The 3′-Untranslated Region of Chloroplast psbA mRNA Stabilizes Binding of Regulatory Proteins to the Leader of the Message

Katz, Yael; Danon, Avihai

doi:10.1074/jbc.m201033200

Cited by 22 publications

(11 citation statements)

References 36 publications

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“…Genetic evidence from tobacco (Monde et al 2000;Eibl et al 1999) and perhaps Chlamydomonas (Barnes et al 2005) for such interactions can be found with reporter genes whose RNA levels are suggestive of cooperation between certain 5¢ and 3¢ UTRs. Also, protein binding to the 5¢ UTR of psbA is enhanced by the 3¢ UTR (Katz and Danon 2002). The psbA model might be relevant, if the 3¢ UTR of tufA acts by inhibiting binding of stabilizing proteins to the 5¢ UTR.…”

Section: Discussionmentioning

confidence: 96%

Distinct roles for the 5′ and 3′ untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: identification of an early intermediate in the in vivo degradation pathway

2006

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Elongation factor Tu in Chlamydomonas reinhardtii is a chloroplast-encoded gene (tufA) whose 1.7-kb mRNA has a relatively short half-life. In the presence of chloramphenicol (CAP), which freezes translating chloroplast ribosomes, a 1.5-kb tufA RNA becomes prominent. Rifampicin-chase analysis indicates that the 1.5-kb RNA is a degradation intermediate, and mapping studies show that it is missing 176-180 nucleotides from the 5' end of tufA. The 5' terminus of the intermediate maps to a section of the untranslated region (UTR) predicted to be highly structured and to encode a small ORF. The intermediate could be detected in older cultures in the absence of CAP, indicating that it is not an artifact of drug treatment. Also, it did not overaccumulate in the chloroplast ribosome-deficient mutant, ac20 cr1, indicating its stabilization is specific to elongation-arrested ribosomes. To determine if the 5' UTR of tufA is destabilizing, the corresponding region of the atpA-aadA-rbcL gene was replaced with the tufA sequence, and introduced into the chloroplast genome; the 3' UTR was also substituted for comparison. Analysis of these transformants showed that the transcripts containing the tufA 3'-UTR accumulate to significantly lower levels. Data from constructs based on the vital reporter, Renilla luciferase, confirmed the importance of the tufA 3'-UTR in determining RNA levels, and suggested that the 5' UTR of tufA affects translation efficiency. These data indicate that the in vivo degradation of tufA mRNA begins in the 5' UTR, and is promoted by translation. The data also suggest, however, that the level of the mature RNA is determined more by the 3' UTR than the 5' UTR.

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Section: Discussionmentioning

confidence: 96%

Distinct roles for the 5′ and 3′ untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: identification of an early intermediate in the in vivo degradation pathway

2006

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“…Most chloroplast mRNAs have an AU-rich 3¢-UTR with a terminal inverted repeat that has been shown to function in mRNA processing and stability, and in promoting translation initiation and polysome association (Hayes et al 1996;Memon et al 1996;Monde et al 2000;Rott et al 1998). Interactions between the 5¢-and 3¢-UTRs have also been shown to impact chloroplast translation (Katz and Danon 2002).…”

Section: Introductionmentioning

confidence: 99%

Contribution of 5′- and 3′-untranslated regions of plastid mRNAs to the expression of Chlamydomonas reinhardtii chloroplast genes

et al. 2005

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Expression of chloroplast genes is primarily regulated posttranscriptionally, and a number of RNA elements, found in either the 5'- or 3'-untranslated regions (UTRs) of plastid mRNAs, that impact gene expression have been identified. Complex regulatory and feedback mechanisms influence both translation and protein accumulation, making assignment of roles for specific RNA elements difficult. To identify specific contributions made by various UTRs on translation of plastid mRNAs, we used a heterologous gfp reporter gene that is fused combinatorially to chloroplast 5'- and 3'-UTRs. In general, the 5'-UTR, including the promoter, of the plastid atpA and psbD genes produced the highest levels of chimeric mRNA and protein accumulation, while the 5'-UTR of the rbcL and psbA genes produced less mRNA and protein. Varying the 3'-UTR had little impact on mRNA and protein accumulation, as long as a 3'-UTR was present. Overall, accumulation of chimeric mRNAs was proportional to protein accumulation, with a few notable exceptions. Light-regulated translation continues to operate in chimeric mRNAs containing the 5'-UTR of either the psbA or psbD mRNAs, despite translation of these two chimeric mRNAs at very different efficiencies, suggesting that translational efficiency and light-regulated translation are separate events. Translation of some chimeric mRNAs was much more efficient than others, suggesting that interactions between the untranslated and coding sequences can dramatically impact translational efficiency.

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“…Since the psbA 39UTR may participate in the efficient translation of psbA mRNA (Katz and Danon, 2002), we constructed a 59psbA-petA-39psbA reporter gene. We also constructed a chimeric gene expressing cytochrome f translated under the control of the psbA 59UTR, followed by the first 144 codons of psbA (i.e., up to the 3rd residue of the third transmembrane helix of D1).…”

Section: Assessment Of the Role Of Ces In The Recovery From Photoinhimentioning

confidence: 99%

Chloroplast Biogenesis of Photosystem II Cores Involves a Series of Assembly-Controlled Steps That Regulate Translation

et al. 2005

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The biogenesis of photosystem II, one of the major photosynthetic protein complexes, involves a cascade of assemblygoverned regulation of translation of its major chloroplast-encoded subunits. In Chlamydomonas reinhardtii, the presence of the reaction center subunit D2 is required for the expression of the other reaction center subunit D1, while the presence of D1 is required for the expression of the core antenna subunit apoCP47. Using chimeric genes expressed in the chloroplast, we demonstrate that the decreased synthesis of D1 or apoCP47 in the absence of protein assembly is due to a genuine downregulation of translation. This regulation is mediated by the 59 untranslated region of the corresponding mRNA and originates from negative feedback exerted by the unassembled D1 or apoCP47 polypeptide. However, autoregulation of translation of subunit D1 is not implicated in the recovery from photoinhibition, which involves an increased translation of psbA mRNA in response to the degradation of photodamaged D1. De novo synthesis and repair of photosystem II complexes are independently controlled.

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The 3′-Untranslated Region of Chloroplast psbA mRNA Stabilizes Binding of Regulatory Proteins to the Leader of the Message

Cited by 22 publications

References 36 publications

Distinct roles for the 5′ and 3′ untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: identification of an early intermediate in the in vivo degradation pathway

Distinct roles for the 5′ and 3′ untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: identification of an early intermediate in the in vivo degradation pathway

Contribution of 5′- and 3′-untranslated regions of plastid mRNAs to the expression of Chlamydomonas reinhardtii chloroplast genes

Chloroplast Biogenesis of Photosystem II Cores Involves a Series of Assembly-Controlled Steps That Regulate Translation

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