Abstract
Background and Aims
The effects of three endophytic Streptomyces on plant growth and the symbiosis of Lucerne and its rhizobial partner were examined in the presence of three levels of soil nitrogen.
Methods
Three Streptomyces strains, LuP30 and LuP47B isolated from the roots of Lucerne (Medicago sativa L.) and EN23 isolated from roots of wheat (Triticum aestivum L.) were added as spores to Lucerne seeds (with and without Sinorhizobium meliloti RRI 128) at three levels of applied NH4NO3: 3, 25 and 50 mg/kg of soil.
Results
Plant growth increased with the addition of the actinobacteria strains alone from 19 % to 33 %. Co-inoculation of LuP30 with rhizobia strain RRI 128 produced the largest increase in shoot weight (46 %) of Lucerne plants growing in soil with 25 mg/kg NH4NO3. Co-inoculation with each of the actinobacteria with the rhizobia increased the number of nodules by more than 100 % compared with RRI128 alone, 4 weeks after rhizobial inoculation. A labelled 15N experiment showed co-inoculation with rhizobia and LuP30 or LuP47B enhanced N2-fixation 47 % and 72 %, respectively.
Conclusions
The actinobacteria significantly improved plant growth and N2-fixation when applied with the rhizobia strain RRI 128 to Lucerne plants growing in soil supplied with 25 mg/kg NH4NO3.
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References
Carro L, Pukall R, Spoker C, Kroppenstedt RM, Trujillo ME (2007) Micromonospora cremea sp. nov. and Micromonospora zamorensis sp. nov., isolated from the rhizosphere of Pisum sativum. Int J Syst Evol Microbiol 62:2971–2977
Carroll BJ, McNeil DL, Gresshoff PM (1985a) Isolation and properties of soybean [Glycine max (L.) merr.] mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci U S A 82:4162–4166
Carroll BJ, McNeil DL, Gresshoff PM (1985b) A supernodulation and nitrate-tolerant symbiotic (nst) soybean mutant. Plant Physiol 78:34–40
Coombs TJ, Franco CMM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608
Dogra RC, Dudeja SS (1993) Fertiliser N and nitrogen fixation in legume-Rhizobium symbiosis. Ann Biol 9:149–164
Dusha I (2002) Nitrogen control of bacterial signal production in Rhizobium meliloti- alfalfa symbiosis. Indian J Exp Biol 40:981–988
El-Tarabily KA, Hardy GESJ, Sivasithamparam K (2010) Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions in the United Arab Emirates. Eur J Plant Pathol 128:527–539
El-Tarabily KA, Nassar HA, Sivasithamparam K (2008) Promotion of growth of bean (Phaseolus vulgaris L.) in a calcareous soil by a phosphate-solubilizing, rhizosphere-competent isolate of Micromonospora endolithica. Appl Soil Ecol 39:161–171
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
Ferguson BJ, Indrasumunar A, Hayashi S, Lin M, Lin Y, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61–76
Franco CMM, Michelsen P, Percy N, Conn V, Listiana E, Moll S, Loria R, Coombs TJ (2007) Actinobacterial endophytes for improved crop performance. Australas Plant Pathol 36:524–531
García LC, Martínez-Molina E, Trujillo ME (2010) Micromonospora pisi sp. nov., isolated from root nodules of Pisum sativum. Int J Syst Evol Microbiol 60:331–337
Glloudemans T, Bisseling T (1989) Plant gene expression in early stages of rhizobium legume symbiosis. Plant Sci 65:1–13
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, Varshney RK (2015a) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. Springerplus 4:1–10
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015b) Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea. Org Agric 5:123–133
Gregor AK, Klubek 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
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
Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Rock phosphate-solubilizing actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24:2565–2575
Heichel RWF, Vance CP (1979) Nitrate-N and Rhizobium strain roles in alfalfa seedling nodulation and growth. Crop Sci 19:512–518
Herridge DF, Robertson MJ, Cocks B, Peoples MB, Holland JF, Heuke L (2005) Low nodulation and nitrogen fixation of mungbean reduce biomass and grain yields. Aust J Exp Agric 45:269–277
Le HX, Franco CMM, Ballard RA (2014) Isolation and characterisation of endophytic actinobacteria and their effect on the early growth and nodulation of Lucerne (Medicago sativa L.). In: VVSR Gupta, M Unkovich, BN Kaiser (eds) The 17th Australian nitrogen fixation conference, Adelaide: Australia.
Le HX, Franco CMM, Ballard RA, Drew EA (2015) Isolation and characterisation of endophytic actinobacteria and their effect on the early growth and nodulation of Lucerne (Medicago sativa L.). Plant Soil. doi:10.1007/s11104-015-2652-9
Li D-M, Alexander M (1988) Co-inoculation with antibiotic-producing bacteria to increase colonization and nodulation by rhizobia. Plant Soil 108:211–219
Li D-M, Alexander M (1990) Factors affecting co-inoculation with antibiotic-producing bacteria to enhance rhizobial colonization and nodulation. Plant Soil 129:195–201
Li D, Kinkema M, Gresshoff PM (2009) Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. J Plant Physiol 166:955–967
Lucínski R, Polcyn W, Ratajczak L (2002) Nitrate reduction and nitrogen fixation in symbiotic association Rhizobium-legumes. Acta Biochim Pol 49:537–546
Martínez-Hidalgo P, Galindo-Villardón P, Trujillo ME, Igual JM, Martínez-Molina E (2014) Micromonospora from nitrogen fixing nodules of alfalfa (Medicago sativa L.). a new promising plant probiotic bacteria. Sci Rep 4:1–9
McKnight T (1949) Efficiency of isolates of Rhizobium in the cowpea (Vigna unguiculata) group, with proposed additions to this group. Qd J Agric Sci 6:61–76
Miles AA, Misra SS (1938) The estimation of the bactericidal power of the blood. J Hyg 38:732–749
Mortier V, Holsters M, Goormatchtig S (2012) Never too many? How legumes control nodule numbers. Plant Cell Environ 35:245–258
Nimmnoi P, Pongsilp N, Lumyong S (2014) Co-inoculation of soybean (Glycine max) with actinomycetes and Bradyrhizobium japonicum enhances plant growth, nitrogenase activity and plant growth. J Plant Nutr 37:432–446
Pattison T, Moody P, Bagshaw J (2010) Soil health for vegetable production in Australia. The State of Queensland, Department of Employment, Economic Developement and Innovation
Puiatti M, Sodek L (1999) Ethylene and the inhibition of nodulation and nodule activity by nitrate in soybean. Rev Bras Fisiol Veg 11:169–174
Reid DE, Ferguson BJ, Hayashi S, Lin Y, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108:789–795
Samac DA, Willert AM, Mcbride MJ, Kinkel LL (2003) Effect of antibiotic-proucing Streptomyces on nodulation and leaf spot in alfalfa. Appl Soil Ecol 22:55–66
Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M (2005) Characterization of bacterial community structure in rhizosphere soil of grain legumes. Microb Ecol 49:407–415
Soe KM, Bhromsiri A, Karladee D, Yamakawa T (2012) Effects of endophytic actinomycetes and Bradyrhizobium japonicum strains on growth, nodulation, nitrogen fixation and seed weight of different soybean varieties. Soil Sci Plant Nutr 58:319–325
Solans M, Ruiz OA, Wall LG (2015) Effect of actinobacteria on Lotus tenuis-Mesorhizobium loti symbiosis: preliminary study. Symbiosis 65:33–37
Solans M, Vobis G, Wall LG (2009) Saprophytic actinomycetes promote nodulation in Medicago sativa-Sinorhizobium meliloti symbiosis in the presence of high nitrogen. J Plant Growth Regul 28:106–114
Streeter JG (1985) Nitrate inhibition of legume nodule growth and activity. Plant Physiol 77:325–328
Streeter JG (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E, Alonso P, Martínez-Molina E (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281
Trujillo ME, Kroppenstedt RM, Fernández-Molonero C, Schumann P, Martínez-Molina E (2007) Micromonospora lupini sp. nov. and Micromonospora saelicesensis sp. nov., isolated from root nodules of lupinus angustifolius. Int J Syst Evol Microbiol 57:2799–2804
Trujillo ME, Kroppenstedt RM, Schumann P, Martínez-Molina E (2006) Kribbella lupini sp. nov., isolated from the roots of Lupinus angustifolius. Int J Syst Evol Microbiol 56:407–411
Acknowledgments
We are grateful to SARDI for the supply of Lucerne seed and S. meliloti strain RRI 128, and Dr. Brent Kaiser for his advice and assistance with the 15N analyses.
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Le, X.H., Ballard, R.A. & Franco, C.M.M. Effects of endophytic Streptomyces and mineral nitrogen on Lucerne (Medicago sativa L.) growth and its symbiosis with rhizobia. Plant Soil 405, 25–34 (2016). https://doi.org/10.1007/s11104-015-2704-1
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DOI: https://doi.org/10.1007/s11104-015-2704-1