The CRM domain: An RNA binding module derived from an ancient ribosome-associated protein

Barkan, Alice; Klipcan, Larik; Ostersetzer, Oren; Kawamura, Tetsuya; Asakura, Yukari; Watkins, Kenneth P.

doi:10.1261/rna.139607

Cited by 101 publications

(137 citation statements)

References 40 publications

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“…It is becoming apparent that the emergence of these organelle-specific features of RNA metabolism was paralleled by the evolution of an RNA binding protein repertoire that is largely distinct from that in either bacteria or in the nuclearcytosolic compartment. Previously described examples of RNA binding protein classes that are found specifically in organelles include the PPR, CRM, and PORR families, each of which functions in organelle-specific aspects of RNA metabolism (Small and Peeters, 2000;Barkan et al, 2007;Schmitz-Linneweber and Small, 2008;Kroeger et al, 2009). Results presented here strongly suggest that DUF794 is, likewise, the product of a coevolutionary process that spawned a diversity of noncanonical RNA binding motifs in conjunction with the emergence of the complex RNA metabolism characteristic of plant organelles.…”

Section: Duf794 and The Plant Apo Protein Familymentioning

confidence: 58%

APO1 Promotes the Splicing of Chloroplast Group II Introns and Harbors a Plant-Specific Zinc-Dependent RNA Binding Domain

et al. 2011

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Arabidopsis thaliana APO1 is required for the accumulation of the chloroplast photosystem I and NADH dehydrogenase complexes and had been proposed to facilitate the incorporation of [4Fe-4S] clusters into these complexes. The identification of maize (Zea mays) APO1 in coimmunoprecipitates with a protein involved in chloroplast RNA splicing prompted us to investigate a role for APO1 in splicing. We show here that APO1 promotes the splicing of several chloroplast group II introns: in Arabidopsis apo1 mutants, ycf3-intron 2 remains completely unspliced, petD intron splicing is strongly reduced, and the splicing of several other introns is compromised. These splicing defects can account for the loss of photosynthetic complexes in apo1 mutants. Recombinant APO1 from both maize and Arabidopsis binds RNA with high affinity in vitro, demonstrating that DUF794, the domain of unknown function that makes up almost the entirety of APO1, is an RNA binding domain. We provide evidence that DUF794 harbors two motifs that resemble zinc fingers, that these bind zinc, and that they are essential for APO1 function. DUF794 is found in a plant-specific protein family whose members are all predicted to localize to mitochondria or chloroplasts. Thus, DUF794 adds a new example to the repertoire of plant-specific RNA binding domains that emerged as a product of nuclear-organellar coevolution.

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Section: Duf794 and The Plant Apo Protein Familymentioning

confidence: 58%

APO1 Promotes the Splicing of Chloroplast Group II Introns and Harbors a Plant-Specific Zinc-Dependent RNA Binding Domain

et al. 2011

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“…These domains include RNA recognition motifs (RRMs), serine-argininerich motifs (Manley and Tacke, 1996), RGG boxes (Kiledjian and Dreyfuss, 1992), K homology motifs (Burd and Dreyfuss, 1994), and chloroplast RNA splicing and ribosome maturation (CRM) domains (Barkan et al, 2007). RBPs containing RRMs are the most common among eukaryotes (Anantharaman et al, 2002;Burd and Dreyfuss, 1994).…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic and Expression Analysis of RNA-binding Proteins with Triple RNA Recognition Motifs in Plants

Peal¹,

Jambunathan²,

Mahalingam³

2011

Molecules and Cells

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The superfamily of RNA binding proteins (RBPs) is vastly expanded in plants compared to other eukaryotes. A subfamily of RBPs that contain three RNA recognition motifs (RRMs) from the Arabidopsis (24), rice (19) and poplar (37) genomes was analyzed in this study. Phylogenetic analysis with full-length protein sequences of 80 RBPs identified nine clades. The largest clade, comprising 23 members, showed high homology to human RBPs involved in oxidative signaling. Digital northern analysis revealed that Arabidopsis RBPs are transcriptionally responsive to biotic, abiotic and hormonal treatments. Northern blot analysis of eight Arabidopsis RBPs belonging to the tobacco RBP45/47 family showed that these genes respond to ozone stress. AtRBP45b, which shows closest homology to the yeast oxidative stress regulatory protein, CSX1, was expressed in multiple tissues. Two novel splice variant forms of AtRBP45b were identified by 3'RACE analysis. Based on RT-PCR, splice variant AtRBP45b-SV1 was observed only in response to mechanical wounding caused by pathogen or chemical infiltrations and was not detectable in response to salt or temperature stress. Electrophoretic mobility shift assay demonstrated that recombinant full-length and splice variant forms of AtRBP45b bound synthetic RNA. Identifying in vivo RNA targets of AtRBP45b will aid in determining the precise functional role of these proteins during oxidative signaling.

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“…The genetic identification of nuclear genes involved in chloroplast group II intron splicing led to the recognition of a protein family defined by a novel RNA binding domain denoted the chloroplast RNA splicing and ribosome maturation (CRM) domain (also called the CRS1-YhbY domain/Pfam PF01985) (Till et al 2001;Ostheimer et al 2003;Barkan et al 2007). This domain is derived from a prokaryotic pre-ribosome binding protein, and is found in a family comprising 14 orthologous groups in vascular plants ).…”

Section: Introductionmentioning

confidence: 99%

Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts

Asakura¹,

Bayraktar²,

Barkan³

2008

RNA

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Chloroplast genomes in angiosperms encode ;20 group II introns, approximately half of which are classified as subgroup IIB. The splicing of all but one of the subgroup IIB introns requires a heterodimer containing the peptidyl-tRNA hydrolase homolog CRS2 and one of two closely related proteins, CAF1 or CAF2, that harbor a recently recognized RNA binding domain called the CRM domain. Two CRS2/CAF-dependent introns require, in addition, a CRM domain protein called CFM2 that is only distantly related to CAF1 and CAF2. Here, we show that CFM3, a close relative of CFM2, associates in vivo with those CRS2/CAFdependent introns that are not CFM2 ligands. Mutant phenotypes in rice and Arabidopsis support a role for CFM3 in the splicing of most of the introns with which it associates. These results show that either CAF1 or CAF2 and either CFM2 or CFM3 simultaneously bind most chloroplast subgroup IIB introns in vivo, and that the CAF and CFM subunits play nonredundant roles in splicing. These results suggest that the expansion of the CRM protein family in plants resulted in two subfamilies that play different roles in group II intron splicing, with further diversification within a subfamily to accommodate multiple intron ligands.

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The CRM domain: An RNA binding module derived from an ancient ribosome-associated protein

Cited by 101 publications

References 40 publications

APO1 Promotes the Splicing of Chloroplast Group II Introns and Harbors a Plant-Specific Zinc-Dependent RNA Binding Domain

APO1 Promotes the Splicing of Chloroplast Group II Introns and Harbors a Plant-Specific Zinc-Dependent RNA Binding Domain

Phylogenetic and Expression Analysis of RNA-binding Proteins with Triple RNA Recognition Motifs in Plants

Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts

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