Skip to main content
SpringerLink
Log in

Lectin genes in the Frankia alni genome

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Frankia alni strain ACN14a’s genome was scanned for the presence of determinants involved in interactions with its host plant, Alnus spp. One such determinant type is lectin, proteins that bind specifically to sugar motifs. The genome of F. alni was found to contain 7 such lectin-coding genes, five of which were of the ricinB-type. The proteins coded by these genes contain either only the lectin domain, or also a heat shock protein or a serine-threonine kinase domain upstream. These lectins were found to have several homologs in Streptomyces spp., and a few in other bacterial genomes among which none in Frankia EAN1pec and CcI3 and two in strain EUN1f. One of these F. alni genes, FRAAL0616, was cloned in E. coli, fused with a reporter gene yielding a fusion protein that was found to bind to both root hairs and to bacterial hyphae. This protein was also found to modify the dynamics of nodule formation in A. glutinosa, resulting in a higher number of nodules per root. Its role could thus be to permit binding of microbial cells to root hairs and help symbiosis to occur under conditions of low Frankia cell counts such as in pioneer situations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adham SA, Honrubia P, Diaz M, Fernandez-Abalos JM, Santamaria RI, Gil JA (2001) Expression of the genes coding for the xylanase Xys1 and the cellulase Cel1 from the straw-decomposing Streptomyces halstedii JM8 cloned into the amino-acid producer Brevibacterium lactofermentum ATCC13869. Arch Microbiol 177:91–97

    Article  PubMed  CAS  Google Scholar 

  • Alloisio N, Queiroux C, Fournier P, Pujic P, Normand P, Vallenet D, Médigue C, Yamaura M, Kakoi K, Kucho K (2010) The Frankia alni symbiotic transcriptome. Mol Plant Microb Interact 23:593–607

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Arveby A, Huss-Danell K (1988) Presence and dispersal of infective Frankia in peat and meadow soils in Sweden. Biol Fertil Soils 6:39–44

    Article  Google Scholar 

  • Bosco M, Fernandez MP, Simonet P, Materassi R, Normand P (1992) Evidence that some Frankia sp. strains are able to cross boundaries between Alnus and Elaeagnus host specificity groups. Appl Environ Microbiol 58:1569–1576

    PubMed  CAS  Google Scholar 

  • Bouwmeester K, Govers F (2009) Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J Exp Bot 60:4383–4396

    Article  PubMed  CAS  Google Scholar 

  • Broughton WT, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080

    PubMed  CAS  Google Scholar 

  • Bru C, Courcelle E, Carrere S, Beausse Y, Dalmar S, Kahn D (2005) The ProDom database of protein domain families: more emphasis on 3D. Nucleic Acids Res 33:D212–D215

    Article  PubMed  CAS  Google Scholar 

  • Burleigh S, Dawson J (1994) Occurrence of Myrica-nodulating Frankia in Hawaiian volcanic soils. Plant Soil 164:283–289

    Article  CAS  Google Scholar 

  • Ceremonie H, Debelle F, Fernandez MP (1999) Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301

    CAS  Google Scholar 

  • Chaboud A, Lalonde M (1983) Lectin binding on surfaces of Frankia strains. Can J Bot 61:2889–2897

    Article  CAS  Google Scholar 

  • Chrispeels MJ, Raikhel NV (1991) Lectins, lectin genes, and their role in plant defense. Plant Cell 3:1–9

    Article  PubMed  CAS  Google Scholar 

  • Danelishvili L, Yamazaki Y, Selker J, Bermudez LE (2010) Secreted Mycobacterium tuberculosis Rv3654c and Rv3655c proteins participate in the suppression of macrophage apoptosis. PLoS ONE 5:e10474

    Article  PubMed  Google Scholar 

  • Drickamer K, Taylor ME (1993) Biology of animal lectins. Annu Rev Cell Biol 9:237–264

    Article  PubMed  CAS  Google Scholar 

  • Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16:374–381

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol 39:783–791

    Article  Google Scholar 

  • Fernandez C, Szabo IM (1982) Studies on the selection of streptomycetes in the rhizoplane of sugar-cane. Folia Microbiol 27:423–427

    Article  CAS  Google Scholar 

  • Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932

    Article  PubMed  CAS  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224

    Article  PubMed  CAS  Google Scholar 

  • Gtari M, Brusetti L, Skander G, Mora D, Boudabous A, Daffonchio D (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 234:349–355

    Article  PubMed  CAS  Google Scholar 

  • Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P, Domenach AM (2003) A possible role for phenylacetic acid (PAA) in Alnus glutinosa nodulation by Frankia. Plant Soil 254:193–205

    Article  CAS  Google Scholar 

  • Hocher V, Auguy F, Argout X, Laplaze L, Franche C, Bogusz D (2006) Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytol 169:681–688

    Article  PubMed  Google Scholar 

  • Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 156:1–12

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinform 23:2947–2948

    Article  CAS  Google Scholar 

  • Lis H, Sharon N (1998) Lectins: carbohydrate-specific proteins that mediate cellular recognition. Chem Rev 98:637–674

    Article  PubMed  CAS  Google Scholar 

  • Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLOS Biol 6:e68

    Article  PubMed  Google Scholar 

  • Martinez Zamora MG, Castagnaro AP, Diaz Ricci JC (2008) Genetic diversity of Pto-like serine/threonine kinase disease resistance genes in cultivated and wild strawberries. J Mol Evol 67:211–221

    Article  PubMed  CAS  Google Scholar 

  • Mastronunzio JE, Tisa LS, Normand P, Benson DR (2008) Comparative secretome analysis suggests low plant cell wall degrading capacity in Frankia symbionts. BMC Genomics 9:47

    Article  PubMed  Google Scholar 

  • Mocsai A, Ruland J, Tybulewicz VL (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 10:387–402

    Article  PubMed  CAS  Google Scholar 

  • Mort A, Normand P, Lalonde M (1983) 2-o-methyl-d-mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol 29:993–1002

    Article  CAS  Google Scholar 

  • Murry M, Fontaine M, Torrey J (1984) Growth kinetics and nitrogenase induction in Frankia sp. HFPArI3 grown in batch culture. Plant Soil 78:61–78

    Google Scholar 

  • Nalin R, Normand P, Domenach AM (1997) Distribution and N2-fixing activity of Frankia strains in relation to soil depth. Physiol Plant 99:732–738

    Article  CAS  Google Scholar 

  • Navarro E, Bousquet J, Moiroud A, Munive A, Piou D, Normand P (2003) Molecular phylogeny of Alnus (Betulaceae), inferred from nuclear ribosomal DNA ITS sequences. Plant Soil 254:207–217

    Article  CAS  Google Scholar 

  • Normand P, Chapelon C (1997) Direct characterization of Frankia and of close phyletic neighbors from an Alnus viridis rhizosphere. Physiol Plant 99:722–731

    Article  CAS  Google Scholar 

  • Normand P, Fernandez M (2009) Evolution and diversity of Frankia. In: Pawlowski K (ed) Prokaryotic symbionts in plants. Springer, Berlin, pp 103–125

    Google Scholar 

  • Normand P, Lalonde M (1982) Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol 28:1133–1142

    Article  Google Scholar 

  • Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 46:1–9

    Article  PubMed  CAS  Google Scholar 

  • Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007a) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15

    Article  PubMed  Google Scholar 

  • Normand P, Queiroux C, Tisa L, Benson D, Cruveiller S, Rouy Z, Medigue C (2007b) Exploring the genomes of Frankia sp. Physiol Plant 13:331–343

    Article  Google Scholar 

  • Persson T, Benson D, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce DC, Detter C, Tapia R, Han S, Han J, Woyke T, Pitluck S, Pennacchio L, Nolan M, Ivanova N, Pati A, Land ML, Pawlowski K, Berry AB (2011) Genome sequence of Candidatus Frankia datiscae Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schep LJ, Temple WA, Butt GA, Beasley MD (2009) Ricin as a weapon of mass terror—separating fact from fiction. Environ Int 35:1267–1271

    Article  PubMed  CAS  Google Scholar 

  • Smolander A (1990) Frankia populations in soils under different tree species—with special emphasis on soils under Betula pendula. Plant Soil 121:1–10

    Article  Google Scholar 

  • Torsvik V, Goksoyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    PubMed  CAS  Google Scholar 

  • Vallenet D, Labarre L, Rouy Z, Barbe V, Bocs S, Cruveiller S, Lajus A, Pascal G, Scarpelli C, Medigue C (2006) MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34:53–65

    Article  PubMed  CAS  Google Scholar 

  • van Rhijn P, Goldberg RB, Hirsch AM (1998) Lotus corniculatus nodulation specificity is changed by the presence of a soybean lectin gene. Plant Cell 10:1233–1250

    Article  PubMed  Google Scholar 

  • van Rhijn P, Fujishige NA, Lim PO, Hirsch AM (2001) Sugar-binding activity of pea lectin enhances heterologous infection of transgenic alfalfa plants by Rhizobium leguminosarum biovar viciae. Plant Physiol 126:133–144

    Article  PubMed  Google Scholar 

  • Vujaklija D, Schroder W, Abramic M, Zou P, Lescic I, Franke P, Pigac J (2002) A novel streptomycete lipase: cloning, sequencing and high-level expression of the Streptomyces rimosus GDS(L)-lipase gene. Arch Microbiol 178:124–130

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Thanks are expressed to Danis Abrouk (Université Lyon) for help with formatting large data sets for analysis. Thanks are expressed to the Greenhouse for help with plant growing and to the DTAMB for access to Q-PCR (FR Bioenvironnement et Santé).

Author information

Authors and Affiliations

  1. Ecologie Microbienne, UMR5557 CNRS, Universite Lyon, Universite Lyon1, 16 rue Dubois, 69622, Villeurbanne cedex, France

    Petar Pujic, Pascale Fournier, Nicole Alloisio, Anne-Emmanuelle Hay, Joelle Maréchal, Stéphanie Anchisi & Philippe Normand

Authors
  1. Petar Pujic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pascale Fournier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicole Alloisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne-Emmanuelle Hay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joelle Maréchal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stéphanie Anchisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Philippe Normand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philippe Normand.

Additional information

Communicated by Eriko Takano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 67 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pujic, P., Fournier, P., Alloisio, N. et al. Lectin genes in the Frankia alni genome. Arch Microbiol 194, 47–56 (2012). https://doi.org/10.1007/s00203-011-0770-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-011-0770-1

Keywords

Search

Navigation