Regulation of plastid rDNA transcription by interaction of CDF2 with two different RNA polymerases

Bligny, Muriel; Courtois, Florence; Thaminy, Safia; Chang, Chung‐Liang; Lagrange, Thierry; Baruah-Wolff, Jahnabi; Stern, David B.; Lerbs-Mache, Silva

doi:10.1093/emboj/19.8.1851

Cited by 72 publications

(53 citation statements)

References 47 publications

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“…In addition to PEP, one or more nuclear-encoded plastid RNAP (NEP) is required for transcription in plastids of higher plants (Liere and Maliga, 1999;Bligny et al, 2000). NEP activity is probably represented by phage-type RNAPs (reviewed in Hess and Bö rner, 1999).…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis Phage-Type RNA Polymerases: Accurate in Vitro Transcription of Organellar Genes

Kühn¹,

Bohne²,

Liere

et al. 2007

The Plant Cell

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The T7 bacteriophage RNA polymerase (RNAP) performs all steps of transcription, including promoter recognition, initiation, and elongation as a single-polypeptide enzyme. Arabidopsis thaliana possesses three nuclear-encoded T7 phage-type RNAPs that localize to mitochondria (RpoTm), plastids (RpoTp), or presumably both organelles (RpoTmp). Their specific functions are as yet unresolved. We have established an in vitro transcription system to examine the abilities of the three Arabidopsis phage-type RNAPs to synthesize RNA and to recognize organellar promoters. All three RpoT genes were shown to encode transcriptionally active RNAPs. RpoTmp displayed no significant promoter specificity, whereas RpoTm and RpoTp were able to accurately initiate transcription from overlapping subsets of mitochondrial and plastidial promoters without the aid of protein cofactors. Our study strongly suggests RpoTm to be the enzyme that transcribes most, if not all, mitochondrial genes in Arabidopsis. Intrinsic promoter specificity, a feature that RpoTm and RpoTp share with the T7 RNAP, appears to have been conserved over the long period of evolution of nuclear-encoded mitochondrial and plastidial RNAPs. Selective promoter recognition by the Arabidopsis phage-type RNAPs in vitro implies that auxiliary factors are required for efficient initiation of transcription in vivo.

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Section: Introductionmentioning

confidence: 99%

Arabidopsis Phage-Type RNA Polymerases: Accurate in Vitro Transcription of Organellar Genes

Kühn¹,

Bohne²,

Liere

et al. 2007

The Plant Cell

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“…This model has recently been challenged by the discovery that both RNA polymerases, NEP and PEP, are already present in dry seeds of Arabidopsis (18). Furthermore, NEP enzymes are present in mature chloroplasts (3,19) when NEP transcripts are rare, thus indicating a general switch in the regulation of the plastid NEP transcriptional activities during chloroplast differentiation. Two different models have recently been proposed to explain developmental switching from principally NEP to principally PEP transcripts in plastids.…”

mentioning

confidence: 99%

Intraplastidial trafficking of a phage-type RNA polymerase is mediated by a thylakoid RING-H2 protein

Azevedo

Courtois

Hakimi

et al. 2008

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

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The plastid genome of dicotyledonous plants is transcribed by three different RNA polymerases; an eubacterial-type enzyme, PEP; and two phage-type enzymes, RPOTp and RPOTmp. RPOTp plays an important role in chloroplast transcription, biogenesis, and mesophyll cell proliferation. RPOTmp fulfills a specific function in the transcription of the rrn operon in proplasts/amyloplasts during seed imbibition/germination and a more general function in chloroplasts during later developmental stages. In chloroplasts, RPOTmp is tightly associated with thylakoid membranes indicating that functional switching of RPOTmp is connected to thylakoid association. By using the yeast two-hybrid system, we have identified two proteins that interact with RPOTmp. The two proteins are very similar, both characterized by three N-terminal transmembrane domains and a C-terminal RING domain. We show that at least one of these proteins is an intrinsic thylakoid membrane protein that fixes RPOTmp on the stromal side of the thylakoid membrane, probably via the RING domain. A model is presented in which light by triggering the synthesis of the RING protein determines membrane association and functional switching of RPOTmp.chloroplast ͉ RING finger T ranscription of this small organellar genome is accomplished by three different RNA polymerases in a developmentally regulated manner (1, 2). One of the three RNA polymerases is of the eubacterial type, and its subunits are encoded on the plastid genome [plastid-encoded RNA polymerase (PEP)]. The two other RNA polymerases are nucleus-encoded [nucleus encoded plastid RNA polymerase (NEP)] and of the phage type (3, 4). Three different genes have been identified in Arabidopsis coding for NEP proteins that are localized in mitochondria (RPOTm, At1g68990), plastids (RPOTp, At2g24120), or in both organelles (RPOTmp, At5g15700; refs. 5 and 6). However, only two genes (RPOTp and RPOTm) have been detected in monocotyledons (4,7,8), thus raising the question of the function of RPOTmp in plastids of dicotyledon plants. Recent results have shown that RPOTp can be regarded as the principal NEP enzyme in chloroplasts playing an important role in chloroplast transcription, biogenesis, and mesophyll cell proliferation (9, 10). Results obtained with RPOTmp indicate partial replacement of RPOTp in RPOTp mutants (10, 11), an early function in lightinduced accumulation of several plastid mRNAs (12, 13), and specific transcription of the rrn operon of Arabidopsis from the PC promoter during seed imbibition and germination (10).Most of the plastid transcription units are preceded by NEP as well as PEP promoters and could be transcribed by the two types of RNA polymerase. However, with a few exceptions, NEP transcripts are barely detectable in mature chloroplasts, and most of the so-far-determined NEP promoters have been analyzed in PEP-deficient photosynthetically inactive plant material (14-17). These results led to an initial model of plastid transcription attributing special importance to NEP for the transcription of ho...

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“…The RUA, Ϫ35, and Ϫ10 promoter elements are conserved in each of the species except pea, suggesting a shared mechanism for the regulation of rRNA transcription in monocots and dicots. Interestingly, RUA also is present in spinach, a species in which PrrnP1 is not recognized as a promoter (Iratni et al, 1994(Iratni et al, , 1997Bligny et al, 2000). Conservation of a functional PrrnP1 promoter in spinach has been confirmed by showing that it is recognized faithfully by the PEP in tobacco plastids when driving the expression of a reporter gene.…”

Section: Conservation Of Prrnp1 Promoter Elementsmentioning

confidence: 97%

“…Transcription from the PrrnP1 and Pc promoters in Arabidopsis chloroplasts is not mutually exclusive, because both promoters are recognized simultaneously (Sriraman et al, 1998a). Thus, Arabidopsis is different from spinach, in which only Pc is used (Iratni et al, 1994(Iratni et al, , 1997Bligny et al, 2000).…”

Section: Conservation Of Prrnp1 Promoter Elementsmentioning

confidence: 99%

“…In spinach, the transcription of rrn initiates in the same region, but from a promoter distinct from the PrrnP1 or the PrrnP2 promoters. This promoter, Pc, is the only promoter upstream of the rrn operon in spinach and probably also is recognized by the nucleus-encoded plastid RNA polymerase (Iratni et al, 1997;Bligny et al, 2000). Pc is used as a second rrn promoter in Arabidopsis (Sriraman et al, 1998a) and is recognized in mustard chloroplasts (Pfannschmidt and Link, 1997).…”

Section: Introductionmentioning

confidence: 99%

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Unique Architecture of the Plastid Ribosomal RNA Operon Promoter Recognized by the Multisubunit RNA Polymerase in Tobacco and Other Higher Plants

et al. 2003

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Expression of the plastid rRNA operon ( rrn ) during development is highly regulated at the level of transcription. The plastid rrn operon in most higher plants is transcribed by the plastid-encoded RNA polymerase (PEP), the multisubunit plastid RNA polymerase from PrrnP1, a 70 -type promoter with conserved ؊ 10 and ؊ 35 core promoter elements. To identify functionally important sequences, the tobacco PrrnP1 was dissected in vivo and in vitro. Based on in vivo deletion analysis, sequences upstream of nucleotide ؊ 83 do not significantly contribute to promoter function. The in vitro analyses identified an essential hexameric sequence upstream of the ؊ 35 element (GTGGGA; the rRNA operon upstream activator [RUA]) that is conserved in monocot and dicot species and suggested that the ؊ 10 element plays only a limited role in PrrnP1 recognition. Mutations in the initial transcribed sequence ( ؉ 9 to ؉ 14) enhanced transcription, the characteristic of strong promoters in prokaryotes. We propose that interaction with the ؊ 10 element in PrrnP1 is replaced in part by direct PEP-RUA (protein-DNA) interaction or by protein-protein interaction between the PEP and an RUA binding transcription factor.

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Regulation of plastid rDNA transcription by interaction of CDF2 with two different RNA polymerases

Cited by 72 publications

References 47 publications

Arabidopsis Phage-Type RNA Polymerases: Accurate in Vitro Transcription of Organellar Genes

Arabidopsis Phage-Type RNA Polymerases: Accurate in Vitro Transcription of Organellar Genes

Intraplastidial trafficking of a phage-type RNA polymerase is mediated by a thylakoid RING-H2 protein

Unique Architecture of the Plastid Ribosomal RNA Operon Promoter Recognized by the Multisubunit RNA Polymerase in Tobacco and Other Higher Plants

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