A functional RNase P protein subunit of bacterial origin in some eukaryotes

Lai, Lien B.; Bernal‐Bayard, Pilar; Mohannath, Gireesha; Lai, Stella M.; Gopalan, Venkat; Vioque, Agustı́n

doi:10.1007/s00438-011-0651-y

Cited by 26 publications

(46 citation statements)

References 44 publications

(48 reference statements)

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“…PRORP enzymes from A. thaliana and Ostreococcus tauri are sufficient to catalyze cleavage of mitochondrial pre-tRNAs in vitro (2,26). However, human mitochondrial RNase P requires two additional protein components for efficient tRNA maturation, a tRNA methyltransferase termed MRPP1 and its binding partner MRPP2 that has promiscuous alcohol dehydrogenase activity (1).…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5′ processing

Howard¹,

Lim²,

Fierke

et al. 2012

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

110

235

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Ribonuclease P (RNase P) catalyzes the maturation of the 5′ end of tRNA precursors. Typically these enzymes are ribonucleoproteins with a conserved RNA component responsible for catalysis. However, protein-only RNase P (PRORP) enzymes process precursor tRNAs in human mitochondria and in all tRNA-using compartments of Arabidopsis thaliana. PRORP enzymes are nuclear encoded and conserved among many eukaryotes, having evolved recently as yeast mitochondrial genomes encode an RNase P RNA. Here we report the crystal structure of PRORP1 from A. thaliana at 1.75 Å resolution, revealing a prototypical metallonuclease domain tethered to a pentatricopeptide repeat (PPR) domain by a structural zinc-binding domain. The metallonuclease domain is a unique high-resolution structure of a Nedd4-BP1, YacP Nucleases (NYN) domain that is a member of the PIN domain-like fold superfamily, including the FLAP nuclease family. The structural similarity between PRORP1 and the FLAP nuclease family suggests that they evolved from a common ancestor. Biochemical data reveal that conserved aspartate residues in PRORP1 are important for catalytic activity and metal binding and that the PPR domain also enhances activity, likely through an interaction with pre-tRNA. These results provide a foundation for understanding tRNA maturation in organelles. Furthermore, these studies allow for a molecular-level comparison of the catalytic strategies used by the only known naturally evolved protein and RNA-based catalysts that perform the same biological function, pre-tRNA maturation, thereby providing insight into the differences between the prebiotic RNA world and the present protein-dominated world.catalytic mechanism | magnesium | molecular recognition A ccording to the RNA world hypothesis, RNA played dual roles as carrier of genetic information and catalyst in a prebiotic world. However, over eons of evolution, proteins with their expanded 20-aa alphabet and greater structural and functional complexity took over many RNA-based functions. Structural insights into this evolutionary transition are limited because of the lack of examples of RNA and protein macromolecules that perform the same biological function in nature. One notable exception is ribonuclease P (RNase P) that catalyzes maturation of the 5′ end of tRNA across all domains of life. Until recently, all known RNase P enzymes included a catalytic RNA component. The discovery of a protein-only RNase P [proteinacous RNase P (PRORP)] from human mitochondria and Arabidopsis thaliana has dramatically shifted this paradigm (1-3). These enzymes represent a unique class of metallonucleases and are conserved among many eukaroytes (1, 2). A. thaliana encodes three PRORP enzymes (PRORP1, -2, and -3) that catalyze pretRNA processing (2). PRORP1 localizes to the mitochondria and chloroplast whereas PRORP2 and PRORP3 localize to the nucleus (2), suggesting that protein-based enzymes catalyze pretRNA maturation in these cellular locations (2, 3). To gain mechanistic and evolutionary insights into the PRORP...

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Section: Discussionmentioning

confidence: 99%

Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5′ processing

Howard¹,

Lim²,

Fierke

et al. 2012

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

110

235

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“…Given the substrate promiscuity of RNA-based nuclear RNase P (Tables 1 and 3), it is surprising that a new, multicomponent complex had to be recruited for this function. An MRPP3 homologous, nuclear-encoded, component located in mitochondria and chloroplasts with RNase P activity (PRORP1) was found in Arabidopsis thaliana (93) and in an unknown location in Ostreococcus tauri (95). This finding represents an example of a relatively recent evolutionary event where RNA function may have been replaced by a showing the general distribution of the protein subunits of RNases P/MRP in the three domains of life.…”

Section: Exceptions To the Rule: Uncommon Sources For Rnase P/mrp Funmentioning

confidence: 92%

“…The numbers indicate how many proteins are found in each domain. Bacteria possess just one protein with neither sequence nor structural homology to the archaeal or eukaryotic proteins, although a protein subunit of bacterial origin has been found in prasinophyte algae such as Ostreococcus tauri, the smallest known free-living eukaryote (95). Four RNase P proteins in archaea are homologous with eukaryotic ones, and up to eight proteins are shared between eukaryotic RNases P/MRP.…”

Section: Exceptions To the Rule: Uncommon Sources For Rnase P/mrp Funmentioning

confidence: 99%

Ribonucleases P/MRP and the Expanding Ribonucleoprotein World

et al. 2012

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SummaryOne of the hallmarks of life is the widespread use of certain essential ribozymes. The ubiquitous ribonuclease P (RNase P) and eukaryotic RNase MRP are essential complexes where a structured, noncoding RNA acts in catalysis. Recent discoveries have elucidated the three-dimensional structure of the ancestral ribonucleoprotein complex, suggested the possibility of a proteinonly composition in organelles, and even noted the absence of RNase P in a non-free-living organism. With respect to these last two findings, import mechanisms for RNases P/MRP into mitochondria have been demonstrated, and RNase P is present in organisms with some of the smallest known genomes. Together, these results have led to an ongoing debate regarding the precise definition of how ''essential'' these ribozymes truly are. IUBMBIUBMB Life, 64(6): [521][522][523][524][525][526][527][528] 2012

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“…SDR5C1 and TRMT10C form a complex and are proposed to play a scaffolding role in pre-tRNA maturation catalyzed by human PRORP (Vilardo et al 2012;Vilardo and Rossmanith 2015). In contrast to the mammalian enzyme, the recombinant PRORPs from plants, some protists, and algae do not require additional proteins for efficient catalysis, offering a simpler model system to understand the function of this new class of nuclease Lai et al 2011;Taschner et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Differential substrate recognition by isozymes of plant protein-only Ribonuclease P

Howard

Karasik

Klemm

et al. 2016

RNA

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Ribonuclease P (RNase P) catalyzes the cleavage of leader sequences from precursor tRNA (pre-tRNA). Typically, these enzymes are ribonucleic protein complexes that are found in all domains of life. However, a new class of RNase P has been discovered that is composed entirely of protein, termed protein-only RNase P (PRORP). To investigate the molecular determinants of PRORP substrate recognition, we measured the binding affinities and cleavage kinetics of Arabidopsis PRORP1 for varied pre-tRNA substrates. This analysis revealed that PRORP1 does not make significant contacts within the trailer or beyond N −1 of the leader, indicating that this enzyme recognizes primarily the tRNA body. To determine the extent to which sequence variation within the tRNA body modulates substrate selectivity and to provide insight into the evolution and function of PRORP enzymes, we measured the reactivity of the three Arabidopsis PRORP isozymes (PRORP1-3) with four pre-tRNA substrates. A 13-fold range in catalytic efficiencies (10 4 -10 5 M −1 s −1 ) was observed, demonstrating moderate selectivity for pre-tRNA substrates. Although PRORPs bind the different pre-tRNA species with affinities varying by as much as 100-fold, the three isozymes have similar affinities for a given pre-tRNA, suggesting similar binding modes. However, PRORP isozymes have varying degrees of cleavage fidelity, which is dependent on the pre-tRNA species and the presence of a 3 ′ -discriminator base. This work defines molecular determinants of PRORP substrate recognition that provides insight into this new class of RNA processing enzymes.

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A functional RNase P protein subunit of bacterial origin in some eukaryotes

Cited by 26 publications

References 44 publications

Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5′ processing

Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5′ processing

Ribonucleases P/MRP and the Expanding Ribonucleoprotein World

Differential substrate recognition by isozymes of plant protein-only Ribonuclease P

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