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Non Coding RNAs in Plants pp 193–208Cite as

Regulatory Roles of Novel Small RNAs from Pseudogenes

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Part of the book series: RNA Technologies ((RNATECHN))

Abstract

Arising from gene duplications or retrotranspositions, pseudogenes are genomic sequences with high sequence similarity to functional genes but unable to encode the same type of functional molecular products as what their parental sequences produce. For those that are copies of protein-coding genes, this means that they have lost the potential of encoding a functional protein due to disruption in their putative open reading frames. Several computational algorithms have been developed for detecting pseudogenes in recent years and their applications have annotated hundreds and thousands of pseudogenes in higher eukaryotic genomes, including the rice and Arabidopsis genomes. While conventional wisdom considers pseudogenes as dead and inactive sequences, emerging evidence indicates that a large number of higher eukaryotic pseudogenes are transcriptionally alive and that furthermore many of the pseudogene transcripts may play a critical role in regulating gene expression. In particular, analyses of the RNAs from both plant and mammalian tissues or organs using deep-sequencing technology have uncovered scores of pseudogene-derived small RNAs. Their sequence features, together with carefully designed biochemical and genetic experiments, indicate that small RNAs from pseudogenes may function at different molecular levels, either as small interference RNAs directly regulating functional genes or modulating epigenomic silencing in the pseudogenic regions, or as decoy RNAs counteracting the inhibitory effectiveness of miRNAs supposedly targeting functional genes. These exciting discoveries suggest that pseudogenes may represent a hidden layer of regulatory elements in eukaryotic genomes, whose functional importance has just started to be unveiled and appreciated.

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References

  • Allen E, Xie Z, Gustafson AM et al (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Balakirev ES, Ayala FJ (2003) Pseudogenes: are they “Junk” or functional DNA? Annu Rev Genet 37:123–151

    Article  PubMed  CAS  Google Scholar 

  • Balasubramanian S, Zheng D, Liu YJ et al (2009) Comparative analysis of processed ribosomal protein pseudogenes in four mammalian genomes. Genome Biol 10:R2

    Article  PubMed  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132

    Article  PubMed  CAS  Google Scholar 

  • Benovoy D, Drouin G (2006) Processed pseudogenes, processed genes, and spontaneous mutations in the Arabidopsis genome. J Mol Evol 62:511–522

    Article  PubMed  CAS  Google Scholar 

  • Birchler JA, Kavi HH (2008) Molecular biology. Slicing and dicing for small RNAs. Science 320:1023–1024

    Article  PubMed  CAS  Google Scholar 

  • Bischof JM, Chiang AP, Scheetz TE et al (2006) Genome-wide identification of pseudogenes capable of disease-causing gene conversion. Hum Mutat 27:545–552

    Article  PubMed  CAS  Google Scholar 

  • Borsani O, Zhu J, Verslues PE et al (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280

    Article  PubMed  CAS  Google Scholar 

  • Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D, Liu FL, Zhang L (1998) The evolution of the alcohol dehydrogenase gene family by loss of introns in plants of the genus Leavenworthia (Brassicaceae). Mol Biol Evol 15:552–559

    Article  PubMed  CAS  Google Scholar 

  • Coin L, Durbin R (2004) Improved techniques for the identification of pseudogenes. Bioinformatics 20:i94–i100

    Article  PubMed  CAS  Google Scholar 

  • Cole ST, Eiglmeier K, Parkhill J et al (2001) Massive gene decay in the leprosy bacillus. Nature 409:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • Drouin G, Dover GA (1987) A plant processed pseudogene. Nature 328:557–558

    Article  CAS  Google Scholar 

  • Duret L, Chureau C, Samain S et al (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312:1653–1655

    Article  PubMed  CAS  Google Scholar 

  • Frith MC, Wilming LG, Forrest A et al (2006) Pseudo-messenger RNA: phantoms of the transcriptome. PLoS Genet 2:e23

    Article  PubMed  Google Scholar 

  • Gingerich DJ, Hanada K, Shiu SH et al (2007) Large-scale, lineage-specific expansion of a bric-a-brac/tramtrack/broad complex ubiquitin-ligase gene family in rice. Plant Cell 19:2329–2348

    Article  PubMed  CAS  Google Scholar 

  • Glusman G, Yanai I, Rubin I et al (2001) The complete human olfactory subgenome. Genome Res 11:685–702

    Article  PubMed  CAS  Google Scholar 

  • Gojobori T, Ishii K, Nei M (1982) Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. J Mol Evol 18:414–423

    Article  PubMed  CAS  Google Scholar 

  • Graur D, Shuali Y, Li WH (1989) Deletions in processed pseudogenes accumulate faster in rodents than in humans. J Mol Evol 28:279–285

    Article  PubMed  CAS  Google Scholar 

  • Guo X, Wang Y, Keightley PD et al (2007) Patterns of selective constraints in noncoding DNA of rice. BMC Evol Biol 7:208

    Article  PubMed  Google Scholar 

  • Guo X, Zhang Z, Gerstein MB et al (2009) Small RNAs originated from pseudogenes: cis- or trans-acting? PLoS Comput Biol 5:e1000449

    Article  PubMed  Google Scholar 

  • Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614

    Article  PubMed  CAS  Google Scholar 

  • Harrison PM, Gerstein M (2002) Studying genomes through the aeons: protein families, pseudogenes and proteome evolution. J Mol Biol 318:1155–1174

    Article  PubMed  CAS  Google Scholar 

  • Harrison PM, Echols N, Gerstein MB (2001) Digging for dead genes: an analysis of the characteristics of the pseudogene population in the Caenorhabditis elegans genome. Nucleic Acids Res 29:818–830

    Article  PubMed  CAS  Google Scholar 

  • Harrison P, Kumar A, Lan N et al (2002a) A small reservoir of disabled ORFs in the yeast genome and its implications for the dynamics of proteome evolution. J Mol Biol 316:409–419

    Article  PubMed  CAS  Google Scholar 

  • Harrison PM, Hegyi H, Balasubramanian S et al (2002b) Molecular fossils in the human genome: identification and analysis of the pseudogenes in chromosomes 21 and 22. Genome Res 12:272–280

    Article  PubMed  CAS  Google Scholar 

  • Harrison PM, Milburn D, Zhang Z et al (2003) Identification of pseudogenes in the Drosophila melanogaster genome. Nucleic Acids Res 31:1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Harrison PM, Zheng D, Zhang Z et al (2005) Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability. Nucleic Acids Res 33:2374–2383

    Article  PubMed  CAS  Google Scholar 

  • Homma K, Fukuchi S, Kawabata T et al (2002) A systematic investigation identifies a significant number of probable pseudogenes in the Escherichia coli genome. Gene 294:25–33

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Jacq C, Miller JR, Brownlee GG (1977) A pseudogene structure in 5S DNA of Xenopus laevis. Cell 12:109–120

    Article  PubMed  CAS  Google Scholar 

  • Karro JE, Yan Y, Zheng D et al (2007) Pseudogene.org: a comprehensive database and comparison platform for pseudogene annotation. Nucleic Acids Res 35:D55–D60

    Article  PubMed  CAS  Google Scholar 

  • Kasschau KD, Fahlgren N, Chapman EJ et al (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5:e57

    Article  PubMed  Google Scholar 

  • Khelifi A, Duret L, Mouchiroud D (2005) HOPPSIGEN: a database of human and mouse processed pseudogenes. Nucleic Acids Res 33:D59–D66

    Article  PubMed  Google Scholar 

  • Korneev S, O’Shea M (2002) Evolution of nitric oxide synthase regulatory genes by DNA inversion. Mol Biol Evol 19:1228–1233

    Article  PubMed  CAS  Google Scholar 

  • Korneev SA, Park JH, O’Shea M (1999) Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene. J Neurosci 19:7711–7720

    PubMed  CAS  Google Scholar 

  • Korneev SA, Straub V, Kemenes I et al (2005) Timed and targeted differential regulation of nitric oxide synthase (NOS) and anti-NOS genes by reward conditioning leading to long-term memory formation. J Neurosci 25:1188–1192

    Article  PubMed  CAS  Google Scholar 

  • Lerat E, Ochman H (2004) Psi-Phi: exploring the outer limits of bacterial pseudogenes. Genome Res 14:2273–2278

    Article  PubMed  CAS  Google Scholar 

  • Lerat E, Ochman H (2005) Recognizing the pseudogenes in bacterial genomes. Nucleic Acids Res 33:3125–3132

    Article  PubMed  CAS  Google Scholar 

  • Li WH, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Harrison PM, Kunin V et al (2004) Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol 5:R64

    Article  PubMed  Google Scholar 

  • Lu C, Kulkarni K, Souret FF et al (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 16:1276–1288

    Article  PubMed  CAS  Google Scholar 

  • Mighell AJ, Smith NR, Robinson PA et al (2000) Vertebrate pseudogenes. FEBS Lett 468:109–114

    Article  PubMed  CAS  Google Scholar 

  • Nam J, Kim J, Lee S et al (2004) Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc Natl Acad Sci USA 101:1910–1915

    Article  PubMed  CAS  Google Scholar 

  • Nelson DR, Schuler MA, Paquette SM et al (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135:756–772

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Davalos LM (2006) The nature and dynamics of bacterial genomes. Science 311:1730–1733

    Article  PubMed  CAS  Google Scholar 

  • Ogata H, Audic S, Renesto-Audiffren P et al (2001) Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293:2093–2098

    Article  PubMed  CAS  Google Scholar 

  • Ohshima K, Hattori M, Yada T et al (2003) Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates. Genome Biol 4:R74

    Article  PubMed  Google Scholar 

  • Ota T, Nei M (1995) Evolution of immunoglobulin VH pseudogenes in chickens. Mol Biol Evol 12:94–102

    Article  PubMed  CAS  Google Scholar 

  • Parkhill J, Wren BW, Thomson NR et al (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523–527

    Article  PubMed  CAS  Google Scholar 

  • Poliseno L, Salmena L, Zhang J et al (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465:1033–1038

    Article  PubMed  CAS  Google Scholar 

  • Sabot F, Schulman AH (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity 97:381–388

    Article  PubMed  CAS  Google Scholar 

  • Sasidharan R, Gerstein M (2008) Genomics: protein fossils live on as RNA. Nature 453:729–731

    Article  PubMed  CAS  Google Scholar 

  • Svensson O, Arvestad L, Lagergren J (2006) Genome-wide survey for biologically functional pseudogenes. PLoS Comput Biol 2:e46

    Article  PubMed  Google Scholar 

  • Swarbreck D, Wilks C, Lamesch P et al (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014

    Article  PubMed  CAS  Google Scholar 

  • Tam OH, Aravin AA, Stein P et al (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453:534–538

    Article  PubMed  CAS  Google Scholar 

  • Thibaud-Nissen F, Ouyang S, Buell CR (2009) Identification and characterization of pseudogenes in the rice gene complement. BMC Genomics 10:317

    Google Scholar 

  • Torrents D, Suyama M, Zdobnov E et al (2003) A genome-wide survey of human pseudogenes. Genome Res 13:2559–2567

    Article  PubMed  CAS  Google Scholar 

  • Tourmen Y, Baris O, Dessen P et al (2002) Structure and chromosomal distribution of human mitochondrial pseudogenes. Genomics 80:71–77

    Article  PubMed  CAS  Google Scholar 

  • van Baren MJ, Brent MR (2006) Iterative gene prediction and pseudogene removal improves genome annotation. Genome Res 16:678–685

    Article  PubMed  Google Scholar 

  • Vanin EF (1985) Processed pseudogenes – characteristics and evolution. Annu Rev Genet 19:253–272

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Shi X, Hao B et al (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Totoki Y, Toyoda A et al (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453:539–543

    Article  PubMed  CAS  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    Article  PubMed  CAS  Google Scholar 

  • Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12:885–893

    PubMed  CAS  Google Scholar 

  • Yamada K, Lim J, Dale JM et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846

    Article  PubMed  CAS  Google Scholar 

  • Yano Y, Saito R, Yoshida N et al (2004) A new role for expressed pseudogenes as ncRNA: regulation of mRNA stability of its homologous coding gene. J Mol Med 82:414–422

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Wang J, Lin W et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

  • Zhang Z, Gerstein M (2003) Identification and characterization of over 100 mitochondrial ribosomal protein pseudogenes in the human genome. Genomics 81:468–480

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZL, Gerstein M (2004) Large-scale analysis of pseudogenes in the human genome. Curr Opin Genet Dev 14:328–335

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Harrison P, Gerstein M (2002) Identification and analysis of over 2000 ribosomal protein pseudogenes in the human genome. Genome Res 12:1466–1482

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Harrison PM, Liu Y et al (2003) Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res 13:2541–2558

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Carriero N, Gerstein M (2004) Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet 20:62–67

    Article  PubMed  Google Scholar 

  • Zhang Y, Wu Y, Liu Y et al (2005) Computational identification of 69 retroposons in Arabidopsis. Plant Physiol 138:935–948

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Carriero N, Zheng D et al (2006) PseudoPipe: an automated pseudogene identification pipeline. Bioinformatics 22:1437–1439

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZD, Frankish A, Hunt T et al (2010) Identification and analysis of unitary pseudogenes: historic and contemporary gene losses in humans and other primates. Genome Biol 11:R26

    Article  PubMed  Google Scholar 

  • Zheng DY, Gerstein MB (2007) The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they? Trends Genet 23:219–224

    Article  PubMed  CAS  Google Scholar 

  • Zheng D, Zhang Z, Harrison PM et al (2005) Integrated pseudogene annotation for human chromosome 22: evidence for transcription. J Mol Biol 349:27–45

    Article  PubMed  CAS  Google Scholar 

  • Zheng D, Frankish A, Baertsch R et al (2007) Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolution. Genome Res 17:839–851

    Article  PubMed  CAS  Google Scholar 

  • Zou C, Lehti-Shiu MD, Thibaud-Nissen F et al (2009) Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol 151:3–15

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology and Departments of Genetics and Neuroscience, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY, 10461, USA

    Deyou Zheng

  2. Department of Neurology, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY, 10461, USA

    Xingyi Guo

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  1. Xingyi Guo
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  2. Deyou Zheng
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Correspondence to Deyou Zheng .

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Editors and Affiliations

  1. Institute of Chemistry/Biochemistry, Free University Berlin, Thielallee 63, Berlin, 14195, Berlin, Germany

    Volker A. Erdmann

  2. Inst. Bioorganic Chemistry, PAN Poznan, ul. Z. Noskowskiego 12/14, Poznan, 61-704, Poland

    Jan Barciszewski

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Guo, X., Zheng, D. (2011). Regulatory Roles of Novel Small RNAs from Pseudogenes. In: Erdmann, V., Barciszewski, J. (eds) Non Coding RNAs in Plants. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19454-2_12

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