Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes

Kropat, Janette; Oster, Ulrike; Rüdiger, Wolfhart; Beck, Christoph F.

doi:10.1073/pnas.94.25.14168

Cited by 237 publications

(218 citation statements)

References 38 publications

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“…In Chlamydomonas, intermediates in the chlorophyll biosynthetic pathway modulate the accumulation of transcripts of several nuclear chloroplast genes (Johanningmeier and Howell, 1984;Kropat et al, 1997). Arabidopsis mutants that do not react to norflurazoninduced photo-oxidative damage by repression of Lhcb transcription (genomes uncoupled 1 -5: gun1 -5) were affected in genes encoding proteins involved in tetrapyrrole metabolism: the products of GUN2/HY1 and GUN3/HY2 contribute to heme degradation in the ''Fe branch'' of tetrapyrrole biosynthesis (Mochizuki et al, 2001), GUN5 encodes the CHL H subunit of the Mg-chelatase (Mochizuki et al, 2001), and GUN4 binds product and substrate of Mgchelatase, and activates Mg-chelatase (Larkin et al, 2003).…”

Section: Tetrapyrrole Signallingmentioning

confidence: 99%

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Leister¹

2005

Gene

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Post-endosymbiotic evolution of chloroplasts was characterized by a massive transfer of cyanobacterial genes to the nucleus, followed by re-routing of many of their encoded proteins. In consequence, most plastid proteins are nucleus-encoded, enabling an anterograde (nucleusto-plastid) control of the organelle. The regulation of chloroplast functions includes also cross-talk between chloroplasts and mitochondria, as well as retrograde (plastid-to-nucleus) signalling. Genetic analyses reveal that redox state, flux through the chlorophyll biosynthetic pathway, sugar sensing and reactive oxygen species contribute to retrograde signalling. However, the identity of the messenger molecule(s) remains largely unknown. Novel facets of the chloroplast -mitochondrion cross-talk have been revealed by the characterization of mitochondrial mutants affected in chloroplast properties. Studies of the nuclear chloroplast transcriptome imply the existence of at least three distinct types of transcriptional regulation: a master switch, acting in a binary mode by either inducing or repressing the same large set of genes; a ''mixed response'' with about equal numbers of up-and down-regulated genes; and mechanisms supporting the specific co-regulation of nuclear genes for photosynthesis and for plastid gene expression. The recent discovery of the latter mode of control highlights a possibly ancient route to co-ordinate chloroplast and nuclear genome expression. D

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Section: Tetrapyrrole Signallingmentioning

confidence: 99%

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Leister¹

2005

Gene

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“…The role of plastids in the control of nuclear gene expression and photomorphogenesis is believed to occur through a plastid signaling pathway. Biochemical and genetic methods have identi®ed two possible components, chlorophyll precursors (Johanningmeier and Howell, 1984;Kropat et al, 1997;Nobuyoshi et al, 2001) and the plastoquinone redox state (Alfonso et al, 2000;Escoubas et al, 1995;Pfanneschmidt et al, 1999). In previous studies (Cao et al, 2000), blocking photosynthesis of wild-type seedlings with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) caused a decrease in the expression of the ferredoxin gene but had no effect on the subset of light-induced genes whose expression is decreased in cr88 seedlings.…”

Section: Indirect Effect Of Cr88 In Photomorphogenesis and Nitrate Asmentioning

confidence: 99%

“…These observations led to the proposal that communication between plastids and nucleus is mediated through a`plastid signal' (Oelmuller and Briggs, 1990). Genetic and biochemical studies using green algae have identi®ed chlorophyll precursors, tetrapyrroles, and the redox state of chloroplast as possible signals (Escoubas et al, 1995;Johanningmeier, 1988;Johanningmeier and Howell, 1984;Kropat et al, 1997). The isolation of gun mutants in Arabidopsis that are defective in this communication, and the identi®cation of these genes also point towards tetrapyrrole involvement in the`plastid signal' (Nobuyoshi et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

The chlorate‐resistant and photomorphogenesis‐defective mutant cr88 encodes a chloroplast‐targeted HSP90

et al. 2003

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SummaryThe cr88 mutant of Arabidopsis is a novel chlorate-resistant mutant that displays long hypocotyls in red light, but not in far red or blue light, and is delayed in the greening process. In cotyledons and young leaves, plastids are less developed compared with those of the wild type. In addition, a subset of light-regulated genes are under-expressed in this mutant. To understand the pleiotropic phenotypes of cr88, we isolated the CR88 gene through map-based cloning. We found that CR88 encodes a chloroplast-targeted 90-kDa heat shock protein (HSP90). The CR88 gene is expressed at highest levels during early post-germination stages and in leaves and reproductive organs. It is constitutively expressed but is also light and heat shock inducible. Chloroplast import experiments showed that the protein is localized to the stroma compartment of the chloroplast. The possible function of an HSP90 in the chloroplast and a plausible explanation of the pleiotropic phenotypes observed in cr88 are discussed.

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“…Plastid-dependent regulation of nuclear genes has been previously described. In Chlamydomonas reinhardtii, the chlorophyll precursors act as intermediates in the light-regulated signaling pathway controlling the transcription rate of the nuclear heat shock genes hsp70a (cytosolic) and hsp70b (chloroplastic; Kropat et al, 1997). Light regulation of Fed-1 (chloroplastic ferredoxin) mRNA abundance in leaves of green plants is posttranscriptionally regulated.…”

Section: Discussionmentioning

confidence: 99%

“…We have, at present, no data for suggesting which is the molecular identity of the chloroplast signal exiting the chloroplast. Previous works have suggested that protoporphyrin IX may act as a possible diffusing compound reaching the cytoplasm through an envelope-localized ABC transporter (Kropat et al, 1997;Moller et al, 2001). However, we did not observe changes in protoporphyrin IX levels in barley mutants impaired in chloroplast-dependent cor gene expression.…”

Section: Discussionmentioning

confidence: 99%

cor Gene Expression in Barley Mutants Affected in Chloroplast Development and Photosynthetic Electron Transport

Bosco¹,

Busconi²,

Govoni³

et al. 2003

Plant Physiology

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The expression of several barley (Hordeum vulgare) cold-regulated (cor) genes during cold acclimation was blocked in the albino mutant a n , implying a chloroplast control on mRNAs accumulation. By using albino and xantha mutants ordered according to the step in chloroplast biogenesis affected, we show that the cold-dependent accumulation of cor14b, tmc-ap3, and blt14 mRNAs depends on plastid developmental stage. Plants acquire the ability to fully express cor genes only after the development of primary thylakoid membranes in their chloroplasts. To investigate the chloroplast-dependent mechanism involved in cor gene expression, the activity of a 643-bp cor14b promoter fragment was assayed in wild-type and albino mutant a n leaf explants using transient ␤-glucuronidase reporter expression assay. Deletion analysis identified a 27-bp region between nucleotides Ϫ274 and Ϫ247 with respect to the transcription start point, encompassing a boundary of some element that contributes to the cold-induced expression of cor14b. However, cor14b promoter was equally active in green and in albino a n leaves, suggesting that chloroplast controls cor14b expression by posttranscriptional mechanisms. Barley mutants lacking either photosystem I or II reaction center complexes were then used to evaluate the effects of redox state of electron transport chain components on COR14b accumulation. In the mutants analyzed, the amount of COR14b protein, but not the steady-state level of the corresponding mRNA, was dependent on the redox state of the electron transport chain. Treatments of the vir-zb63 mutant with electron transport chain inhibitors showed that oxidized plastoquinone promotes COR14b accumulation, thus suggesting a molecular relationship between plastoquinone/plastoquinol pool and COR14b.Plastid proteins are encoded by both nuclear and plastid genomes. Interaction between the two genetic systems is therefore needed for a coordinated response to environmental factors affecting chloroplast biogenesis (Goldschmidt-Clermont, 1998). Impaired plastid function leads to a decline of many mRNAs encoded in the nucleus, suggesting that plastid signals are required for the nuclear gene expression (Oelmü ller et al., 1986). In barley (Hordeum vulgare), the albostrians mutant, lacking plastid ribosomes, showed an altered expression of many nuclear genes when compared with the corresponding wild type, as shown by the decreased level of nuclear gene transcripts encoding chloroplast as well as a few nonchloroplast proteins. Thus, a role for plastid factors in the control of the nuclear genome was inferred (Hess et al., 1994).In the chloroplast membranes, environmental conditions (e.g. excess light and/or low temperature) affect light-induced electron transport rate, and thus the plastoquinone redox state reflects the balance between light harvesting and energy use. Overreduction of plastoquinone pool causes photoinhibition of photosynthesis . The redox state of the plastoquinone controls several functions involved in chloroplast biogenesis: the...

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Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes

Cited by 237 publications

References 38 publications

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

The chlorate‐resistant and photomorphogenesis‐defective mutant cr88 encodes a chloroplast‐targeted HSP90

cor Gene Expression in Barley Mutants Affected in Chloroplast Development and Photosynthetic Electron Transport

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