1887

Abstract

has been shown previously to synthesize, in response to nodulation by sp. ACN14a, an array of peptides called symbiotic up-regulated peptides (ASUPs). In a previous study one peptide (Ag5) was shown to bind to nitrogen-fixing vesicles and to modify their porosity. Here we analyse four other ASUPs, alongside Ag5, to determine whether they have different physiological effects on grown sp. ACN14a. The five studied peptides were shown to have different effects on nitrogen fixation, respiration, growth, the release of ions and amino acids, as well as on cell clumping and cell lysis. The mRNA abundance for all five peptides was quantified in symbiotic nodules and one (Ag11) was found to be more abundant in the meristem part of the nodule. These findings point to some peptides having complementary effects on cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000291
2016-07-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/7/1173.html?itemId=/content/journal/micro/10.1099/mic.0.000291&mimeType=html&fmt=ahah

References

  1. Alloisio N., Félix S., Maréchal J., Pujic P., Rouy Z., Vallenet D., Medigue C., Normand P.. 2007; Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol Plant13:440–453[CrossRef]
    [Google Scholar]
  2. Alloisio N., Queiroux C., Fournier P., Pujic P., Normand P., Vallenet D., Médigue C., Yamaura M., Kakoi K. et al. 2010; The Frankia alni symbiotic transcriptome. Mol Plant Microb Interact23:593–607 [CrossRef]
    [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  4. Belarmino L. C., Benko-Iseppon A. M.. 2010; Databank based mining on the track of antimicrobial weapons in plant genomes. Curr Protein Pept Sci11:195–198 [CrossRef][PubMed]
    [Google Scholar]
  5. Bell C. D., Soltis D. E., Soltis P. S.. 2010; The age and diversification of the angiosperms re-revisited. Am J Bot97:1–8 [CrossRef][PubMed]
    [Google Scholar]
  6. Berry A. M., Harriott O. T., Moreau R. A., Osman S. F., Benson D. R., Jones A. D.. 1993; Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci U S A90:6091–6094[PubMed][CrossRef]
    [Google Scholar]
  7. Berry A. M., Thayer J. R., Enderlin C. S., Jones A. D.. 1990; Patterns of (N-13) ammonium uptake and assimilation by Frankia HFPArI3. Arch Microbiol154:510–513[CrossRef]
    [Google Scholar]
  8. Brogden K. A.. 2005; Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat Rev Microbiol3:238–250[CrossRef]
    [Google Scholar]
  9. Broughton W. J., Dilworth M. J.. 1971; Control of leghaemoglobin synthesis in snake beans. Biochem J125:1075–1080[PubMed][CrossRef]
    [Google Scholar]
  10. Carro L., Pujic P., Alloisio N., Fournier P., Boubakri H., Hay A. E., Poly F., François P., Hocher V. et al. 2015; Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. ISME J9:1723–1733 [CrossRef][PubMed]
    [Google Scholar]
  11. Chu H., Pazgier M., Jung G., Nuccio S. P., Castillo P. A., de Jong M. F., Winter M. G., Winter S. E., Wehkamp J. et al. 2012; Human alpha-defensin 6 promotes mucosal innate immunity through self-assembled peptide nanonets. Science337:477–481 [CrossRef][PubMed]
    [Google Scholar]
  12. Cournoyer B., Normand P.. 1992; Relationship between electroporation conditions, electropermeability and respiratory activity from Frankia strain ACN14a. FEMS Microbiol Lett94:95–100 [CrossRef]
    [Google Scholar]
  13. Demina I. V., Persson T., Santos P., Plaszczyca M., Pawlowski K.. 2013; Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: Actinorhizal nodules contain a specific class of defensins. PLoS One8:e72442 [CrossRef][PubMed]
    [Google Scholar]
  14. Fant F., Vranken W. F., Borremans F. A.. 1999; The three-dimensional solution structure of Aesculus hippocastanum antimicrobial protein 1 determined by 1H nuclear magnetic resonance. Proteins37:388–403[PubMed][CrossRef]
    [Google Scholar]
  15. Felsenstein J.. 1985; Confidence limits on phylogenies: An approach using the bootstrap. Evolution39:783–791 [CrossRef]
    [Google Scholar]
  16. Gruber C. W., Muttenthaler M.. 2012; Discovery of defense- and neuropeptides in social ants by genome-mining. PLoS One7:e32559 [CrossRef][PubMed]
    [Google Scholar]
  17. Gtari M., Ghodhbane-Gtari F., Nouioui I., Ktari A., Hezbri K., Mimouni W., Sbissi I., Ayari A., Yamanaka T. et al. 2015; Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep5:13112 [CrossRef][PubMed]
    [Google Scholar]
  18. Gtari M., Tisa L. S., Normand P.. 2014; Diversity of Frankia strains, actinobacterial symbionts of actinorhizal plants. In Symbiotic Endophytes, Soil Biology, Series 37 pp.123–148 . Edited by Aroca R.. Berlin & Heidelberg: Springer Verlag;
    [Google Scholar]
  19. Hammad Y., Marechal J., Cournoyer B., Normand P., Domenach A. M.. 2001; Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankia sp. strain ACN14a-tsr by root exudates of its symbiotic host Alnus glutinosa and cloning of the sodF gene. Can J Microbiol47:541–547[CrossRef]
    [Google Scholar]
  20. Hammad Y., Nalin R., Marechal J., Fiasson K., Pepin R., Berry A. M., Normand P., Domenach A.-M.. 2003; A possible role for phenylacetic acid (PAA) in Alnus glutinosa nodulation by Frankia. Plant Soil254:193–205[CrossRef]
    [Google Scholar]
  21. Hazlett L., Wu M.. 2011; Defensins in innate immunity. Cell Tissue Res343:175–188 [CrossRef][PubMed]
    [Google Scholar]
  22. Henderson J., Ricker R., Bidlingmeyer B., Woodward C.. 2000; Rapid, accurate, sensitive, and reproducible HPLC analysis of aminoacids. Amino acid analysis using Zorbax Eclipse-AAA columns and the Agilent 1100 HPLC. Agilent Technologies Inc., Publication Number 5980-1193E1–10
    [Google Scholar]
  23. Hocher V., Alloisio N., Auguy F., Fournier P., Doumas P., Pujic P., Gherbi H., Queiroux C., Da Silva C. et al. 2011; Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol156:1–12[CrossRef]
    [Google Scholar]
  24. Kucho K., Hay A. E., Normand P.. 2010; The Determinants of the Actinorhizal symbiosis. Microbes Environ25:241–252 [CrossRef][PubMed]
    [Google Scholar]
  25. Lehrer R. I.. 2004; Primate defensins. Nat Rev Microbiol2:727–738[CrossRef]
    [Google Scholar]
  26. Login F. H., Balmand S., Vallier A., Vincent-Monegat C., Vigneron A., Weiss-Gayet M., Rochat D., Heddi A.. 2011; Antimicrobial peptides keep insect endosymbionts under control. Science334:362–365[CrossRef]
    [Google Scholar]
  27. Lundquist P. O., Näsholm T., Huss-Danell K.. 2003; Nitrogenase activity and root nodule metabolism in response to O2 and short-term N2 deprivation in dark-treated Frankia-Alnus incana plants. Physiol Plant119:244–252[CrossRef]
    [Google Scholar]
  28. Mort A., Normand P., Lalonde M.. 1983; 2-o-methyl-d-mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol29:993–1002[CrossRef]
    [Google Scholar]
  29. Myers A. K., Tisa L. S.. 2003; Effect of electroporation conditions on cell viability of Frankia EuI1c. Plant Soil254:83–88 [CrossRef]
    [Google Scholar]
  30. Normand P., Benson D. R.. 2015;Frankia In Bergey's Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Ltd;
    [Google Scholar]
  31. Normand P., Lalonde M.. 1982; Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol28:1133–1142[CrossRef]
    [Google Scholar]
  32. Normand P., Lapierre P., Tisa L. S., Gogarten J. P., Alloisio N., Bagnarol E., Bassi C. A., Berry A. M., Bickhart D. M. et al. 2007; Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res17:7–15 [CrossRef][PubMed]
    [Google Scholar]
  33. Normand P., Simonet P., Prin Y., Moiroud A.. 1987; Formation and regeneration of Frankia protoplasts. Physiol Plant70:259–266[CrossRef]
    [Google Scholar]
  34. Poon I., Baxter A. A., Lay F. T., Mills G. D., Adda C. G., Payne J. A., Phan T. K., Ryan G. F., White J. A. et al. 2014; Phosphoinositide-mediated oligomerization of a defensin induces cell lysis. Elife3:e01808 [CrossRef][PubMed]
    [Google Scholar]
  35. Prin Y., Neyra M., Diem H.. 1990; Estimation of Frankia growth using Bradford protein and INT reduction activity estimations: application to inoculum standardization. FEMS Microbiol Lett69:91–95 [CrossRef]
    [Google Scholar]
  36. Pujic P., Fournier P., Alloisio N., Hay A. E., Marechal J., Anchisi S., Normand P.. 2012; Lectin genes in the Frankia alni genome. Arch Microbiol194:47–56[CrossRef]
    [Google Scholar]
  37. Saitou N., Nei M.. 1987; The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425[PubMed]
    [Google Scholar]
  38. Seufi A. M., Hafez E. E., Galal F. H.. 2011; Identification, phylogenetic analysis and expression profile of an anionic insect defensin gene, with antibacterial activity, from bacterial-challenged cotton leafworm, Spodoptera littoralis. BMC Mol Biol12:47 [CrossRef][PubMed]
    [Google Scholar]
  39. Spencer J. D., Schwaderer A. L., DiRosario J. D., McHugh K. M., McGillivary G., Justice S. S., Carpenter A. R., Baker P. B., Harder J. et al. 2011; Ribonuclease 7 is a potent antimicrobial peptide within the human urinary tract. Kidney Int80:174–180 [CrossRef][PubMed]
    [Google Scholar]
  40. Steiner H., Hultmark D., Engstrom A., Bennich H., Boman H. G.. 1981; Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature292:246–248 [CrossRef][PubMed]
    [Google Scholar]
  41. Stewart W. D., Fitzgerald G. P., Burris R. H.. 1967; In situ studies on nitrogen fixation with the acetylene reduction technique. Science158:536 [CrossRef][PubMed]
    [Google Scholar]
  42. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. 2013; MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  43. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. 1997; The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  44. Tisa L. S., Ensign J. C.. 1987; Formation and regeneration of protoplasts of the actinorhizal nitrogen-fixing actinomycete Frankia. Appl Environ Microbiol53:53–56
    [Google Scholar]
  45. Torrey J. G., Tjepkema J. D.. 1979; Symbiotic nitrogen fixation in actinomycete-nodulated plants. Preface and program. Bot Gaz140S:Si–Sv
    [Google Scholar]
  46. Tsai Y.-L., Benson D.. 1989; Physiological characteristics of glutamine synthetases I and II of Frankia sp. Strain CpI1. Arch Microb152:382–386[CrossRef]
    [Google Scholar]
  47. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A. et al. 2010; Plant peptides govern terminal differentiation of bacteria in symbiosis. Science327:1122–1126 [CrossRef][PubMed]
    [Google Scholar]
  48. Yamaguchi Y., Ouchi Y.. 2012; Antimicrobial peptide defensin: Identification of novel isoforms and the characterization of their physiological roles and their significance in the pathogenesis of diseases. Proc Jpn Acad Ser B Phys Biol Sci88:152–166[PubMed][CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000291
Loading
/content/journal/micro/10.1099/mic.0.000291
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error