Journal of Biosciences

, Volume 38, Issue 4, pp 727–732 | Cite as

Characterization of pseudogenes in members of the order Frankineae

  • Saubashya SurEmail author
  • Sangita Saha
  • Louis S Tisa
  • Asim K Bothra
  • Arnab Sen


Pseudogenes are defined as non-functional relatives of genes whose protein-coding abilities are lost and are no longer expressed within cells. They are an outcome of accumulation of mutations within a gene whose end product is not essential for survival. Proper investigation of the procedure of pseudogenization is relevant for estimating occurrence of duplications in genomes. Frankineae houses an interesting group of microorganisms, carving a niche in the microbial world. This study was undertaken with the objective of determining the abundance of pseudogenes, understanding strength of purifying selection, investigating evidence of pseudogene expression, and analysing their molecular nature, their origin, evolution and deterioration patterns amongst domain families. Investigation revealed the occurrence of 956 core pFAM families sharing common characteristics indicating co-evolution. WD40, Rve_3, DDE_Tnp_IS240 and phage integrase core domains are larger families, having more pseudogenes, signifying a probability of harmful foreign genes being disabled within transposable elements. High selective pressure depicted that gene families rapidly duplicating and evolving undoubtedly facilitated creation of a number of pseudogenes in Frankineae. Codon usage analysis between protein-coding genes and pseudogenes indicated a wide degree of variation with respect to different factors. Moreover, the majority of pseudogenes were under the effect of purifying selection. Frankineae pseudogenes were under stronger selective constraints, indicating that they were functional for a very long time and became pseudogenes abruptly. The origin and deterioration of pseudogenes has been attributed to selection and mutational pressure acting upon sequences for adapting to stressed soil environments.


Duplications Frankia pseudogenes transposable elements 



The authors thank the Bioinformatics Division of the Department of Biotechnology (DBT), India, for providing financial assistance in setting up Bioinformatics Facility in the University of North Bengal. SS acknowledges DBT for providing fellowship. The work is partially funded by UGC project on Frankia awarded to AS. AS also acknowledges the receipt of DBT-CREST award.

Supplementary material

12038_2013_9356_MOESM1_ESM.pdf (168 kb)
ESM 1 (PDF 168 kb)


  1. Andersson JO and Andersson SG 2001 Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol. Biol. Evol. 18 829–839PubMedCrossRefGoogle Scholar
  2. Beauchemin N, Gtari M, Ghodhbane-Gtari F, Furnholm T, Sen A, Wall L, Tavares F, et al. 2012 What can the genome of an infective ineffective (Fix-) Frankia. Strain (EuI1c) that is able to form nodules with its host plant tell us about actinorhizal symbiosis and Frankia evolution. The 112th General Meeting of the American Society for Microbiology American Society for Microbiology, San Francisco, CAGoogle Scholar
  3. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL and Sonnhammer ELL 2000 The Pfam protein families database. Nucleic Acids Res. 28 263–266PubMedCrossRefGoogle Scholar
  4. Bickhart DM, Gogarten JP, Lapierre P, Tisa LS, Normand P and Benson DR 2009 Insertion sequence content reflects genome plasticity in strains of the root nodule actinobacterium Frankia. BMC Genomics 10 468Google Scholar
  5. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, et al. 2000 Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat. Biotechnol. 18 630–634PubMedCrossRefGoogle Scholar
  6. DasSarma S 1993 Identification and analysis of the gas vesicle gene cluster on an unstable plasmid of Halobacterium halobium. Experientia 49 482–486PubMedCrossRefGoogle Scholar
  7. Didelot X, Urwin R, Maiden MCJ and Falush D 2009 Genealogical typing of Neisseria meningitides. Microbiology 155 3176–3186PubMedCrossRefGoogle Scholar
  8. Ghodhbane-Gtari F, Beauchemin N, Bruce D, Chain P, Chen A, Walston Davenport K, Deshpande S, et al. 2013. Draft Genome sequence of Frankia sp. strain CN3, an atypical, non-infective (Nod-) ineffective (Fix-) isolate from Coriaria nepalensis. Genome Announc. 1 00085–00013Google Scholar
  9. Fuxelius HH, Darby AC, Cho NH and Andersson SGE 2008 Visualization of pseudogenes in intracellular bacteria reveals the different tracks to gene destruction. Genome Biol. 9 R42PubMedCrossRefGoogle Scholar
  10. Lawrence JG and Ochman H 1997 Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44 383–387PubMedCrossRefGoogle Scholar
  11. Lawrence JG and Ochman H 1998 Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. USA 95 9413–9417PubMedCrossRefGoogle Scholar
  12. Lerat E and Ochman H 2005 Recognizing pseudogenes in bacterial genomes. Nucleic Acids Res. 33 3125–3132PubMedCrossRefGoogle Scholar
  13. Liu Y, Harrison PM, Kunin V and Gerstein M 2004 Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol. 5 R64PubMedCrossRefGoogle Scholar
  14. Markowitz VM, Ivanova N, Palaniappan K, Szeto E and Korzeniewski, et al. 2006 An experimental metagenome data management and analysis system. Bioinformatics 22 e359–e367Google Scholar
  15. Mockler TC, Chan S, Sundaresan A, Chen H, Jacobsen SE and Ecker JR 2005 Applications of DNA tiling arrays for whole-genome analysis. Genomics 85 1–15PubMedCrossRefGoogle Scholar
  16. Normand P, Queiroux C, Tisa LS, Benson DR, Rouy Z, Cruveiller S and Medigue C 2007 Exploring the genomes of Frankia. Physiol. Plantarum 130 331–343CrossRefGoogle Scholar
  17. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, et al. 2007 Genome characteristics of facultatively symbiotic Frankia sp strains reflect host range and host plant biogeography. Genome Res. 17 7–15PubMedCrossRefGoogle Scholar
  18. Peden J 1999 Analysis of codon usage. PhD Thesis, University of Nottingham, United KingdomGoogle Scholar
  19. Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, et al. 2011. Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J. Bacteriol. 193 7017–7018PubMedCrossRefGoogle Scholar
  20. Petrov DA and Hartl DL 2000 Pseudogene evolution and natural selection for a compact genome. J. Hered. 91 221–227PubMedCrossRefGoogle Scholar
  21. Sakai H, Koyanagi KO, Imanishi T, Itoh T and Gojobori T 2007 Frequent emergence and functional resurrection of processed pseudogenes in the human and mouse genomes. Gene 389 196–203PubMedCrossRefGoogle Scholar
  22. Santos CL, Vieira J, Tavares F, Benson DR, Tisa LS, Berry AM, Moradas-Ferreira P and Normand P 2008 On the nature of FUR evolution: Phylogenetic trends in actinobacteria. BMC Evol. Biol. 8 185PubMedCrossRefGoogle Scholar
  23. Sen A, Sur S, Bothra AK, Benson DR, Normand P and Tisa LS 2008 The implication of lifestyle on codon usage patterns and predicted highly expressed genes for three Frankia genomes. Anton. van Leewen. 93 335–346CrossRefGoogle Scholar
  24. Sen A, Beauchemin N, Bruce D, Chain P, Chen A, Walston Davenport K, Deshpande S, Detter C, et al. 2013 Draft genome sequence of Frankia sp. strain QA3, a nitrogen-fixing actinobacterium isolated from the root nodule of Alnus nitida. Genome Announc. 1 e00103–e00113Google Scholar
  25. Stackbrandt E, Rainey FA and Ward-Rainey NL 1997 Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int. J. Syst. Bacteriol. 47 479–491CrossRefGoogle Scholar
  26. Sur S, Bothra AK, Bajwa M, Tisa LS and Sen A 2008 In silico analysis of Chlorobium geomes divulge insights into the lifestyle of the bacteria. Res. J. Microbiol. 3 600–613CrossRefGoogle Scholar
  27. Torrents D, Suyama M, Zdobnov E and Bork P 2003 A genome-wide survey of human pseudogenes. Genome Res. 13 2559–2567PubMedCrossRefGoogle Scholar
  28. Wu G, Culley DE and Zhang W 2005 Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151 2175–87PubMedCrossRefGoogle Scholar
  29. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK and Yu J 2006 KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom. Proteom. Bioinform. 4 259–263CrossRefGoogle Scholar
  30. Zou C, Lehti-Shiu MD, Thibaud-Nissen F, Prakash T, Buell CR and Shiu SH 2009 Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol. 151 3–15PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2013

Authors and Affiliations

  • Saubashya Sur
    • 1
    Email author
  • Sangita Saha
    • 1
  • Louis S Tisa
    • 2
  • Asim K Bothra
    • 3
  • Arnab Sen
    • 1
  1. 1.Bioinformatics Facility, Department of BotanyUniversity of North BengalSiliguriIndia
  2. 2.Department of Molecular, Cellular, & Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.Raiganj University CollegeRaiganjIndia

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