Identification of Two Pentatricopeptide Repeat Genes Required for RNA Editing and Zinc Binding by C-terminal Cytidine Deaminase-like Domains

Hayes, Michael L.; Giang, Karolyn; Berhane, Beniam T.; Mulligan, R. Michael

doi:10.1074/jbc.m113.485755

Cited by 72 publications

(90 citation statements)

References 56 publications

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“…In addition, there are several examples in which the DYW deaminase domain is present in a PPR, but may be eliminated by truncation and still support editing of the cognate sites (19,30,31). Finally, PPR genes have been shown to undergo truncation in evolution (19), indicating that the DYW deaminase domain is dispensable in an evolutionary context.…”

Section: Resultsmentioning

confidence: 99%

“…DYW1 has an intact DYW deaminase domain; however, the N-terminal PLS-like region is small and composed of degenerate repeats. Furthermore, DYW1 has canonical zinc binding motifs and has been shown to bind zinc ions (19,20). Mutagenesis of the zinc binding motifs and the catalytic glutamate residue of DYW1 ablated that ability to edit the ndhD site (20).…”

Section: Resultsmentioning

confidence: 99%

“…The requirement of the glutamate residue of the HXE domain and zinc binding by the DYW deaminase domain are two key features that are expected for an editing deaminase. They strongly support the hypothesis that the DYW deaminase domain provides the catalytic activity for the editing reaction.There are several examples in which the DYW deaminase is dispensable for complementation of a knock-out mutant phenotype (19,30,31,47). The truncation of OTP84 had markedly different effects on the three editing site targets.…”

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confidence: 99%

“…This region has canonical zinc binding motifs (HXE, CXXC) (18 -20), which are conserved in deaminases that act on nucleotides, RNA, and DNA (16,(21)(22)(23)(24)(25)(26). The DYW deaminase domain has recently been shown to bind zinc ions (19,20). In addition, mutagenesis of the zinc binding motifs has been shown to interfere with editing in transgenic plants (20) and through transient expression in protoplasts (27).…”

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confidence: 99%

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A Conserved Glutamate Residue in the C-terminal Deaminase Domain of Pentatricopeptide Repeat Proteins Is Required for RNA Editing Activity

Hayes

Dang

Diaz

et al. 2015

Journal of Biological Chemistry

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Background: Pentatricopeptide repeat (PPR) proteins that are required for RNA editing frequently include a C-terminal DYW deaminase domain. Results: Mutagenesis of a glutamate residue in the conserved deaminase HXE motif results in loss of editing activity. Conclusion:The glutamate residue is required for editing. Significance: The DYW deaminase domain of PPR proteins has the molecular characteristics of a deaminase.Many transcripts expressed from plant organelle genomes are modified by C-to-U RNA editing. Nuclear encoded pentatricopeptide repeat (PPR) proteins include an RNA binding domain that provides site specificity. In addition, many PPR proteins include a C-terminal DYW deaminase domain with characteristic zinc binding motifs (CXXC, HXE) and has recently been shown to bind zinc ions. The glutamate residue of the HXE motif is catalytically required in the reaction catalyzed by cytidine deaminase. In this work, we examine the activity of the DYW deaminase domain through truncation or mutagenesis of the HXE motif. OTP84 is required for editing three chloroplast sites, and transgenes expressing OTP84 with C-terminal truncations were capable of editing only one of the three cognate sites at high efficiency. These results suggest that the deaminase domain of OTP84 is required for editing two of the sites, but another deaminase is able to supply the deamination activity for the third site. OTP84 and CREF7 transgenes were mutagenized to replace the glutamate residue of the HXE motif, and transgenic plants expressing OTP84-E824A and CREF7-E554A were unable to efficiently edit the cognate editing sites for these genes. In addition, plants expressing CREF7-E554A exhibited substantially reduced capacity to edit a non-cognate site, rpoA C200. These results indicate that the DYW deaminase domains of PPR proteins are involved in editing their cognate editing sites, and in some cases may participate in editing additional sites in the chloroplast.RNA editing takes place in most land plant chloroplasts and mitochondria (1, 2). In flowering plants, the transcripts of chloroplasts and mitochondria are modified post-transcriptionally by C-to-U editing with about 35 C-to-U editing events in chloroplasts and hundreds of editing sites in the mitochondria (3).Editing in higher plants and in Physcomitrella patens is known to require nuclear proteins (4 -8).Pentatricopeptide repeat (PPR) 2 genes have been shown to be required for RNA editing (9), and form a large family of protein-coding genes in higher plants with over 400 members in Arabidopsis (10). The known editing factors are members of the PLS subfamily of PPR proteins, which are composed of characteristic P, L (long), and S (short) repeats (11). Amino acid residues located in specific locations within the repeats have been shown to specify the base recognized in the cis-element (12)(13)(14), and the PLS repeat domain interacts with specific nucleotides within the cis-element to provide site specificity for RNA editing (12,15).The PLS subfamily of PPR proteins also includes ...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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A Conserved Glutamate Residue in the C-terminal Deaminase Domain of Pentatricopeptide Repeat Proteins Is Required for RNA Editing Activity

Hayes

Dang

Diaz

et al. 2015

Journal of Biological Chemistry

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“…In plants, this process occurs mainly in chloroplasts and mitochondria involving pentatricopeptide proteins for target recognition. Which factor catalyzes the deamination is still not clear, but certain subtypes of pentatricopeptide proteins containing a C-terminal DYW domain bind zinc and may contribute directly to the deaminating activity (Hayes et al, 2013;Shikanai, 2015). Recently, C-to-U editing also was discovered in nuclear plant tRNA-Ser(AGA) and tRNA-Ser(GCT), but the biological function of this modification and the responsible deaminase are still unknown (Zhou et al, 2014).…”

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Of the nine cytidine deaminase like genes in Arabidopsis thaliana eight are pseudogenes and only one is required to maintain pyrimidine homeostasis in vivo

2016

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CYTIDINE DEAMINASE (CDA) catalyzes the deamination of cytidine to uridine and ammonia in the catabolic route of C nucleotides. The Arabidopsis (Arabidopsis thaliana) CDA gene family comprises nine members, one of which (AtCDA) was shown previously in vitro to encode an active CDA. A possible role in C-to-U RNA editing or in antiviral defense has been discussed for other members. A comprehensive bioinformatic analysis of plant CDA sequences, combined with biochemical functionality tests, strongly suggests that all Arabidopsis CDA family members except AtCDA are pseudogenes and that most plants only require a single CDA gene. Soybean (Glycine max) possesses three CDA genes, but only two encode functional enzymes and just one has very high catalytic efficiency. AtCDA and soybean CDAs are located in the cytosol. The functionality of AtCDA in vivo was demonstrated with loss-of-function mutants accumulating high amounts of cytidine but also CMP, cytosine, and some uridine in seeds. Cytidine hydrolysis in cda mutants is likely caused by NUCLEOSIDE HYDROLASE1 (NSH1) because cytosine accumulation is strongly reduced in a cda nsh1 double mutant. Altered responses of the cda mutants to fluorocytidine and fluorouridine indicate that a dual specific nucleoside kinase is involved in cytidine as well as uridine salvage. CDA mutants display a reduction in rosette size and have fewer leaves compared with the wild type, which is probably not caused by defective pyrimidine catabolism but by the accumulation of pyrimidine catabolism intermediates reaching toxic concentrations.

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The Cross-Talk Between Genomes

Budar

Mireau

2017

Annual Plant Reviews, Volume 50

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Identification of Two Pentatricopeptide Repeat Genes Required for RNA Editing and Zinc Binding by C-terminal Cytidine Deaminase-like Domains

Cited by 72 publications

References 56 publications

A Conserved Glutamate Residue in the C-terminal Deaminase Domain of Pentatricopeptide Repeat Proteins Is Required for RNA Editing Activity

A Conserved Glutamate Residue in the C-terminal Deaminase Domain of Pentatricopeptide Repeat Proteins Is Required for RNA Editing Activity

Of the nine cytidine deaminase like genes in Arabidopsis thaliana eight are pseudogenes and only one is required to maintain pyrimidine homeostasis in vivo

The Cross-Talk Between Genomes

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