A chloroplast‐localized PPR protein required for plastid ribosome accumulation

Abstract

SummaryThe pentatricopeptide repeat (PPR) is a degenerate 35-amino acid repeating motif that is found in animal, fungal, and plant proteins. The PPR protein family is particularly large in plants, where the majority of family members are predicted to be targeted to mitochondria or chloroplasts. PPR proteins are believed to fall into the larger family of helical repeat proteins, which typically bind macromolecules through a surface formed by the stacking of consecutive helical repeating units. Prior ®ndings implicate several PPR proteins in organellar RNA metabolism, but the biological functions of few PPR proteins have been explored and in no case has a direct substrate been de®nitively identi®ed. We present a characterization of the maize nuclear gene ppr2, which encodes a chloroplast PPR protein. PPR2 is found in large, heterogeneous protein complexes in the chloroplast stroma, some of which may be associated with RNA. Null ppr2 mutants have albino leaves and lack plastid rRNA and translation products. Plastid rRNAs are absent in both dark-and light-grown leaf tissues, indicating that their absence does not result from photo-oxidative damage. The population of plastid transcripts in ppr2 mutants is similar to that in other maize mutants lacking plastid ribosomes, and no ppr2-speci®c defects in plastid RNA metabolism have been detected. Taken together, the results suggest that ppr2 functions in the synthesis or assembly of one or more component of the plastid translation machinery.

Disruption of a Rice Pentatricopeptide Repeat Protein Causes a Seedling-Specific Albino Phenotype and Its Utilization to Enhance Seed Purity in Hybrid Rice Production

“…Fisk et al (1999) first reported a maize PPR gene, (for CHLOROPLAST RNA PROCESSING1), which was implicated by genetic analysis in processing and translation of plastid pet transcripts. Similar effects on plastid transcripts were subsequently observed in other mutants from Arabidopsis (Hashimoto et al, 2003;Meierhoff et al, 2003;Yamazaki et al, 2004;ChateignerBoutin et al, 2008ChateignerBoutin et al, , 2011Chi et al, 2008;Okuda et al, 2009Okuda et al, , 2010Yu et al, 2009;Johnson et al, 2010), rice (Kazama and Toriyama, 2003;Komori et al, 2004;Gothandam et al, 2005), and maize (Williams and Barkan, 2003;Schmitz-Linneweber et al, 2006;Pfalz et al, 2009;Prikryl et al, 2011). Additional evidence for a role of PPR proteins in regulating organelle gene expression has also come from positional cloning of several cytoplasmic male sterility (CMS) restorer genes from petunia (Petunia hybrida; Bentolila et al, 2002) and radish (Raphanus sativus; Brown et al, 2003;Desloire et al, 2003;Koizuka et al, 2003).…”

“…Both DG1 and YS1 encode chloroplast-targeted PPR proteins and YS1 has been shown to be required for editing of rpoB transcripts (Chi et al, 2008;Zhou et al, 2009). The null mutation of the maize PPR2 gene leads to albino seedlings, but does not affect seed development or gametogenesis (Williams and Barkan, 2003). Maize PPR4 (ZmPPR4) is a chloroplast-targeted protein harboring both a PPR tract and an RNA recognition motif and it facilitates transsplicing of chloroplast rps12 premRNA (Schmitz-Linneweber et al, 2006).…”

Effects of Reduced Chloroplast Gene Copy Number on Chloroplast Gene Expression in Maize

“…These authors contrasted the w2 RNA phenotype with those of two other albino mutants (w1 and iojap) that had normal levels of chloroplast DNA but aberrant transcript populations. In hindsight, it is clear that the w1 and iojap RNA and DNA content are typical of mutants in the grasses that lack plastid ribosomes: the ribosome deficiency results in stereotypical changes in transcript patterns presumably caused by the loss of PEP and enhanced transcription by NEP (Williams and Barkan, 2003;Prikryl et al, 2008;Zhelyazkova et al, 2012b). The fact that the transcript populations in w2-Burnham mutants more closely resemble those in wild-type plants than those in mutants lacking plastid ribosomes is interesting, because plastid ribosome abundance is drastically reduced in v2-Burnham mutants.…”

Arabidopsis GLUTAMINE-RICH PROTEIN23Is Essential for Early Embryogenesis and Encodes a Novel Nuclear PPR Motif Protein That Interacts with RNA Polymerase II Subunit III

“…The role of the PPR motif is still not clear. It would be interesting to know whether the PPR motif itself can bind DNA or RNA, as PPR proteins have been shown to possess DNA or RNA binding activity (Barkan et al, 1994;Ikeda and Gray, 1999;Lahmy et al, 2000;Small and Peeters, 2000;Mancebo et al, 2001;Liu and McKeehan, 2002;Tsuchiya et al, 2002;Meierhoff et al, 2003;Mili and Pinol-Roma, 2003;Nakamura et al, 2003;Williams and Barkan, 2003;Lurin et al, 2004;Schmitz-Linneweber et al, 2005).…”

“…2003; Mili and Pinol-Roma, 2003;Nakamura et al, 2003;Williams and Barkan, 2003;Lurin et al, 2004;Schmitz-Linneweber et al, 2005). A few functions have been identified, such as those that enable the restoration of cytoplasmic male fertility (Bentolila et al, 2002;Brown et al, 2003;Desloire et al, 2003;Kazama and Toriyama, 2003;Koizuka et al, 2003;Laforest et al, 2003;Akagi et al, 2004;Komori et al, 2004;Klein et al, 2005) and organelle biogenesis (Barkan et al, 1994;Fisk et al, 1999;Hashimoto et al, 2003;Yamazaki et al, 2004;Kotera et al, 2005).…”