Module-intron correlation and intron sliding in family F/10 xylanase genes - PubMed

Module-intron correlation and intron sliding in family F/10 xylanase genes

Y Sato et al. Gene. 1999.

Abstract

Xylanases are classified into two families, numbered F/10 and G/11 according to the similarity of amino acid sequences of their catalytic domain (Henrissat, B., Bairoch, A., 1993. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788). Three-dimensional structure of the catalytic domain of the family F/10 xylanase was reported (White, A., Withers, S.G., Gilkes, N.R., Rose, D.R., 1994. Crystal structure of the catalytic domain of the beta-1,4-glycanase Cex from Cellulomonas fimi. Biochemistry 33, 12546-12552). The domain was decomposed into 22 modules by centripetal profiles (Go, M., Nosaka, M., 1987. Protein architecture and the origin of introns. Cold Spring Harbor Symp. Quant. Biol. 52, 915-924; Noguti, T., Sakakibara, H., Go, M., 1993. Localization of hydrogen-bonds within modules in barnase. Proteins 16, 357-363). A module is a contiguous polypeptide segment of amino acid residues having a compact conformation within a globular domain. Collected 31 intron sites of the family F/10 xylanase genes from fungus were found to be correlated to module boundaries with considerable statistical force (p values <0.001). The relationship between the intron locations and protein structures provides supporting evidence for the ancient origin of introns, because such a relationship cannot be expected by random insertion of introns into eukaryotic genes, but it rather suggests pre-existence of introns in the ancestral genes of prokaryotes and eukaryotes. A phylogenetic tree of the fungal and bacterial xylanase sequences made two clusters; one includes both the bacterial and fungal genes, but the other consists of only fungal genes. The mixed cluster of bacterial genes without introns and the fungal genes with introns further supports the ancient origin of introns. Comparison of the conserved base sequences of introns indicates that sliding of a splice site occurred in Aspergillus kawachii gene by one base from the ancestral position. Substrate-binding sites of xylanase are localized on eight modules, and introns are found at both termini of six out of these functional modules. This result suggests that introns might play a functional role in shuffling the exons encoding the substrate-binding modules.

Similar articles

• An investigation of the nature and function of module 10 in a family F/10 xylanase FXYN of Streptomyces olivaceoviridis E-86 by module shuffling with the Cex of Cellulomonas fimi and by site-directed mutagenesis.

  Kaneko S, Kuno A, Fujimoto Z, Shimizu D, Machida S, Sato Y, Yura K, Go M, Mizuno H, Taira K, Kusakabe I, Hayashi K. Kaneko S, et al. FEBS Lett. 1999 Oct 22;460(1):61-6. doi: 10.1016/s0014-5793(99)01318-6. FEBS Lett. 1999. PMID: 10571062

• Centripetal modules and ancient introns.

  Roy SW, Nosaka M, de Souza SJ, Gilbert W. Roy SW, et al. Gene. 1999 Sep 30;238(1):85-91. doi: 10.1016/s0378-1119(99)00292-9. Gene. 1999. PMID: 10570987

• Module shuffling of a family F/10 xylanase: replacement of modules M4 and M5 of the FXYN of Streptomyces olivaceoviridis E-86 with those of the Cex of Cellulomonas fimi.

  Kaneko S, Iwamatsu S, Kuno A, Fujimoto Z, Sato Y, Yura K, Go M, Mizuno H, Taira K, Hasegawa T, Kusakabe I, Hayashi K. Kaneko S, et al. Protein Eng. 2000 Dec;13(12):873-9. doi: 10.1093/protein/13.12.873. Protein Eng. 2000. PMID: 11239087

• Protein structures and split genes.

  Go M. Go M. Adv Biophys. 1985;19:91-131. doi: 10.1016/0065-227x(85)90052-8. Adv Biophys. 1985. PMID: 3915183 Review.

• Structure and function analysis of Pseudomonas plant cell wall hydrolases.

  Hazlewood GP, Gilbert HJ. Hazlewood GP, et al. Prog Nucleic Acid Res Mol Biol. 1998;61:211-41. doi: 10.1016/s0079-6603(08)60828-4. Prog Nucleic Acid Res Mol Biol. 1998. PMID: 9752722 Review.

Cited by

• Splice Sites Seldom Slide: Intron Evolution in Oomycetes.

  Sêton Bocco S, Csűrös M. Sêton Bocco S, et al. Genome Biol Evol. 2016 Aug 25;8(8):2340-50. doi: 10.1093/gbe/evw157. Genome Biol Evol. 2016. PMID: 27412607 Free PMC article.

• Back in time to the Gly-rich prototype of the phosphate binding elementary function.

  Zheng Z, Goncearenco A, Berezovsky IN. Zheng Z, et al. Curr Res Struct Biol. 2024 Apr 9;7:100142. doi: 10.1016/j.crstbi.2024.100142. eCollection 2024. Curr Res Struct Biol. 2024. PMID: 38655428 Free PMC article. Review.

• Intron evolution as a population-genetic process.

  Lynch M. Lynch M. Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6118-23. doi: 10.1073/pnas.092595699. Proc Natl Acad Sci U S A. 2002. PMID: 11983904 Free PMC article.

• A new Drosophila spliceosomal intron position is common in plants.

  Tarrio R, Rodríguez-Trelles F, Ayala FJ. Tarrio R, et al. Proc Natl Acad Sci U S A. 2003 May 27;100(11):6580-3. doi: 10.1073/pnas.0731952100. Epub 2003 May 15. Proc Natl Acad Sci U S A. 2003. PMID: 12750476 Free PMC article.

• Retention of local conformational compactness in unfolding of barnase; Contribution of end-to-end interactions within quasi-modules.

  Shinoda K, Takahashi KI, Go M. Shinoda K, et al. Biophysics (Nagoya-shi). 2007 May 25;3:1-12. doi: 10.2142/biophysics.3.1. eCollection 2007. Biophysics (Nagoya-shi). 2007. PMID: 27857562 Free PMC article.

Publication types

MeSH terms

Substances

LinkOut - more resources

• Full Text Sources

  • Elsevier Science

• Miscellaneous

  • NCI CPTAC Assay Portal