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Plant Systematics and Evolution

, Volume 304, Issue 4, pp 521–533 | Cite as

An insight into the evolution of introns in the gyrase A gene of plants

  • Mrinalini Manna
  • Dhirendra Fartyal
  • V. Mohan M. Achary
  • Aakrati Agarwal
  • Malireddy K. Reddy
Original Article
  • 79 Downloads

Abstract

DNA gyrase is a type II topoisomerase essential for replication and transcription in prokaryotes and eukaryotic cell organelles. The functional gyrase enzyme is an A2B2 tetramer encoded by the gyrA and gyrB genes. Most of the eukaryotic gyrase A genes possess introns while they are intron-less in prokaryotes. In the present study, we found out the evolutionary passage of intron development in gyrase A gene with the help of bioinformatics approaches. All the plant gyrase A genes studied by us were found to be a part of the nuclear genome, and their respective proteins were targeted to the organelles. Except the green alga Bathycoccus prasinos, these genes contained introns, and the positions of the homologous introns were found to be highly conserved in diverse plant lineages despite having variation in their nucleotide sequence compositions and lengths. However, in red, brown, and green algae: Chlorella variabilis and Chlamydomonas reinhardtii, homologous intron positions were not conserved, which might be due to the independent acquisition of introns. The study makes it amply evident that the introns appeared in the gene following endosymbiotic gene transfer of the gyrase A to the nuclear genome of an ancestral green plant. The land plants appear to have acquired intron-bearing gyrase A gene from a common ancestral green algae and subsequently lesser re-arrangement of introns at homologous positions resulted in their positional conservation. However, the introns which are known to be under lesser selection pressure evolved differently in various plant species in terms of base composition and lengths.

Keywords

Endosymbiosis Gyrase A Introns Introns early model Introns late model 

Notes

Acknowledgements

The authors are grateful to the International Centre for Genetic Engineering and Biotechnology (ICGEB), New Delhi, for providing infrastructure facilities. MM, DF, VMMA, and AA convey special thanks to MKR for conceiving the idea and providing necessary guidance. MM and AA were supported by Senior Research Fellowships of Council of Scientific and Industrial Research (CSIR), New Delhi, DF was supported by INSPIRE Fellowship of Department of Science and Technology, India, and VMMA was supported by fellowship of Department of Biotechnology (DBT), New Delhi.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical statement

Authors comply with all rules of the journal following the COPE guidelines; all authors have contributed to and approved the final manuscript.

Supplementary material

606_2018_1503_MOESM1_ESM.pdf (352 kb)
Supplementary material 1 (PDF 352 kb)
606_2018_1503_MOESM2_ESM.pdf (273 kb)
Supplementary material 2 (PDF 273 kb)

References

  1. Ahmadinejad N, Dagan T, Gruenheit N, Martin W, Gabaldon T (2010) Evolution of spliceosomal introns following endosymbiotic gene transfer. BMC Evol Biol 10:57.  https://doi.org/10.1186/1471-2148-10-57 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Blake CC (1985) Exons and the evolution of proteins. Int Rev Cytol 93:149–185CrossRefPubMedGoogle Scholar
  3. Cech TR (1986) The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44:207–210.  https://doi.org/10.1016/0092-8674(86)90751-8 CrossRefPubMedGoogle Scholar
  4. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annual Rev Biochem 70:369–413.  https://doi.org/10.1146/annurev.biochem.70.1.369 CrossRefGoogle Scholar
  5. Coates JC, E-Aiman U, Charrier B (2015) Understanding “green” multicellularity: do seaweeds hold the key? Frontiers Pl Sci 5:737.  https://doi.org/10.3389/fpls.2014.00737 Google Scholar
  6. Cozzarelli NR (1980) DNA gyrase and the supercoiling of DNA. Science 207:953–960.  https://doi.org/10.1126/science.6243420 CrossRefPubMedGoogle Scholar
  7. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: Robust phylogenetic analysis for the non-specialist. Nucl Acids Res 36 (Web Server issue): W465–W469.  https://doi.org/10.1093/nar/gkn180 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Doolittle WF, Stoltzfus A (1993) Molecular evolution. Genes-in-pieces revisited. Nature 361:403.  https://doi.org/10.1038/361403a0 CrossRefPubMedGoogle Scholar
  9. Drlica K, Snyder M (1978) Superhelical Escherichia coli DNA: relaxation by coumermycin. J Molec Biol 120:145–154.  https://doi.org/10.1016/0022-2836(78)90061-X CrossRefPubMedGoogle Scholar
  10. Elo A, Lyznik A, Gonzalez DO, Kachman SD, Mackenzie SA (2003) Nuclear genes that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Pl Cell 15:1619–1631.  https://doi.org/10.1105/tpc.010009 CrossRefGoogle Scholar
  11. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Molec Biol 300:1005–1016.  https://doi.org/10.1006/jmbi.2000.3903 CrossRefPubMedGoogle Scholar
  12. Gellert M (1981) DNA topoisomerases. Annual Rev Biochem 50:879–910.  https://doi.org/10.1146/annurev.bi.50.070181.004311 CrossRefGoogle Scholar
  13. Gilbert W (1978) Why genes in pieces? Nature 271:501.  https://doi.org/10.1038/271501a0 CrossRefPubMedGoogle Scholar
  14. Gilbert W (1987) The exon theory of genes. Cold Spring Harb Symp Quant Biol 52:901–905CrossRefPubMedGoogle Scholar
  15. Gilbert W, Glynias M (1993) On the ancient nature of introns. Gene 135:137–144CrossRefPubMedGoogle Scholar
  16. Grabowski PJ, Seiler SR, Shrap PA (1985) A multicomponent complex is involved in splicing of messenger RNA precursors. Cell 42:345–353.  https://doi.org/10.1016/S0092-8674(85)80130-6 CrossRefPubMedGoogle Scholar
  17. Hardison RC (2012) Evolution of haemoglobin and its genes. Cold Spring Harb Prospect Med 2:a011627.  https://doi.org/10.1101/cshperspect.a011627 Google Scholar
  18. Heinhorst S, Cannon GC, Weissbach A (1985) Chloroplast DNA synthesis during the cell cycle in cultured cells of Nicotianatabacum: inhibition by nalidixic acid and hydroxyurea. Arch Biochem Biophys 239:475–479CrossRefGoogle Scholar
  19. Holland SK, Blake CC (1987) Proteins, exons and molecular evolution. Biosystems 20:181–206.  https://doi.org/10.1016/0303-2647(87)90044-X CrossRefPubMedGoogle Scholar
  20. Kolkman JA, Stemmer WP (2001) Directed evolution of proteins by exon shuffling. Nat Biotechnol 19:423–428CrossRefGoogle Scholar
  21. Krebs JE, Goldstein ES, Kilpatrick ST (2013) Lewin’s genes XI. Jones & Bartlett Pibl, SudburyGoogle Scholar
  22. Langkjaer RB, Casaregola S, Ussery QW, Gaillardin C, Pislkur J (2003) Sequence analysis of three mitochondrial DNA molecules reveals interesting differences among Saccharomyces yeasts. Nucl Acids Res 31:3081–3091CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lowe T, Chan P (2011) Genomic tRNA database. Available at: http://lowelab.ucsc.edu/tRNAscan-SE/
  24. Martin W, Harrmann RG (1998) Gene transfer from Organelle to the Nucleus: how Much, What Happens, and Why? Pl Physiol 118:9–17.  https://doi.org/10.1104/pp.118.1.9 CrossRefGoogle Scholar
  25. Mattick JS (1994) Introns: evolution and function. Curr Opin Genet Developm 4:823–831CrossRefGoogle Scholar
  26. Moore MJ, Sharp PA (1993) Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 365:364–368.  https://doi.org/10.1038/365364a0 CrossRefPubMedGoogle Scholar
  27. Morello L, Breviario D (2008) Plant spliceosomal introns: not only cut and paste. Curr Genomics 9:227–238.  https://doi.org/10.2174/138920208784533629 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nilsen TW (2003) The spliceosome: the most complex macromolecular machine in the cell? BioEssays 25:1147–1149.  https://doi.org/10.1002/bies.10394 CrossRefPubMedGoogle Scholar
  29. Ovcharenko I, Loots GG, Hardison RC, Miller W, Stubbs L (2004) zPicture: dynamic alignment and visualization tool for analyzing conservation profiles. Genome Res 14: 472–477.  https://doi.org/10.1101/gr.2129504 Google Scholar
  30. Patthy L (1991) Exons–original building blocks of proteins? BioEssays 13:187–192CrossRefPubMedGoogle Scholar
  31. Patthy L (1999) Genome evolution and the evolution of exon-shuffling–a review. Gene 238:103–144CrossRefPubMedGoogle Scholar
  32. Plant AL, Gray JC (1988) Introns in chloroplast protein-coding genes of land plants. Photosynthesis Res 16:23–39.  https://doi.org/10.1007/BF00039484 CrossRefPubMedGoogle Scholar
  33. Rogozin IB, Carmel L, Csuros M, Koonin EV (2012) Origin and evolution of spliceosomal introns. Biol Direct 7:11.  https://doi.org/10.1186/1745-6150-7-11 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Roy SW (2003) Recent evidence for the exon theory of genes. Genetica 118:251–266CrossRefGoogle Scholar
  35. Shaw AJ, Szövényi P, Shaw B (2011) Bryophyte diversity and evolution: windows into the early evolution of land plants. Amer J Bot 98:352–369.  https://doi.org/10.3732/ajb.1000316 CrossRefGoogle Scholar
  36. Sheveleva EV, Hallick RB (2004) Recent horizontal intron transfer to a chloroplast genome. Nucl Acids Res 32:803–810.  https://doi.org/10.1093/nar/gkh225 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Stoltzfus A, Spencer DF, Zuker M, Logsdon JMJ, Doolittle WF (1994) Testing the exon theory of genes: the evidence from protein structure. Science 265:202–207. http://www.jstor.org/stable/2884169
  38. Taanman JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1401:103–123.  https://doi.org/10.1016/S0005-2728(98)00161-3 CrossRefGoogle Scholar
  39. Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Molec Biol Evol 23:1324–1338.  https://doi.org/10.1093/molbev/msk018 CrossRefPubMedGoogle Scholar
  40. Wall MK, Mitchenall LA, Maxwell A (2004) Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc Natl Acad Sci USA 101:7821–7826.  https://doi.org/10.1073/pnas.0400836101 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wang JC (1996) DNA topoisomerases. Annual Rev Biochem 65:635–692.  https://doi.org/10.1146/annurev.bi.65.070196.003223 CrossRefGoogle Scholar
  42. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216.  https://doi.org/10.1016/S0074-7696(08)62066-5 CrossRefPubMedGoogle Scholar
  43. Yoshihisa T (2014) Handling tRNA introns, archaeal way and eukaryotic way. Frontiers Genet 5:213.  https://doi.org/10.3389/fgene.2014.00213 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Mrinalini Manna
    • 1
  • Dhirendra Fartyal
    • 1
    • 2
  • V. Mohan M. Achary
    • 1
  • Aakrati Agarwal
    • 1
    • 3
  • Malireddy K. Reddy
    • 1
  1. 1.Crop Improvement GroupInternational Centre for Genetic Engineering and BiotechnologyNew DelhiIndia
  2. 2.Uttarakhand Technical UniversityDehradunIndia
  3. 3.Plant Molecular Biology Lab, Department of BotanyUniversity of DelhiNew DelhiIndia

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