Further Characterization of Ribosome Binding to Thylakoid Membranes

Hurewitz, J.; Jagendorf, André T.

doi:10.1104/pp.84.1.31

Cited by 14 publications

(6 citation statements)

References 19 publications

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“…Assessment of the effects of antibiotics on protein synthesis in chloroplasts provides important information regarding the basic features of the chloroplast translation system, which also remains to be fully characterized. Certain antibiotics have previously been shown to inhibit chloroplast translation in organello, and perturb development in vivo (Conte et al 2009;Harris et al 1994;Day and Goldschmidt-Clermont 2011;Eichacker et al 1990;Ellis 1969Ellis , 1971Hurewitz and Jagendorf 1987;Kim et al 1994). In order to collect comparative information, such as dose-dependency, among antibiotics that affect chloroplast protein synthesis, we examined the direct effects of antibiotics on translation activity in our chloroplast extract.…”

Section: Resultsmentioning

confidence: 99%

ppGpp inhibits peptide elongation cycle of chloroplast translation system in vitro

Nomura

Takabayashi

Kuroda³

et al. 2011

Plant Mol Biol

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Chloroplasts possess common biosynthetic pathways for generating guanosine 3',5'-(bis)pyrophosphate (ppGpp) from GDP and ATP by RelA-SpoT homolog enzymes. To date, several hypothetical targets of ppGpp in chloroplasts have been suggested, but they remain largely unverified. In this study, we have investigated effects of ppGpp on translation apparatus in chloroplasts by developing in vitro protein synthesis system based on an extract of chloroplasts isolated from pea (Pisum sativum). The chloroplast extracts showed stable protein synthesis activity in vitro, and the activity was sensitive to various types of antibiotics. We have demonstrated that ppGpp inhibits the activity of chloroplast translation in dose-effective manner, as does the toxic nonhydrolyzable GTP analog guanosine 5'-(β,γ-imido)triphosphate (GDPNP). We further examined polyuridylic acid-directed polyphenylalanine synthesis as a measure of peptide elongation activity in the pea chloroplast extract. Both ppGpp and GDPNP as well as antibiotics, fusidic acid and thiostrepton, inhibited the peptide elongation cycle of the translation system, but GDP in the similar range of the tested ppGpp concentration did not affect the activity. Our results thus show that ppGpp directly affect the translation system of chloroplasts, as they do that of bacteria. We suggest that the role of the ppGpp signaling system in translation in bacteria is conserved in the translation system of chloroplasts.

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Section: Resultsmentioning

confidence: 99%

ppGpp inhibits peptide elongation cycle of chloroplast translation system in vitro

Nomura

Takabayashi

Kuroda³

et al. 2011

Plant Mol Biol

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“…Early studies in Chlamydomonas and pea concluded that chloroplast translation always initiates in the stroma and that some ribosomes subsequently become coupled to the thylakoid membrane via the nascent peptide (32,33). Later reports identified several chloroplast mRNAs that are translated in association with the thylakoid membrane, but the results were sometimes conflicting (22,34,35).…”

Section: Discussionmentioning

confidence: 98%

Genome-wide analysis of thylakoid-bound ribosomes in maize reveals principles of cotranslational targeting to the thylakoid membrane

Zoschke

Barkan

2015

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

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Chloroplast genomes encode ∼37 proteins that integrate into the thylakoid membrane. The mechanisms that target these proteins to the membrane are largely unexplored. We used ribosome profiling to provide a comprehensive, high-resolution map of ribosome positions on chloroplast mRNAs in separated membrane and soluble fractions in maize seedlings. The results show that translation invariably initiates off the thylakoid membrane and that ribosomes synthesizing a subset of membrane proteins subsequently become attached to the membrane in a nucleaseresistant fashion. The transition from soluble to membraneattached ribosomes occurs shortly after the first transmembrane segment in the nascent peptide has emerged from the ribosome. Membrane proteins whose translation terminates before emergence of a transmembrane segment are translated in the stroma and targeted to the membrane posttranslationally. These results indicate that the first transmembrane segment generally comprises the signal that links ribosomes to thylakoid membranes for cotranslational integration. The sole exception is cytochrome f, whose cleavable N-terminal cpSecA-dependent signal sequence engages the thylakoid membrane cotranslationally. The distinct behavior of ribosomes synthesizing the inner envelope protein CemA indicates that sorting signals for the thylakoid and envelope membranes are distinguished cotranslationally. In addition, the fractionation behavior of ribosomes in polycistronic transcription units encoding both membrane and soluble proteins adds to the evidence that the removal of upstream ORFs by RNA processing is not typically required for the translation of internal genes in polycistronic chloroplast mRNAs.ribosome profiling | protein targeting | plastid | chloroplast | SecA

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“…Given the altered pigmentation of prpl28‐1 mutant seeds, it can be speculated that the formation of the photosynthetic machinery, which is associated with the greening process, is disturbed. For instance, a specific role of PRPL28 in the translation process on the surface of thylakoid membranes might be hypothesised (Minami and Watanabe, 1984; Hurewitz and Jagendorf, 1987; Zhang et al. , 1999).…”

Section: Discussionmentioning

confidence: 99%

Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development

Romani¹,

Tadini²,

Rossi³

et al. 2012

The Plant Journal

127

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SUMMARYA lack of individual plastid ribosomal proteins (PRPs) can have diverse phenotypic effects in Arabidopsis thaliana, ranging from embryo lethality to compromised vitality, with the latter being associated with photosynthetic lesions and decreases in the expression of plastid proteins. In this study, reverse genetics was employed to study the function of eight PRPs, five of which (PRPS1, -S20, -L27, -L28 and -L35) have not been functionally characterised before. In the case of PRPS17, only leaky alleles or RNA interference lines had been analysed previously. PRPL1 and PRPL4 have been described as essential for embryo development, but their mutant phenotypes are analysed in detail here. We found that PRPS20, -L1, -L4, -L27 and -L35 are required for basal ribosome activity, which becomes crucial at the globular stage and during the transition from the globular to the heart stage of embryogenesis. Thus, lack of any of these PRPs leads to alterations in cell division patterns, and embryo development ceases prior to the heart stage. PRPL28 is essential at the latest stages of embryo-seedling development, during the greening process. PRPS1, -S17 and -L24 appear not to be required for basal ribosome activity and the organism can complete its entire life cycle in their absence. Interestingly, despite the prokaryotic origin of plastids, the significance of individual PRPs for plant development cannot be predicted from the relative phenotypic severity of the corresponding mutants in prokaryotic systems.

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Further Characterization of Ribosome Binding to Thylakoid Membranes

Cited by 14 publications

References 19 publications

ppGpp inhibits peptide elongation cycle of chloroplast translation system in vitro

ppGpp inhibits peptide elongation cycle of chloroplast translation system in vitro

Genome-wide analysis of thylakoid-bound ribosomes in maize reveals principles of cotranslational targeting to the thylakoid membrane

Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development

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