Archives of Microbiology

, Volume 189, Issue 3, pp 279–288 | Cite as

The 5′ untranslated region of fruA mRNA is required for translational enhancement of FruA synthesis during Myxococcus xanthus development

Original Paper


The fruA gene encodes a DNA-binding response regulator protein essential for the development of Myxococcus xanthus. This gene is transcribed with an unusually long (235 nucleotides) 5′ untranslated region (UTR) that has been shown to be absolutely necessary for the induction of FruA synthesis during development. With lacZ as a reporter, it was found in this report that each regional deletion mutation within 5′ UTR caused a decrease in β-galactosidase production. Base substitution mutations that were designed to alter local stem-loop structures also decreased fruA-lacZ expression, however their compensatory mutations could not rescue fruA-lacZ expression at all. A moderate decrease in β-galactosidase activity was observed from the fruA-lacZ transcriptional fusion lacking fruA 5′ UTR; in contrast, expression of the fruA-lacZ translational fusion lacking the 5′ UTR was severely impaired. In addition, both the amount and stability of fruA-lacZ mRNA were just moderately reduced in the absence of this 5′ UTR. These results suggest that the function of the 5′ UTR of fruA mRNA requires integrity of almost the entire region and may depend on the primary sequence. More importantly, fruA 5′ UTR modulates the expression of its own gene mainly by enhancing translation efficiency of the transcript.


Myxococcus xanthus fruA gene Untranslated region Translational control 





Open reading frame


Upstream ORF


Untranslated region



We thank one of the manuscript reviewer for pointing out that the result of Δ56–109 suggests translation of the uORF may not be required for translation of fruA.

Supplementary material


  1. Dworkin M (1996) Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60:70–102PubMedGoogle Scholar
  2. Ellehauge E, Nørregaard-Madsen M, Søgaard-Andersen L (1998) The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol Microbiol 30:807–817PubMedCrossRefGoogle Scholar
  3. Hodgkin J, Kaiser D (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci USA 74:2938–2942PubMedCrossRefGoogle Scholar
  4. Horiuchi T, Akiyama T., Inouye S, Komano T (2003) Regulation of FRUA expression during vegetative growth and development of Myxococcus xanthus. J Mol Microbiol Biotechnol 5:87–96PubMedCrossRefGoogle Scholar
  5. Horton RM, Ho SN, Pullen JK, Hunt HD, Cai Z, Pease LR (1993) Gene splicing by overlap extension. Methods Enzymol 217:270–279PubMedCrossRefGoogle Scholar
  6. Kaberdin VR, Bläsi U (2006) Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol Rev 30:967–979PubMedCrossRefGoogle Scholar
  7. Kaiser D (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci USA 76:5952–5956PubMedCrossRefGoogle Scholar
  8. Kaiser D (1986) Control of multicellular development: Dictyostelium and Myxococcus. Annu Rev Genet 20:539–566PubMedCrossRefGoogle Scholar
  9. Kaiser D (2004) Signaling in myxobacteria. Annu Rev Microbiol 58:75–98PubMedCrossRefGoogle Scholar
  10. Kashefi K, Hartzell PL (1995) Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF-defect. Mol Microbiol 15:483–494PubMedCrossRefGoogle Scholar
  11. Kim SK, Kaiser D (1990) Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus. Genes Dev 4:896–904PubMedCrossRefGoogle Scholar
  12. Kroos L, Kuspa A, Kaiser D (1986) A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol 117:252–266PubMedCrossRefGoogle Scholar
  13. Kruse T, Lobedanz S, Berthelsen NM, Søgaard-Andersen L (2001) C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Mol Microbiol 40:156–168PubMedCrossRefGoogle Scholar
  14. Lobedanz S, Søgaard-Andersen L (2003) Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev 17:2151–2161PubMedCrossRefGoogle Scholar
  15. Lovett PS, Rogers EJ (1996) Ribosome regulation by the nascent peptide. Microbiol Rev 60:366–385PubMedGoogle Scholar
  16. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46:813–826PubMedCrossRefGoogle Scholar
  17. Minton NP (1984) Improved plasmid vectors for the isolation of translational lac gene fusions. Gene 31:269–273PubMedCrossRefGoogle Scholar
  18. Morris DR, Geballe AP (2000) Upstream Open Reading Frames as Regulators of mRNA Translation. Mol Cell Biol 20:8635–8642PubMedCrossRefGoogle Scholar
  19. Ogawa M, Fujitani S, Mao X, Inouye S, Komano T (1996) FruA, a putative transcription factor essential for the development of Myxococcus xanthus. Mol Microbiol 22:757–767PubMedCrossRefGoogle Scholar
  20. Pontrelli L, Sidiropoulos KG, Adeli K (2004) Translational control of apolipoprotein B mRNA: regulation via cis elements in the 5’ and 3’ untranslated regions. Biochemistry 43:6734–6744PubMedCrossRefGoogle Scholar
  21. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring HarborGoogle Scholar
  22. Shimkets LJ, Asher SJ (1988) Use of recombination techniques to examine the structure of the csg locus of Myxococcus xanthus. Mol Gen Genet 211:63–71PubMedCrossRefGoogle Scholar
  23. Søgaard-Andersen L, Overgaard M, Lobedanz S, Ellehauge E, Jelsbak L, Rasmussen AA (2003) Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus. Mol Microbiol 48:1–8PubMedCrossRefGoogle Scholar
  24. Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ (1987) Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9:27–39CrossRefGoogle Scholar
  25. Srinivasan D, Kroos L (2004) Mutational analysis of the fruA promoter region demonstrates that C-Box and 5-base-pair elements are important for expression of an essential developmental gene of Myxococcus xanthus. J Bacteriol 186:5961–5967PubMedCrossRefGoogle Scholar
  26. Ueki T, Inouye S (2003) Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. Proc Natl Acad Sci USA 100:8782–8787PubMedCrossRefGoogle Scholar
  27. Wu Q, Mao XH (2004) The 5′ untranslated region of fruA mRNA in Myxococcus xanthus positively regulates the expression of its own gene. Chin Sci Bull 49:2266–2271CrossRefGoogle Scholar
  28. Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119PubMedCrossRefGoogle Scholar
  29. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Nianhua Ding
    • 1
  • Ying Zheng
    • 1
    • 2
  • Qian Wu
    • 1
    • 3
  • Xiaohua Mao
    • 1
  1. 1.Key laboratory of Developmental Genes and Human Diseases of Ministry of Education, Department of Genetics and Developmental BiologySoutheast University School of Basic Medical SciencesNanjingChina
  2. 2.Nanjing Center for Disease ControlNanjingChina
  3. 3.School of Public HealthNanjing Medical UniversityNanjingChina

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