Skip to main content
Log in

Intron gain, a dominant evolutionary process supporting high levels of gene expression in rice

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Presence of introns in eukaryotic genes, their evolution and biological function has been a subject of considerable debate ever since their discovery in 1977. To understand the effect of number of introns on the structural and functional characteristics of rice genes, we carried out whole genome analysis of the relationship of the number of introns per gene with predicted cDNA sequence (CDS) length, average exon length and gene expression patterns. There was a direct correlation between the number of introns and the average CDS length among the expressed rice genes, as determined by expressed sequence tags (EST) support. The percentage of expressed genes in groups of rice genes representing different intron numbers showed a significant positive correlation with the number of introns providing evidence for higher level of expression for intron-rich genes. This was further supported by higher abundance of ESTs for the intron-rich genes in the rice EST database. Higher number of introns may be providing post-transcriptional stability to the mRNA leading to higher expression levels. Here we first report the detailed genome wide analysis of distribution pattern of introns in rice that provides important insight in to understanding the evolution, structure and expression of genes in plant species. Particularly, the complex gene structure and functional advantage of the intron containing genes supports the gain of intron theory for the evolution of eukaryotic genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

CDS:

Coding DNA sequence

EST:

Expressed sequence tags

References

  • Aparicio S, Chapman J, Stupka E, Putnam N, Chia J-M, Dehal P, Christoffels A, Rash S, Hoon S, Smit A (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297(5585):1301–1310

    Article  CAS  PubMed  Google Scholar 

  • Betrán E, Thornton K, Long M (2002) Retroposed new genes out of the X in Drosophila. Genome Res 12(12):1854–1859

    Article  PubMed  PubMed Central  Google Scholar 

  • Carola M, Finer JJ (2015) The intron and 5′ distal region of the soybean Gmubi promoter contribute to very high levels of gene expression in transiently and stably transformed tissues. Plant Cell Rep 34(1):111–120

    Article  Google Scholar 

  • Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83(4–5):303–315

    Article  CAS  PubMed  Google Scholar 

  • Edgell DR, Belfort M, Shub DA (2000) Barriers to intron promiscuity in bacteria. J Bacteriol 182(19):5281–5289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert W (1987) The exon theory of genes. In: Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, pp 901–905

  • Gilbert W, De Souza SJ, Long M (1997) Origin of genes. Proc Natl Acad Sci 94(15):7698–7703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu K (2006) Intron exclusion and the mystery of intron loss. FEBS Lett 580(27):6361–6365

    Article  CAS  PubMed  Google Scholar 

  • Jeffares DC, Mourier T, Penny D (2006) The biology of intron gain and loss. Trends Genet 22(1):16–22

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301(5631):376–379

    Article  PubMed  Google Scholar 

  • Li W, Zhang P, Fellers JP, Friebe B, Gill BS (2004) Sequence composition, organization, and evolution of the core Triticeae genome. Plant J 40(4):500–511

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Zhu W, Silva JC, Gu X, Buell CR (2006) Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 7(5):R41

    Article  PubMed  PubMed Central  Google Scholar 

  • Llopart A, Comeron JM, Brunet FG, Lachaise D, Long M (2002) Intron presence–absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci 99(12):8121–8126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307(5713):1321–1324

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401–1404

    Article  CAS  PubMed  Google Scholar 

  • Marais G, Piganeau G (2002) Hill-Robertson interference is a minor determinant of variations in codon bias across Drosophila melanogaster and Caenorhabditis elegans genomes. Mol Biol Evol 19(9):1399–1406

    Article  CAS  PubMed  Google Scholar 

  • Morita S, Tsukamoto S, Sakamoto A, Makino H, Nakauji E, Kaminaka H, Masumura T, Ogihara Y, Satoh S, Tanaka K (2012) Differences in intron-mediated enhancement of gene expression by the first intron of cytosolic superoxide dismutase gene from rice in monocot and dicot plants. Plant Biotechnol 29(1):115–119

    Article  CAS  Google Scholar 

  • Nixon JE, Wang A, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J (2002) A spliceosomal intron in Giardia lamblia. Proc Natl Acad Sci 99(6):3701–3705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patil G, Nicander B (2013) Identification of two additional members of the tRNA isopentenyltransferase family in Physcomitrella patens. Plant Mol Biol 82(4–5):417–426

    Article  CAS  PubMed  Google Scholar 

  • Patil G, Kumar V, Sharma P, Deokar A, Kondawar V, Jain PK, Srinivasan R Promoter Element of an ERF Gene of Arabidopsis Drives Trichome-Specific Expression and Retains Its Specificity in Brassica juncea. In: In vitro cellular & developmental biology-animal, 2010. Springer 233 Spring ST, New York, NY 10013 USA, pp S153-S154

  • Ren X-Y, Vorst O, Fiers MW, Stiekema WJ, Nap J-P (2006) In plants, highly expressed genes are the least compact. Trends Genet 22(10):528–532

    Article  CAS  PubMed  Google Scholar 

  • Roy SW, Gilbert W (2005) Rates of intron loss and gain: implications for early eukaryotic evolution. Proc Natl Acad Sci U S A 102(16):5773–5778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy SW, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7(3):211–221

    PubMed  Google Scholar 

  • Rzhetsky A, Ayala F (1999) The enigma of intron origins. Cell Mol Life Sci 55(1):3–6

    Article  CAS  Google Scholar 

  • Sanderson MJ, Thorne JL, Wikström N, Bremer K (2004) Molecular evidence on plant divergence times. Am J Bot 91(10):1656–1665

    Article  CAS  PubMed  Google Scholar 

  • Sanmiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82(suppl 1):37–44

    Article  CAS  Google Scholar 

  • Urrutia AO, Hurst LD (2003) The signature of selection mediated by expression on human genes. Genome Res 13(10):2260–2264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinogradov AE (2005) Genome size and chromatin condensation in vertebrates. Chromosoma 113(7):362–369

    Article  PubMed  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon–intron structure. Proc Natl Acad Sci 109(4):1187–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Authors are thankful to Dr. Swarup K. Parida (NIPGR, New Delhi, India) and Dr. Amit A. Deokar (University of Saskatchewan, Canada) for valuable input for data analysis

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Rupesh K. Deshmukh or Nagendra K. Singh.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 106 kb)

ESM 2

(PDF 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deshmukh, R.K., Sonah, H. & Singh, N.K. Intron gain, a dominant evolutionary process supporting high levels of gene expression in rice. J. Plant Biochem. Biotechnol. 25, 142–146 (2016). https://doi.org/10.1007/s13562-015-0319-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-015-0319-5

Keywords

Navigation