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Saprophytic Actinomycetes Promote Nodulation in Medicago sativa-Sinorhizobium meliloti Symbiosis in the Presence of High N

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Abstract

Saprophytic rhizoactinomycetes isolated from the root nodule surface of the nitrogen-fixing actinorhizal plant Discaria trinervis, Streptomyces MM40, Actinoplanes ME3, and Micromonospora MM18, previously shown to stimulate nodulation in Frankia-Discaria trinervis symbiosis, were assayed as co-inoculants with Sinorhizobium meliloti 2011 on Medicago sativa. When plants were fertilized with a low level of N (0.07 mM), the inoculation of the actinomycetes alone did not show any effect on plant growth. Meanwhile, when actinomycetes were co-inoculated with S. meliloti, nodulation and plant growth were significantly stimulated compared to plants inoculated with only S. meliloti. The analysis of nodulation kinetics of simultaneously or delayed co-inoculations suggests that the effect of the actinomycetes operates in early infection and nodule development counteracting the autoregulation of nodulation by the plant. Because the actinomycete effect was found in the symbiotic nitrogen-fixing state of the plant, we investigated the effects of the actinomycetes, in single inoculation or co-inoculation with S. meliloti, on plants grown under a high level of N (7 mM) that was inhibitory for nodulation by S. meliloti. The inoculation of the actinomycetes alone did not show any effect on plant growth although high N was available. Unexpectedly, the co-inoculation of actinomycetes with S. meliloti on plants grown with high N (7 mM) significantly stimulates nodulation, clearly counteracting the inhibition of nodulation by high N. These results corroborate that the interaction of rhizoactinomycetes would interfere with the autoregulation of nodulation in alfalfa mediated by high N, opening new research lines of potential agronomical applications.

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References

  • Banerjee MR, Yesmin L, Vessey JK (2005) Plant-growth-promoting rhizobacteria as biofertilizers and biopesticides. In: Raid MK (ed) Handbook of microbial biofertilizers. Food Products Press, New York, pp 137–181

    Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y, Holguin G (1997) Azospirillum-plant relationships: environmental and physiological advances. Can J Microbiol 43:103–121

    Article  CAS  Google Scholar 

  • Caetano-Anollés G, Bauer WD (1988) Feedback regulation of nodule formation in alfalfa. Planta 175:546–557

    Article  Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Ann Rev Microbiol 45:345–382

    Article  Google Scholar 

  • Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680

    CAS  Google Scholar 

  • Fei H, Vessey JK (2003) Involvement of cytokinin in the stimulation of nodulation by low concentrations of ammonium in Pisum sativum L. Physiol Plant 118:447–455

    Article  CAS  Google Scholar 

  • Fei H, Vessey JK (2004) Further investigation of the roles of auxin and cytokinin in the NH4 +-induced stimulation of nodulation using white clover transformed with the auxin-sensitive reporter GH3:gusA. Physiol Plant 121:674–681

    Article  CAS  Google Scholar 

  • Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72

    Article  CAS  Google Scholar 

  • Ferrari A, Wall LG (2008) Co-inoculation of black locust with Rhizobium and Glomus on a desurfaced soil. Soil Sci 173:195–202

    Article  CAS  Google Scholar 

  • Frioni L (1999) Procesos microbianos. Tomo II. Editorial de la Fundación de la universidad Nacional de Río Cuarto, Córdoba

    Google Scholar 

  • Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M (2007) Legumes symbioses: absence of Nod genes in photosynthetic Bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Glick B (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Glick B, Patten C, Holguin G, Penrose D (1999) Biochemical and genetic mechanisms used by growth promoting rhizobacteria. Imperial College Press, London

    Google Scholar 

  • Goodfellow M, Cross T (1974) Actinomycetes. In: Dickinson CH, Pugh GJF (eds) Biology of plant litter decomposition. Academic Press, London, pp 269–289

    Google Scholar 

  • Gregor AK, Klunek B, Varsa EC (2003) Identification and use of actinomycetes for enhanced nodulation of soybean co-inoculated with Bradyrhizobium japonicum. Can J Microbiol 49:483–491

    Article  PubMed  CAS  Google Scholar 

  • Gudden RH, Vessey JK (1997) The stimulating effect of ammonium on nodulation in Pisum sativum L. is not long lived once ammonium supply is discontinued. Plant Soil 195:195–205

    Article  Google Scholar 

  • Guo J-H, Qi H-Y, Ge H-L, Gong L, Zhang L-X, Sun P-H (2002) Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biol Control 29:66–72

    Article  Google Scholar 

  • Höflich G, Wiehe W, Kuhn G (1994) Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experiencia 50:897–905

    Article  Google Scholar 

  • Huss-Danell K (1978) Nitrogenase activity measurements in intact plants of Alnus incana. Physiol Plant 43:372–376

    Article  CAS  Google Scholar 

  • Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–43

    Article  Google Scholar 

  • Knowlton S, Berry A, Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can J Microbiol 26:2877–2882

    Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426

    Article  PubMed  CAS  Google Scholar 

  • Liste HH (1993) Stimulation of symbiosis and growth of Lucerne by combined inoculation with Rhizobium meliloti and Pseudomonas fluorescens. Zentralbl Mikrobiol 148:163–176

    Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Mercier H, Kerbauy GB (1991) Effects of nitrogen source on growth rates and levels of endogenous cytokinins and chlorophyll in protocorms of Epidendrum fulgens. J Plant Physiol 138:195–199

    CAS  Google Scholar 

  • Morgan JAW, Bending GD, White PJ (2005) Biological cost and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739

    Article  PubMed  CAS  Google Scholar 

  • Mulder L, Hogg B, Bersoult A, Cullimore JV (2005) Integration of signaling pathways in the establishment of the legume-rhizobia symbiosis. Physiol Plant 123:207–218

    Article  CAS  Google Scholar 

  • Peters NK, Crist-Estes DK (1989) Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol 91:690–693

    Article  PubMed  CAS  Google Scholar 

  • Rhijn PV, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59:124–142

    PubMed  Google Scholar 

  • Ribaudo CM, Krumpholz EM, Cassán FD, Botín R, Cantore ML, Curá JA (2006) Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 24:175–185

    Article  CAS  Google Scholar 

  • Solans M (2007) Discaria trinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250

    Article  PubMed  Google Scholar 

  • Solans M, Vobis G (2003) Actinomycetes saprofíticos asociados a la rizósfera y rizoplano de Discaria trinervis. Ecol Aust 13:97–107

    Google Scholar 

  • Streeter JG (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23

    Article  CAS  Google Scholar 

  • Takana Y, Omura S (1990) Metabolism and products of actinomycetes-an introduction. Actinomycetologica 4:13–14

    Article  Google Scholar 

  • Tokala RK, Strip JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and pea plant (Pisum sativum). Appl Environ Microbiol 68:2162–2171

    Article  CAS  Google Scholar 

  • Valverde C, Wall LG (1999) Time course of nodule development in the Discaria trinervis (Rhamnaceae)-Frankia symbiosis. New Phytol 141:345–354

    Article  Google Scholar 

  • Valverde C, Wall LG (2005) Ethylene modulates the susceptibility of the root for nodulation in actinorhizal Discaria trinervis. Physiol Plant 124:121–131

    Article  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vobis G (1992) The genus Actinoplanes and related genera. In: Ballow A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The Prokaryotes, a handbook on the biology of bacteria, ecophysiology, isolation, identification, applications, vol 1, 2nd edn. Springer, New York, pp 1029–1060

    Google Scholar 

Download references

Acknowledgments

Financial support for this study was provided through grants from Agencia Nacional de Promoción Científica y Tecnológica PICT 10006 and PICT 20568, Universidad Nacional de Quilmes PPUNQ 0340/03, CONICET PIP 5812, and Universidad Nacional del Comahue 04/B118; all from Argentina. LGW is a member of the Scientific Research Career of CONICET. We thank Professor Gabriel Favelukes for critical reading of the manuscript and his valuable comments.

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Correspondence to Luis Gabriel Wall.

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Solans, M., Vobis, G. & Wall, L.G. Saprophytic Actinomycetes Promote Nodulation in Medicago sativa-Sinorhizobium meliloti Symbiosis in the Presence of High N. J Plant Growth Regul 28, 106–114 (2009). https://doi.org/10.1007/s00344-009-9080-0

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