Revisiting the yeast PPR proteins–application of an iterative hidden Markov model algorithm reveals new members of the rapidly evolving family
Abstract
Pentatricopeptide repeat (PPR) proteins are the largest known RNA-binding protein family, and are found in all eukaryotes, being particularly abundant in higher plants. PPR proteins localize mostly to mitochondria and chloroplasts, and many were shown to modulate organellar genome expression on the posttranscriptional level. Although the genomes of land plants encode hundreds of PPR proteins, only a few have been identified in Fungi and Metazoa. As the current PPR motif profiles are built mainly on the basis of the predominant plant sequences, they are unlikely to be optimal for detecting fungal and animal members of the family, and many putative PPR proteins in these genomes may remain undetected. In order to verify this hypothesis, we designed a hidden Markov model-based bioinformatic tool called Supervised Clustering-based Iterative Phylogenetic Hidden Markov Model algorithm for the Evaluation of tandem Repeat motif families (SCIPHER) using sequence data from orthologous clusters from available yeast genomes. This approach allowed us to assign 12 new proteins in Saccharomyces cerevisiae to the PPR family. Similarly, in other yeast species, we obtained a 5-fold increase in the detection of PPR motifs, compared with the previous tools. All the newly identified S. cerevisiae PPR proteins localize in the mitochondrion and are a part of the RNA processing interaction network. Furthermore, the yeast PPR proteins seem to undergo an accelerated divergent evolution. Analysis of single and double amino acid substitutions in the Dmr1 protein of S. cerevisiae suggests that cooperative interactions between motifs and pseudoreversion could be the force driving this rapid evolution.
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PPR proteins play an important role in the control of eukaryotic mitochondrial gene expression, including transcript end maturation, splicing, editing, RNA stabilization, and transcriptional and translational activation.
“Pentatricopeptide repeat (PPR) proteins play an important role in the control of eukaryotic mitochondrial gene expression, including transcript end maturation, splicing, editing, RNA stabilization, and transcriptional and translational activation (Schmitz-Linneweber and Small 2008; Lipinski et al. 2011; Kühl et al. 2011; Herbert et al. 2013; Wang et al. 2017; Barros and Tzagoloff 2017; Seshadri et”
From <i>Candida albicans</i> PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Lipinski et al. 2011
Thirteen putative C. albicans PPR proteins were identified using the SCIPHER algorithm by Lipinski et al. (2011), and 9 of them show clear orthology to well-characterized PPR proteins of S. cerevisiae and S. pombe.
“Thirteen putative C. albicans PPR proteins were identified using the SCIPHER algorithm by Lipinski et al. (2011), and 9 of them show clear orthology to well-characterized PPR proteins of S. cerevisiae and S. pombe (CaAep3p, CaAep2p, CaDmr1p, CaRpo41p, CaPet111p, CaPet309p, CaAtp22p, CaRmd9p, and CaCbp1p) (Kühl et al. 2011; Lipinski et al. 2011; Herbert et al. 2013).”
From <i>Candida albicans</i> PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Lipinski et al. 2011
Cites
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,062 · see citing works
EMBOSS: the European molecular biology open software suite.
Rice, P., Longden, I., & Bleasby, A. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02024-2 · Cited by 9,466 · see citing works
Protein secondary structure prediction based on position-specific scoring matrices.
Jones, D. C. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.3091 · Cited by 5,741 · see citing works
Eddy, S. R. (1998) · Bioinformatics · doi:10.1093/bioinformatics/14.9.755 · Cited by 5,515 · see citing works
Jacob, H. (1988) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(88)80052-7 · Cited by 4,911 · see citing works
Global analysis of protein localization in budding yeast
Huh, W.-K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., & O'Shea, E. K. (2003) · Nature · doi:10.1038/nature02026 · Cited by 4,248 · cited 1× · see citing works
“cerevisiae localize to the mitochondrion, in agreement with whole-proteome localization studies (Huh et al. 2003) and single-gene analyses, and most of them are implicated in the expression of mitochondrial genome, which is expected for this family.”
BackgroundBioGRID: a general repository for interaction datasets
Stark, C. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj109 · Cited by 3,960 · see citing works
Gietz, R. D., & Sugino, A. (1988) · Gene · doi:10.1016/0378-1119(88)90185-0 · Cited by 2,901 · see citing works
Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method
Gietz, R. D., & Woods, R. A. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)50957-5 · Cited by 2,890 · see citing works
The Pfam protein families database
Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp985 · Cited by 2,694 · see citing works
Pfam: clans, web tools and services
FINN, R. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj149 · Cited by 2,307 · see citing works
The genome sequence of Schizosaccharomyces pombe
Wood, V., Gwilliam, R., Rajandream, M.-A., Lyne, M. H., Lyne, R., Stewart, A., SGOUROS, J. G., Peat, N., Hayles, J., Baker, S. G., et al. (2002) · Nature · doi:10.1038/nature724 · Cited by 1,650 · see citing works
Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., de Montigny, J., Marck, C., Neuvéglise, C., Talla, E., et al. (2004) · Nature · doi:10.1038/nature02579 · Cited by 1,623 · see citing works
Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae
Kellis, M., Birren, B. W., & Lander, E. S. (2004) · Nature · doi:10.1038/nature02424 · Cited by 1,500 · see citing works
Hidden Markov model speed heuristic and iterative HMM search procedure
Johnson, L. S., Eddy, S. R., & Portugaly, E. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-431 · Cited by 1,332 · see citing works
Claire Lurin, A., Andrés, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyère, C., Caboche, M. M., Debast, C. X. E. D., Gualberto, J. M., Hoffmann, B., et al. (2004) · The Plant Cell · doi:10.1105/tpc.104.022236 · Cited by 1,308 · see citing works
Automatic clustering of orthologs and in-paralogs from pairwise species comparisons
Remm, M., Storm, C. E. V., & Sonnhammer, E. L. L. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.5197 · Cited by 1,175 · see citing works
PROSITE, a protein domain database for functional characterization and annotation
Sigrist, C. J. A., Cerutti, L., de Castro, E., Langendijk-Genevaux, P. S., Bulliard, V., Bairoch, A., & Hulo, N. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp885 · Cited by 852 · see citing works
The PPR motif – a TPR-related motif prevalent in plant organellar proteins
Small, I., & Peeters, N. M. (2000) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01520-0 · Cited by 839 · see citing works
Pentatricopeptide repeat proteins: a socket set for organelle gene expression
Schmitz‐Linneweber, C., & Small, I. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.10.001 · Cited by 825 · see citing works
Finding Functional Features in Saccharomyces Genomes by Phylogenetic Footprinting
Cliften, P. F., Sudarsanam, P., Desikan, A., Fulton, L. A., Fulton, B., Majors, J. E., Waterston, R., Cohen, B. A., & Johnston, M. (2003) · Science · doi:10.1126/science.1084337 · Cited by 805 · see citing works
The diploid genome sequence of Candida albicans
Jones, T., Federspiel, N. A., Chibana, H., Dungan, J. M., Kalman, S., Magee, B. B., Newport, G., Thorstenson, Y. R., Agabian, N. M., Magee, P. T., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401648101 · Cited by 768 · see citing works
The Ashbya gossypii Genome as a Tool for Mapping the Ancient Saccharomyces cerevisiae Genome
Dietrich, F. S., Voegeli, S., Brachat, S., Lerch, A., Gates, K., Steiner, S., Mohr, C., Pöhlmann, R., Luedi, P. P., Choi, S., et al. (2004) · Science · doi:10.1126/science.1095781 · Cited by 631 · see citing works
Assembly of the Mitochondrial Membrane System
Tzagoloff, A. (1971) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)62289-6 · Cited by 504 · see citing works
Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis
Jeffries, T. W., Grigoriev, I. V., Grimwood, J., Laplaza, J. M., Aerts, A. L., Salamov, A. A., Schmutz, J., Lindquist, E., Dehal, P., Shapiro, H., et al. (2007) · Nature Biotechnology · doi:10.1038/nbt1290 · Cited by 492 · see citing works
Selectionism and Neutralism in Molecular Evolution
Nei, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi242 · Cited by 412 · see citing works
On the Expansion of the Pentatricopeptide Repeat Gene Family in Plants
O’Toole, N., Hattori, M., Andres, C., Iida, K., Claire Lurin, A., Schmitz‐Linneweber, C., Sugita, M., & Small, I. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn057 · Cited by 385 · see citing works
Lee, H., Chou, J., Cheong, L., Chang, N.-H., Yang, S.-Y., & Leu, J. (2008) · Cell · doi:10.1016/j.cell.2008.10.047 · Cited by 384 · see citing works
Protein annotation and modelling servers at University College London
Buchan, D. W. A., Ward, S. M., Lobley, A., Nugent, T., Bryson, K., & Jones, D. T. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq427 · Cited by 351 · see citing works
Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein
Prikryl, J., Rojas, M., Schuster, G., & Barkan, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012076108 · Cited by 298 · see citing works
Contamine, V., & Picard-Bennoun, M. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.2.281-315.2000 · Cited by 289 · see citing works
Fisk, D. G., Walker, M. B., & Barkan, A. (1999) · The EMBO Journal · doi:10.1093/emboj/18.9.2621 · Cited by 252 · see citing works
Automatic clustering of orthologs and inparalogs shared by multiple proteomes
Alexeyenko, A., Tamaš, I., Liu, G., & Sonnhammer, E. L. L. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl213 · Cited by 248 · see citing works
Scannell, D. R., Frank, A. C., Conant, G. C., Byrne, K. P., Woolfit, M., & Wolfe, K. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608218104 · Cited by 235 · cited 1× · see citing works
“2003), Vanderwaltozyma polyspora (Scannell et al. 2007), Kluyveromyces lactis (Zivanovic et al.”
BackgroundDelannoy, É., Stanley, W. A., Bond, C. S., & Small, I. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351643 · Cited by 230 · see citing works
TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences
Ranganathappa, M. K., Lupas, A. N., & Söding, J. (2007) · BMC Bioinformatics · doi:10.1186/1471-2105-8-2 · Cited by 226 · see citing works
Merz, S., & Westermann, B. (2009) · Genome Biology · doi:10.1186/gb-2009-10-9-r95 · Cited by 213 · see citing works
Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases
Bhalerao, R. P., Salchert, K., Bakó, L., Ökrész, L., Szabados, L., Muranaka, T., Machida, Y., Schell, J., & Koncz, C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5322 · Cited by 203 · see citing works
Long range control circuits within mitochondria and between nucleus and mitochondria
Dujardin, G., Pajot, P., Groudinsky, O., & Słonimski, P. P. (1980) · Molecular and General Genetics MGG · doi:10.1007/bf00271736 · Cited by 161 · see citing works
Pentatricopeptide repeat proteins and their emerging roles in plants
Saha, D., Prasad, A. M., & Srinivasan, R. (2007) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2007.03.026 · Cited by 159 · see citing works
Naithani, S., Saracco, S. A., Butler, C. A., & Fox, T. D. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-08-0490 · Cited by 159 · see citing works
Yeast RPO41 gene product is required for transcription and maintenance of the mitochondrial genome.
Greenleaf, A. L., Kelly, J. L., & Lehman, I. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.10.3391 · Cited by 157 · see citing works
Poutre, C. G., & Fox, T. D. (1987) · Genetics · doi:10.1093/genetics/115.4.637 · Cited by 142 · see citing works
Multiple Molecular Mechanisms Cause Reproductive Isolation between Three Yeast Species
Chou, J., Hung, Y.-S., Lin, K.-H., Lee, H.-Y., & Leu, J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000432 · Cited by 141 · see citing works
SAM-T08, HMM-based protein structure prediction
Karplus, K. J. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp403 · Cited by 135 · see citing works
Nakamura, T., Meierhoff, K., Westhoff, P., & Schuster, G. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03796.x · Cited by 125 · see citing works
Dieckmann, C. L., Koerner, T. J., & Tzagoloff, A. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42907-3 · Cited by 124 · see citing works
Thompson, D. A., & Stahl, F. W. (1999) · Genetics · doi:10.1093/genetics/153.2.621 · Cited by 119 · see citing works
Hollingsworth, M. J., & Martin, N. C. (1986) · Molecular and Cellular Biology · doi:10.1128/mcb.6.4.1058 · Cited by 118 · see citing works
Chou, J., & Leu, J. (2010) · BioEssays · doi:10.1002/bies.200900162 · Cited by 109 · see citing works
PhylomeDB: a database for genome-wide collections of gene phylogenies
Huerta‐Cepas, J., Bueno, A., Dopazo, J., & Gabaldón, T. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm899 · Cited by 105 · see citing works
Davies, S. M. K., Rackham, O., Shearwood, A.-M. J., Hamilton, K. L., Narsai, R., Whelan, J., & Filipovska, A. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.04.048 · Cited by 105 · see citing works
Pentatricopeptide Repeat Proteins in Trypanosoma brucei Function in Mitochondrial Ribosomes
Pusnik, M., Small, I., Read, L. K., Fabbro, T., & Schneider, A. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00708-07 · Cited by 98 · see citing works
Rodeheffer, M. S., Boone, B. E., Bryan, A., & Shadel, G. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009901200 · Cited by 95 · see citing works
Evolutionary Genomics: Yeasts Accelerate beyond BLAST
Wolfe, K. H. (2004) · Current Biology · doi:10.1016/j.cub.2004.05.015 · Cited by 89 · see citing works
Pentatricopeptide repeat domain protein 1 lowers the levels of mitochondrial leucine tRNAs in cells
Rackham, O., Davies, S. M. K., Shearwood, A.-M. J., Hamilton, K. L., Whelan, J., & Filipovska, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp627 · Cited by 86 · see citing works
Coupling the mitochondrial transcription machinery to human disease
Shadel, G. S. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.08.005 · Cited by 85 · see citing works
Lipinski, K. A., Kaniak, A., & Golik, P. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.12.019 · Cited by 79 · see citing works
Mulero, J. J., & Fox, T. D. (1993) · Genetics · doi:10.1093/genetics/133.3.509 · Cited by 78 · see citing works
Dieckmann, C. L., Pape, L. K., & Tzagoloff, A. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.6.1805 · Cited by 77 · see citing works
Bonnefoy, N., Bsat, N., & Fox, T. D. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.7.2359-2372.2001 · Cited by 77 · see citing works
The complete mitochondrial genome sequence of the pathogenic yeast Candida (Torulopsis) glabrata
Koszul, R., Malpertuy, A., Frangeul, L., Bouchier, C., Wincker, P., Thierry, A., Duthoy, S., Ferris, S., Hennequin, C., & Dujon, B. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03749-3 · Cited by 76 · see citing works
Krause, K., Lopes de Souza, R., Roberts, D. G. W., & Dieckmann, C. L. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-02-0126 · Cited by 60 · cited 1× · see citing works
“It was shown that at the inner mitochondrial membrane, Cbp1p was associated with Pet127p—a putative 5#-3# exoribonuclease (Krause et al. 2004).”
BackgroundPayne, M. J., Schweizer, E., & Lukins, H. B. (1991) · Current Genetics · doi:10.1007/bf00309594 · Cited by 53 · see citing works
PPR (pentatricopeptide repeat) proteins in mammals: important aids to mitochondrial gene expression
Lightowlers, R. N., & Chrzanowska‐Lightowlers, Z. M. (2008) · Biochemical Journal · doi:10.1042/bj20081942 · Cited by 53 · see citing works
Nouet, C., Bourens, M., Hlaváček, O., Marsy, S., Lemaire, C., & Dujardin, G. (2006) · Genetics · doi:10.1534/genetics.106.063883 · Cited by 51 · see citing works
Finnegan, P. M., Payne, M. J., Keramidaris, E., & Lukins, H. B. (1991) · Current Genetics · doi:10.1007/bf00312765 · Cited by 49 · see citing works
Zeng, X., Hourset, A., & Tzagoloff, A. (2006) · Genetics · doi:10.1534/genetics.106.065821 · Cited by 49 · see citing works
Cbp1 Is Required for Translation of the Mitochondrial Cytochromeb mRNA of Saccharomyces cerevisiae
Islas-Osuna, M. A., Ellis, T. P., Marnell, L. L., Mittelmeier, T. M., & Dieckmann, C. L. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206132200 · Cited by 47 · see citing works
Groth, C., Petersen, R. F., & Piškur, J. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026284 · Cited by 46 · see citing works
Helfenbein, K. G., Ellis, T. P., Dieckmann, C. L., & Tzagoloff, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301679200 · Cited by 46 · see citing works
Rogowska, A., Puchta, O., Czarnecka, A. M., Kaniak, A., Stępień, P. P., & Golik, P. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-08-0796 · Cited by 41 · see citing works
Ellis, T. P., Lukins, H. B., Nagley, P., & Corner, B. E. (1999) · Genetics · doi:10.1093/genetics/151.4.1353 · Cited by 40 · see citing works
Williams, E. H., Butler, C. A., Bonnefoy, N., & Fox, T. D. (2006) · Genetics · doi:10.1534/genetics.106.064576 · Cited by 40 · see citing works
Payne, M. J., Finnegan, P. M., Smooker, P. M., & Lukins, H. B. (1993) · Current Genetics · doi:10.1007/bf00324676 · Cited by 39 · see citing works
Incipient mitochondrial evolution in yeasts
Tian, G.-L., Macadré, C., Kruszewska, A., Szcześniak, B., Ragnini‐Wilson, A., Grisanti, P., Rinaldi, T., Palleschi, C., Frontali, L., Słonimski, P. P., et al. (1991) · Journal of Molecular Biology · doi:10.1016/0022-2836(91)90262-5 · Cited by 39 · see citing works
Relaxation of yeast mitochondrial functions after whole-genome duplicationPreprint
Jiang, H., Guan, W., Pinney, D., Wang, W., & Gu, Z. (2008) · Genome Research · doi:10.1101/gr.074674.107 · Cited by 36 · see citing works
Puchta, O., Lubas, M., Lipinski, K. A., Piatkowski, J., Malecki, M., & Golik, P. (2010) · Genetics · doi:10.1534/genetics.110.113969 · Cited by 33 · see citing works
Self-citationZiaja, K., Michaelis, G., & Lisowsky, T. (1993) · Journal of Molecular Biology · doi:10.1006/jmbi.1993.1095 · Cited by 32 · see citing works
Mitochondrial chromosome structure: an insight from analysis of complete yeast genomes
Nosek, J., Tomáška, Ľ., Bolotin‐Fukuhara, M., & Miyakawa, I. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2005.00016.x · Cited by 30 · see citing works
Stribinskis, V., & Ramos, K. S. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm023 · Cited by 29 · see citing works
Herbert, C. J., Macadré, C., Bécam, A. ‐., Lazowska, J., & Słonimski, P. P. (1992) · Europe PMC (PubMed Central) · Cited by 28 · see citing works
Complete nucleotide sequence of the mitochondrial DNA from
Zivanovic, Y., Wincker, P., Vacherie, B., Bolotin‐Fukuhara, M., & Fukuhara, H. (2004) · FEMS Yeast Research · doi:10.1016/j.femsyr.2004.09.003 · Cited by 24 · see citing works
Stribinskis, V., Heyman, H., Ellis, S. R., Steffen, M. C., & Martín, N. C. R. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.15.6546-6558.2005 · Cited by 24 · see citing works
Analysis of Mitochondrial Protein Synthesis in Yeast
Funes, S., & Herrmann, J. M. (2007) · Methods in molecular biology · doi:10.1007/978-1-59745-365-3_18 · Cited by 15 · see citing works
Matsuoka, M., Matsubara, M., Inoue, J., Kakehi, M., & Imanaka, T. (1994) · Current Genetics · doi:10.1007/bf00309923 · Cited by 10 · see citing works
Flagged first, then by citations
1 of the 87 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Cheng, S., Gutmann, B., Zhong, X., Ye, Y., Fisher, M. F., Bai, F., Castleden, I. R., Song, Y., Song, B., Huang, J., et al. (2016) · The Plant Journal · doi:10.1111/tpj.13121 · Cited by 329 · see citing works
Yagi, Y., Hayashi, S., Kobayashi, K., Hirayama, T., & Nakamura, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057286 · Cited by 293 · see citing works
An overview of pentatricopeptide repeat proteins and their applications
Manna, S. (2015) · Biochimie · doi:10.1016/j.biochi.2015.04.004 · Cited by 258 · see citing works
Mitochondrial Protein Synthesis, Import, and Assembly
Fox, T. D. (2012) · Genetics · doi:10.1534/genetics.112.141267 · Cited by 221 · see citing works
Control of protein synthesis in yeast mitochondria: The concept of translational activators
Herrmann, J. M., Woellhaf, M. W., & Bonnefoy, N. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.03.007 · Cited by 151 · see citing works
The human mitochondrial transcriptome and the RNA‐binding proteins that regulate its expression
Rackham, O., Mercer, T. R., & Filipovska, A. (2012) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1128 · Cited by 104 · see citing works
Nakamura, T., Yagi, Y., & Kobayashi, K. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs069 · Cited by 88 · see citing works
Helical repeats modular proteins are major players for organelle gene expression
Hammani, K., Bonnard, G., Bouchoucha, A., Gobert, A., Pinker, F., Salinas‐Giegé, T., & Giegé, P. (2013) · Biochimie · doi:10.1016/j.biochi.2013.08.031 · Cited by 86 · see citing works
Human pentatricopeptide proteins
Lightowlers, R., & Chrzanowska-Lightowlers, Z. (2013) · RNA Biology · doi:10.4161/rna.24770 · Cited by 47 · see citing works
Modular recognition of nucleic acids by PUF, TALE and PPRproteins
Filipovska, A., & Rackham, O. (2012) · Molecular BioSystems · doi:10.1039/c2mb05392f · Cited by 69 · see citing works
Kühl, I., Dujeancourt, L., Gaisne, M., Herbert, C. J., & Bonnefoy, N. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr511 · Cited by 58 · see citing works
The role of mammalian PPR domain proteins in the regulation of mitochondrial gene expression
Rackham, O., & Filipovska, A. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.10.007 · Cited by 58 · see citing works
Kobayashi, K., Kawabata, M., Hisano, K., Kazama, T., Matsuoka, K., Sugita, M., & Nakamura, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1084 · Cited by 57 · see citing works
Jhuang, H., Lee, H., & Leu, J. (2016) · EMBO Reports · doi:10.15252/embr.201643311 · Cited by 57 · see citing works
Yeast PPR proteins, watchdogs of mitochondrial gene expression
Herbert, C. J., Golik, P., & Bonnefoy, N. (2013) · RNA Biology · doi:10.4161/rna.25392 · Cited by 54 · see citing works
Self-citationSchallenberg‐Rüdinger, M., Lenz, H., Polsakiewicz, M., Gott, J. M., & Knoop, V. (2013) · RNA Biology · doi:10.4161/rna.25755 · Cited by 53 · see citing works
Silva, D. D., Poliquin, S., Zeng, R., Zamudio‐Ochoa, A., Marrero, N., Pérez-Martı́nez, X., Fontanesi, F., & Barrientos, A. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx426 · Cited by 48 · see citing works
Filipovska, A., & Rackham, O. (2013) · RNA Biology · doi:10.4161/rna.24769 · Cited by 42 · see citing works
Tourasse, N. J., Choquet, Y., & Vallon, O. (2013) · RNA Biology · doi:10.4161/rna.26127 · Cited by 39 · see citing works
Mitochondrial Protein Synthesis: Efficiency and Accuracy
Kehrein, K., Bonnefoy, N., & Ott, M. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4896 · Cited by 38 · see citing works
Starting the engine of the powerhouse: mitochondrial transcription and beyond
Miranda, M., Bonekamp, N. A., & Kühl, I. (2022) · Biological Chemistry · doi:10.1515/hsz-2021-0416 · Cited by 34 · see citing works
Zamudio‐Ochoa, A., Camacho‐Villasana, Y., García-Guerrero, A. E., & Pérez-Martı́nez, X. (2014) · RNA Biology · doi:10.4161/rna.29780 · Cited by 36 · see citing works
Seshadri, S. R., Banarjee, C., Barros, M. H., & Fontanesi, F. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa424 · Cited by 30 · see citing works
Hillen, H. S., Markov, D. A., Wojtas, I. D., Hofmann, K. B., Lidschreiber, M., Cowan, A. T., Jones, J. L., Temiakov, D., Cramer, P., & Anikin, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009329118 · Cited by 21 · see citing works
Jalal, A. N., Schwarz, C. K. W., Schmitz‐Linneweber, C., Vallon, O., Nickelsen, J., & Bohne, A. (2015) · Molecular Plant · doi:10.1016/j.molp.2014.11.019 · Cited by 24 · see citing works
Ridlon, L., Škodová‐Sveráková, I., Pan, S., Lukeš, J., & Maslov, D. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.501874 · Cited by 23 · see citing works
Cryo-EM Structures Reveal Transcription Initiation Steps by Yeast Mitochondrial RNA Polymerase
Wijngaert, B. D., Sultana, S., Singh, A., Dharia, C., Vanbuel, H., Shen, J., Vasilchuk, D., Martinez, S. E., Kandiah, E., Patel, S. S., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.11.016 · Cited by 21 · see citing works
Herbert, C. J., Mariotte, S., Cornu, D., Sophie, C., Panozzo, C., Michel, T., Dujardin, G., & Bonnefoy, N. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab789 · Cited by 19 · see citing works
Evolution of loss of heterozygosity patterns in hybrid genomes of Candida yeast pathogens
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · BMC Biology · doi:10.1186/s12915-023-01608-z · Cited by 18 · see citing works
Kühl, I., Fox, T. D., & Bonnefoy, N. (2012) · Mitochondrion · doi:10.1016/j.mito.2012.02.002 · Cited by 18 · see citing works
Aep3p-dependent translation of yeast mitochondrialATP8
de Barros, M. H., & Tzagoloff, A. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-11-0775 · Cited by 18 · see citing works
Jones, J. L., Hofmann, K., Cowan, A. T., Temiakov, D., Cramer, P., & Anikin, M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005355 · Cited by 18 · see citing works
Pusnik, M., & Schneider, A. (2011) · Eukaryotic Cell · doi:10.1128/ec.05213-11 · Cited by 16 · see citing works
Dinh, N., & Bonnefoy, N. (2023) · IUBMB Life · doi:10.1002/iub.2801 · Cited by 14 · see citing works
Mitochondrial Genome Evolution and the Emergence of PPR Proteins
Gutmann, B., Gobert, A., & Giegé, P. (2012) · Advances in botanical research · doi:10.1016/b978-0-12-394279-1.00010-7 · Cited by 13 · see citing works
Moda, B. S., Ferreira-Júnior, J. R., & de Barros, M. H. (2016) · Current Genetics · doi:10.1007/s00294-016-0566-6 · Cited by 10 · see citing works
Golik, P. (2024) · IUBMB Life · doi:10.1002/iub.2779 · Cited by 9 · see citing works
Franco, L. V. R., Moda, B. S., Soares, M. A. K. M., & de Barros, M. H. (2019) · FEBS Journal · doi:10.1111/febs.14785 · Cited by 9 · see citing works
Two pentatricopeptide repeat domain proteins are required for the synthesis of respiratory complex I
Solotoff, V., Moseler, R., & Schulte, U. (2015) · Current Genetics · doi:10.1007/s00294-014-0441-2 · Cited by 7 · see citing works
Translational activators align mRNAs at the small mitoribosomal subunit for translation initiation
Bridgers, J. B., Carlström, A., Sherpa, D., Couvillion, M. T., Rovšnik, U., Gao, J., Wan, B., Shao, S., Ott, M., & Churchman, L. S. (2026) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01726-y · Cited by 6 · see citing works
Piątkowski, J., & Golik, P. (2020) · RNA · doi:10.1261/rna.074880.120 · Cited by 4 · see citing works
Kruszewski, J., & Golik, P. (2016) · Biochemistry (Moscow) · doi:10.1134/s0006297916100084 · Cited by 4 · see citing works
Wenda, J. M., Drzewicka, K., Mulica, P., Tetaud, E., di Rago, J. P., Golik, P., & Łabędzka-Dmoch, K. (2024) · GENETICS · doi:10.1093/genetics/iyae124 · Cited by 2 · see citing works
Insights into the translational activation mechanisms of the COX1 mRNA in yeast mitochondria
Zamudio‐Ochoa, A., Camacho‐Villasana, Y., Pedroza-Dávila, U., García-Guerrero, A. E., & Pérez-Martı́nez, X. (2025) · Journal of Cell Science · doi:10.1242/jcs.263694 · Cited by 1 · see citing works
Searching for α−solenoid proteins involved in organellar gene expression
Cattelin, C., Goulancourt, R., Chatellet, E., Astatourian, A., Robert, C. H., Wollman, F.-A., & Lafontaine, I. (2026) · BMC Genomics · doi:10.1186/s12864-026-12754-3 · Cited by 1 · see citing works
Mechanisms and Control of Protein Synthesis in Yeast Mitochondria
Gruschke, S., & Ott, M. (2013) · Springer eBooks · doi:10.1007/978-3-642-39426-3_5 · Cited by 1 · see citing works
A Small Multifunctional Pentatricopeptide Repeat Protein in the Chloroplast of Chlamydomonas
Schwarz, C. K. W., Schmitz‐Linneweber, C., Vallon, O., & Bohne, A. (2015)
Pérez-Martı́nez, X., Zamudio‐Ochoa, A., Camacho‐Villasana, Y., & García-Guerrero, A. E. (2013) · The FASEB Journal · doi:10.1096/fasebj.27.1_supplement.lb150
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807386
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807395
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807368
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807359
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807398
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807371
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807392
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807410
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807362
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807389
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807380
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807347
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807350
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807374
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807353
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · UvA-DARE (University of Amsterdam) · doi:10.6084/m9.figshare.22807377
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807401
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807356
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807407
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807404
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807344
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807383
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807341
Mixão, V., Nunez‐Rodriguez, J. C., del Olmo, V., Księżopolska, E., Saus, E., Boekhout, T., Gácser, A., & Gabaldón, T. (2023) · Figshare · doi:10.6084/m9.figshare.22807365
Singh, J., Sahu, A. K., & Varshney, U. (2026) · Microbiology · doi:10.1099/mic.0.001689
- Authors
- Lipinski, K. A., Puchta, O., Surendranath, V., Kudla, M., & Golik, P.
- Affiliations
- University of Warsaw (PL)
- Institute of Biochemistry and Biophysics, Polish Academy of Sciences (PL)
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-05-04
- Volume
- 28
- Issue
- 10
- Pages
- 2935-2948
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- OpenAlex
- W2128711175
- Cited by
- 62
- References
- 87
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 12 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 1 · 2017: 3 · 2016: 4 · 2015: 3 · 2014: 3 · 2013: 10 · 2012: 8
- FWCI
- 3.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- pentatricopeptide repeat proteins, PPR proteins, yeast, Saccharomyces cerevisiae, hidden Markov models, mitochondrial RNA processing, post-transcriptional regulation, accelerated evolution, protein family identification
- MeSH terms
- Algorithms, Amino Acid Sequence, Markov Chains, Molecular Sequence Data, Phylogeny, Cluster Analysis, Sequence Alignment, RNA-Binding Proteins, Evolution, Molecular, Genomics, Saccharomyces cerevisiae Proteins, Genome, Mitochondrial
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