The Pentatricopeptide Repeats Present in Pet309 Are Necessary for Translation but Not for Stability of the Mitochondrial COX1 mRNA in Yeast

Tavares-Carreón, Faviola; Camacho‐Villasana, Yolanda; Zamudio-Ochoa, Angélica; Shingú-Vázquez, Miguel; Torres‐Larios, Alfredo; Pérez-Martı́nez, Xochitl

doi:10.1074/jbc.m708437200

Cited by 85 publications

(80 citation statements)

References 63 publications

(80 reference statements)

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“…The function of these proteins, particularly PPR proteins, has been well characterized (Schmitz-Linneweber and Small, 2008;Stern et al, 2010;Shikanai and Fujii, 2013). PPR proteins in chloroplast have been implicated as being involved in regulating RNA splicing (Schmitz-Linneweber et al, 2006;de Longevialle et al, 2007;Ichinose et al, 2012), RNA editing (Kotera et al, 2005;Okuda et al, 2007;Chateigner-Boutin et al, 2008;Cai et al, 2009;Yu et al, 2009;Zhou et al, 2009;Tseng et al, 2010;Sosso et al, 2012), RNA cleavage (Meierhoff et al, 2003;Hattori et al, 2007), and translation (Williams and Barkan, 2003;Tavares-Carreón et al, 2008) during plant development. The disruption of tetratricopeptide repeat or PPR proteins generally causes defects in the development of chloroplast, eventually leading to the albino or chlorotic leaf phenotype in plants (Chi et al, 2008(Chi et al, , 2010Cao et al, 2011;Su et al, 2012;Gong et al, 2014).…”

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Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

et al. 2016

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Chloroplast, the photosynthetic organelle in plants, plays a crucial role in plant development and growth through manipulating the capacity of photosynthesis. However, the regulatory mechanism of chloroplast development still remains elusive. Here, we characterized a mutant with defective chloroplasts in rice (Oryza sativa), termed albino leaf1 (al1), which exhibits a distinct albino phenotype in leaves, eventually leading to al1 seedling lethality. Electronic microscopy observation demonstrated that the number of thylakoids was reduced and the structure of thylakoids was disrupted in the al1 mutant during rice development, which eventually led to the breakdown of chloroplast. Molecular cloning revealed that AL1 encodes the sole octotricopeptide repeat protein (RAP) in rice. Genetic complementation of Arabidopsis (Arabidopsis thaliana) rap mutants indicated that the AL1 protein is a functional RAP. Further analysis illustrated that three transcript variants were present in the AL1 gene, and the altered splices occurred at the 39 untranslated region of the AL1 transcript. In addition, our results also indicate that disruption of the AL1 gene results in an altered expression of chloroplast-associated genes. Consistently, proteomic analysis demonstrated that the abundance of photosynthesis-associated proteins is altered significantly, as is that of a group of metabolism-associated proteins. More specifically, we found that the loss of AL1 resulted in altered abundances of ribosomal proteins, suggesting that RAP likely also regulates the homeostasis of ribosomal proteins in rice in addition to the ribosomal RNA. Taken together, we propose that AL1, particularly the AL1a and AL1c isoforms, plays an essential role in chloroplast development in rice.

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Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

et al. 2016

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“…However, the COX1 and ATP6/8 mRNAs are both derived from a single polycistronic COX1-ATP6/8 transcript that is processed to yield the two mRNAs (24), so it might be expected that Aep3p and Pet309p function together. Tavares-Carreón et al (59) showed that the PPR motifs in Pet309p are necessary for Cox1p translation but not for stabilization of the COX1 mRNA. Rmd9p (50) and Ccm1p (57) appear to control the processing and stability of multiple mitochondrial mRNAs.…”

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confidence: 99%

Yeast AEP3p Is an Accessory Factor in Initiation of Mitochondrial Translation

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Kramer

et al. 2009

Journal of Biological Chemistry

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“…All the seven human PPR proteins are predicted to be mitochondrial, and functional analysis confirms their role in the expression of the mitochondrial genome (Lightowlers and Chrzanowska-Lightowlers 2008;Davies et al 2009). Three yeast proteins that can be unambiguously assigned to the PPR family: Pet309p (Manthey and McEwen 1995;Perez-Martinez et al 2003;Tavares-Carreon et al 2008), Aep3p (Ellis et al 2004), and Dmr1p also have mitochondrial localization and function. Involvement in mitochondrial genome expression was also confirmed for PPR proteins in Trypanosoma (Pusnik et al 2007).…”

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confidence: 99%

“…The Pet309 protein (Manthey and McEwen 1995;Perez-Martinez et al 2003;Tavares-Carreon et al 2008) is involved in the processing, stability, and translation of COX1 mRNA, while Aep3p (Ellis et al 2004) is involved in maintaining the stability of the ATP6/8 bicistronic mRNA. The third yeast PPR protein, encoded by the YGR150C ORF, which is the subject of this study, is also found in the proteome of mitochondria (Reinders et al 2006), and a mitochondrial localization and respiratory deficient phenotype were reported in highthroughput studies (Steinmetz et al 2002;Merz and Westermann 2009) and mentioned by other investigators (Ellis et al 2004;Moreno et al 2009).…”

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DMR1 (CCM1/YGR150C) of Saccharomyces cerevisiae Encodes an RNA-Binding Protein from the Pentatricopeptide Repeat Family Required for the Maintenance of the Mitochondrial 15S Ribosomal RNA

et al. 2010

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Pentatricopeptide repeat (PPR) proteins form the largest known RNA-binding protein family and are found in all eukaryotes, being particularly abundant in higher plants. PPR proteins localize mostly in mitochondria and chloroplasts, where they modulate organellar genome expression on the posttranscriptional level. The Saccharomyces cerevisiae DMR1 (CCM1, YGR150C) encodes a PPR protein that localizes to mitochondria. Deletion of DMR1 results in a complete and irreversible loss of respiratory capacity and loss of wild-type mtDNA by conversion to r À /r 0 petites, regardless of the presence of introns in mtDNA. The phenotype of the dmr1D mitochondria is characterized by fragmentation of the small subunit mitochondrial rRNA (15S rRNA), that can be reversed by wild-type Dmr1p. Other mitochondrial transcripts, including the large subunit mitochondrial rRNA (21S rRNA), are not affected by the lack of Dmr1p. The purified Dmr1 protein specifically binds to different regions of 15S rRNA in vitro, consistent with the deletion phenotype. Dmr1p is therefore the first yeast PPR protein, which has an rRNA target and is probably involved in the biogenesis of mitochondrial ribosomes and translation.

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The Pentatricopeptide Repeats Present in Pet309 Are Necessary for Translation but Not for Stability of the Mitochondrial COX1 mRNA in Yeast

Cited by 85 publications

References 63 publications

Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

Yeast AEP3p Is an Accessory Factor in Initiation of Mitochondrial Translation

DMR1 (CCM1/YGR150C) of Saccharomyces cerevisiae Encodes an RNA-Binding Protein from the Pentatricopeptide Repeat Family Required for the Maintenance of the Mitochondrial 15S Ribosomal RNA

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