxidative stress. Arabidopsis has two ClpC genes (ClpC1 and ClpC2), and mutants with down-regulated expression of both genes have a phenotype different from clpC2, suggesting that ClpC1 and ClpC2 act synergistically and͞or that they are only partially redundant. The isolation of a clpC2 mutant represents an important advance in the generation of tools to understand Hsp100 function and insight into the mechanisms of protein quality control in plants.P rotein concentrations within all compartments of the eukaryotic cell are regulated by various mechanisms of protein quality control (1, 2). Chaperones and ATP-dependent proteases are important components of these surveillance systems. In chloroplasts, protein quality control is mediated, in part, by three classes of ATP-dependent proteases that also have chaperone activities: Clp, Lon, and FtsH (3-5). The regulatory (ATPase) and proteolytic domains are located on separate subunits in Clp, whereas in FtsH and Lon they reside on the same polypeptide. These three proteases are evolutionarily derived from the prokaryotic-like ancestors of chloroplasts. A major unanswered question is how the various proteases and chaperones interact to provide an integrated network of protein quality control in the plastid.Photosynthetic organs of the Arabidopsis var2 variegation mutant have green sectors with cells that contain normalappearing chloroplasts and white sectors with cells that have abnormal plastids lacking organized lamellar structures (6, 7). This mutant defines a nuclear recessive gene for a plastidlocalized FtsH homolog (designated AtFtsH2) (8, 9). FtsH genes comprise small multigene families in plants, and the products of these genes are targeted to both plastids and mitochondria (10-12). Arabidopsis contains 12 AtFtsH genes, including three pairs of closely relate...

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“…3 and 4). cpSRP contains a conserved 54-kDa GTPase (cpSRP54) (5,6) but is structurally unique from cytosolic SRPs in that it lacks an RNA moiety (7) and contains a novel 43-kDa protein (cpSRP43) (8,9). The cpSRP⅐LHCP targeting complex, termed transit complex, is directed to a thylakoid translocase containing Albino3 (ALB3) (10,11) by a mechanism that requires cpFtsY (11)(12)(13)(14), a homolog of pro-and eukaryotic SRP receptors, FtsY and SR␣, respectively.…”

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confidence: 99%

“…These adaptor functions associated with cpSRP43 are likely mediated by the putative ankyrin (Ank) domains and chromodomains (chromosome organization modifier) present throughout the protein (see Fig. 1 for domain organization) (9). Ank domains are repetitive ϳ33-amino acid motifs that together form a characteristic and stable structure with surfaces that are tailored for many different macromolecular interactions (for review see Ref.…”

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confidence: 99%