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The Role of Transposable Elements in Pongamia Unigenes and Protein Diversity

Molecular Biotechnology volume 62, pages 31–42 (2020)Cite this article

Abstract

Pongamia pinnata (also called Millettia pinnata), a non-edible oil yielding tree, is well known for its multipurpose benefits and acts as a potential source for medicine and biodiesel preparation. Due to increase in demand for cultivation, understanding of genetic diversity is an important parameter for further breeding and cultivation programme. Transposable elements (TEs) are a major component of plant genome but still, their evolutionary significance in Pongamia remains unexplored. In view to understand the role of TEs in genome diversity, Pongamia unigenes were screened for the presence of TE cassettes. Our analysis showed the presence of all categories of TE cassettes in unigenes with major contribution of long terminal repeat-retrotransposons towards unigene diversity. Interestingly, the insertion of some TEs was also observed in both organellar genomes. The study of insertion of TEs in coding sequence is of great interest as they may be responsible for protein diversity thereby influencing the phenotype. The present investigation confirms the exaptation phenomenon in pyruvate decarboxylase (PDC) gene where the entire exon sequence was derived from Ty3-gypsy like retrotransposon. The study of PDC protein revealed the translation of gypsy element into protein. Furthermore, the phylogenetic study confirmed the diversity in PDC gene due to insertion of the gypsy element, where the PDC genes with and without gypsy insertion were clustered separately.

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References

  1. McClintock, B. (1950). The origin and behavior of mutable loci in maize. Proceedings of the National Academy of Sciences of the USA,6, 344–355.

    Article  Google Scholar 

  2. Baucom, R. S., Estill, J. C., Leebens-Mack, J., & Bennetzen, J. L. (2009). Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Research,2, 243–254.

    Google Scholar 

  3. Kanazawa, A., Liu, B., Kong, F., Arase, S., & Abe, J. (2009). Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. Journal of Molecular Evolution,69, 164–175.

    CAS  Article  Google Scholar 

  4. O’Donnell, K. A., & Burns, K. H. (2010). Mobilizing diversity: Transposable element insertions in genetic variation and disease. Mobile DNA,1, 21.

    Article  Google Scholar 

  5. Chuong, E. B., Elde, N. C., & Feschotte, C. (2017). Regulatory activities of transposable elements: From conflicts to benefits. Nature Reviews Genetics,18, 71–86.

    CAS  Article  Google Scholar 

  6. Almeida, L. M., Silva, I. T., Silva, W. A., Jr., Castro, J. P., Riggs, P. K., Carareto, C. M., et al. (2007). The contribution of transposable elements to Bos taurus gene structure. Gene,390, 180–189.

    CAS  Article  Google Scholar 

  7. Sakai, H., Tanaka, T., & Itoh, T. (2007). Birth and death of genes promoted by transposable elements in Oryza sativa. Gene,392, 59–63.

    CAS  Article  Google Scholar 

  8. Brosius, J., & Gould, S. J. (1992). On “genomenclature”: A comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proceedings of the National academy of Sciences of the United States of America,89, 10706.

    CAS  Article  Google Scholar 

  9. Lopes, F. R., Carazzolle, M. F., Pereira, G. A., Colombo, C. A., & Carareto, C. M. (2008). Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants. Molecular Genetics and Genomics,279, 385–401.

    Article  Google Scholar 

  10. Kawase, M., Fukunaga, K., & Kato, K. (2005). Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Molecular Genetics and Genomics,274, 131–140.

    CAS  Article  Google Scholar 

  11. Magalhaes, J. V., Liu, J., Guimaraes, C. T., Lana, U. G., et al. (2007). A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in Sorghum. Nature Genetics,39, 1156–1161.

    CAS  Article  Google Scholar 

  12. Hisano, H., Tsujimura, M., Yoshida, H., Terachi, T., & Sato, K. (2016). Mitochondrial genome sequences from wild and cultivated barley (Hordeum vulgare). BMC Genomics,17, 824.

    Article  Google Scholar 

  13. Shelke, R. G., & Rangan, L. (2019). Isolation and characterisation of Ty1-copia retrotransposons from Pongamia pinnata. Trees—Structure and Function. https://doi.org/10.1007/s0046.

    Article  Google Scholar 

  14. Kesari, V., Madurai Sathyanarayana, V., Parida, A., & Rangan, L. (2010). Molecular marker-based characterization in candidate plus trees of Pongamia pinnata, a potential biodiesel legume. AoB Plants. https://doi.org/10.1093/aobpla/plq017.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Huang, J., Lu, X., Yan, H., Chen, S., Zhang, W., Huang, R., et al. (2012). Transcriptome characterization and sequencing-based identification of salt-responsive genes in Millettia pinnata, a semi-mangrove plant. DNA Research,19, 195–207.

    CAS  Article  Google Scholar 

  16. Huang, J., Guo, X., Hao, X., Zhang, W., Chen, S., Huang, R., et al. (2016). De novo sequencing and characterization of seed transcriptome of the tree legume Millettia pinnata for gene discovery and SSR marker development. Molecular Breeding,36, 75.

    Article  Google Scholar 

  17. Kazakoff, S. H., Imelfort, M., Edwards, D., Koehorst, J., Biswas, B., Batley, J., et al. (2012). Capturing the biofuel wellhead and powerhouse: The chloroplast and mitochondrial genomes of the leguminous feedstock tree Pongamia pinnata. PLoS ONE,7, e51687.

    CAS  Article  Google Scholar 

  18. Pohlman, R. F., Fedoroff, N. V., & Messing, J. (1984). The nucleotide sequence of the maize controlling element Activator. Cell,37, 635–643.

    CAS  Article  Google Scholar 

  19. Schnable, P. S., Ware, D., Thane, T., et al. (2009). The B73 maize genome: Complexity, diversity, and dynamics. Science,326, 1112–1115.

    CAS  Article  Google Scholar 

  20. Ganko, E. W., Bhattacharjee, V., Schliekelman, P., & Mcdonald, J. F. (2003). Evidence for the contribution of LTR retrotransposon to C. elegans gene evolution. Molecular Biolology and Evolution,20, 1925–1931.

    CAS  Article  Google Scholar 

  21. Debarry, J. D., Ganko, E. W., Mccarthy, E. M., & Mcdonald, J. F. (2006). The contribution of LTR retrotransposon sequences to gene evolution in Mus musculus. Molecular Biology and Evolution,23, 479–481.

    CAS  Article  Google Scholar 

  22. Ma, J., Devos, K. M., & Bennetzen, J. L. (2004). Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Research,14, 860–869.

    CAS  Article  Google Scholar 

  23. Lopes, F. R., Jjingo, D., Da Silva, C. R., Andrade, A. C., Marraccini, P., Teixeira, J. B., et al. (2013). Transcriptional activity, chromosomal distribution and expression effects of transposable elements in Coffea genomes. PLoS ONE,8, e78931.

    CAS  Article  Google Scholar 

  24. Van De Lagemaat, L. N., Landry, J. R., Mager, D. L., & Medstrand, P. (2003). Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genetics,19, 530–536.

    Article  Google Scholar 

  25. Lorenc, A., & Makalowski, W. (2003). Transposable elements and vertebrate protein diversity. Genetica,118, 183–189.

    CAS  Article  Google Scholar 

  26. Orgel, L. E., & Crick, F. H. (1980). Selfesh DNA: The ultimate parasite. Nature,284, 604–607.

    CAS  Article  Google Scholar 

  27. Nekrutenko, A., & Li, W. H. S. (2001). Transposable elements are found in a large number of human protein-coding genes. Trends in Genetics,17, 619–621.

    CAS  Article  Google Scholar 

  28. Makałowski, W., Kischka, T., & Makałowska, I. (2017). Contribution of transposable elements to human proteins. eLS. https://doi.org/10.1002/9780470015902.a0020793.pub2.

    Article  Google Scholar 

  29. Nuzhdin, S. V. (1999). Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica,107, 129–137.

    CAS  Article  Google Scholar 

  30. Gotea, V., & Makalowski, W. (2006). Do transposable elements really contribute to proteomes? Trends in Genetics,22, 260–267.

    CAS  Article  Google Scholar 

  31. Hossain, M. A., Huq, E., Grover, A., Dennis, E. S., Peacock, W. J., & Hodges, T. K. (1996). Characterization of pyruvate decarboxylase genes from rice. Plant Molecular Biology,31, 761–770.

    CAS  Article  Google Scholar 

  32. Talarico, L. A., Ingram, L. O., & Maupin-Furlow, J. A. (2001). Production of the gram-positive Sarcina ventriculi pyruvate decarboxylase in Escherichia coli. Microbiology,147, 2425–2435.

    CAS  Article  Google Scholar 

  33. Ohno, S. (1970). Evolution by gene duplication. London: George Alien & Unwin Ltd.

    Book  Google Scholar 

  34. Robins, D. M., & Samuelson, L. C. (1992). Retrotransposons and the evolution of mammalian gene expression. Genetica,86, 191–201.

    CAS  Article  Google Scholar 

  35. Kursteiner, O., Dupuis, I., & Kuhlemeier, C. (2003). The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiology,132, 968–978.

    Article  Google Scholar 

  36. Mithran, M., Paparelli, E., Novi, G., Perata, P., & Loreti, E. (2014). Analysis of the role of the pyruvate decarboxylase gene family in Arabidopsis thaliana under low-oxygen conditions. Plant Biology,16, 28–34.

    CAS  Article  Google Scholar 

  37. Cavrak, V. V., Lettner, N., Jamge, S., Kosarewicz, A., Bayer, L. M., & Scheid, O. M. (2014). How a retrotransposon exploits the plant’s heat stress response for its activation. PLoS Genetics,10, e1004115.

    Article  Google Scholar 

  38. Ito, H., Kim, J. M., Matsunaga, W., Saze, H., Matsui, A., Endo, T., et al. (2016). A stress-activated transposon in Arabidopsis induces transgenerational abscisic acid insensitivity. Scientific Reports,6, 23181.

    CAS  Article  Google Scholar 

  39. Negi, P., Rai, A. N., & Suprasanna, P. (2016). Moving through the stressed genome: Emerging regulatory roles for transposons in plant stress response. Frontiers in Plant Science,7, 1448.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank MHRD and IIT Guwahati, India for providing fellowship and computational facilities.

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  1. Applied Biodiversity Laboratory, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Assam, 781 039, India

    Rahul G. Shelke & Latha Rangan

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  1. Rahul G. Shelke
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Correspondence to Latha Rangan.

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Shelke, R.G., Rangan, L. The Role of Transposable Elements in Pongamia Unigenes and Protein Diversity. Mol Biotechnol 62, 31–42 (2020). https://doi.org/10.1007/s12033-019-00223-0

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Keywords

  • Pongamia pinnata
  • Pyruvate decarboxylase
  • Transposable elements
  • Ty3-gypsy
  • Unigene