Skip to main content
SpringerLink
Log in

Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a nodulating and plant growth promoting beta-proteobacterium, are influenced by environmental factors

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Burkholderia tuberum STM678T was isolated from a South African legume, but did not renodulate this plant. Until a reliable host is found, studies on this and other interesting beta-rhizobia cannot advance. We investigated B. tuberum STM678T’s ability to induce Fix+ nodules on a small-seeded, easy-to-propagate legume (Macroptilium atropurpureum). Previous studies demonstrated that B. tuberum elicited either Fix- or Fix+ nodules on siratro, but the reasons for this difference were unexplored.

Methods

Experiments to promote effective siratro nodule formation under different environmental conditions were performed. B. tuberum STM678T’s ability to withstand high temperatures and desiccation was checked as well as its potential for promoting plant growth via mechanisms in addition to nitrogen fixation, e.g., phosphate solubilization and siderophore production. Potential genes for these activities were found in the sequenced genomes.

Results

Higher temperatures and reduced watering resulted in reliable, effective nodulation on siratro. Burkholderia spp. solubilize phosphate and produce siderophores. Genes encoding proteins potentially involved in these growth-promoting activities were detected and are described.

Conclusions

Siratro is an excellent model plant for B. tuberum STM678T. We identified genes that might be involved in the ability of diazotrophic Burkholderia species to survive harsh conditions, solubilize phosphate, and produce siderophores.

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
Fig. 7

Similar content being viewed by others

Abbreviations

hpi:

hours post-inoculation

dpi:

days post-inoculation

CAS:

chrome azurol S

References

  • Ahmed B, Quilt P (1980) Effect of soil moisture stress on yield, nodulation and nitrogenase activity of Macroptilium atropurpureum cv. Siratro and Desmodium intortum cv. Greenleaf. Plant Soil 57:187–194

    Article  CAS  Google Scholar 

  • Andrews SC, Robinson AK, Rodriguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    Article  PubMed  CAS  Google Scholar 

  • Boone CM, Olsthoorn MMM, Dakora FD, Spaink HP, Thomas-Oates JE (1999) Structural characterization of lipo-oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes. Carbohyd Res 317:155–163

    Article  CAS  Google Scholar 

  • Brigham RD, Hoover MM (1956) A scarifying cup for small lots of legume seed. Agron J 48:531–532

    Article  Google Scholar 

  • Caballero-Mellado J, Martínez-Aquilar L, Paredes-Valdez G, Estrada-de los Santos P (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J System Evol Microbiol 54:1165–1172

    Article  CAS  Google Scholar 

  • Caballero-Mellado J, Onofre-Lemus J, Estrada-de Los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319

    Article  PubMed  CAS  Google Scholar 

  • Castro-González R, Martínez-Aquilar L, Ramírez-Trujillo A, Estrada-de los Santos P, Caballero-Mellado J (2011) High diversity of culturable Burkholderia species associated with sugarcane. Plant Soil. doi:10.1007/s11104-011-07680-0

  • Chen W-M, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen by β-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, James EK, Coenye T, Chou J-H, Barrios E, de Faria SM, Elliott GN, Sheu SY, Sprent JI, Vandamme P (2006) Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J System Evol Microbiol 56:1847–1851

    Article  CAS  Google Scholar 

  • Chen W-M, de Faria SM, James EK, Elliott GN, Lin KY, Chou J-H, Sheu SY, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J System Evol Microbiol 57:1055–1059

    Article  CAS  Google Scholar 

  • Cheng H-P, Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180:5183–5191

    PubMed  CAS  Google Scholar 

  • Collavino M, Riccillo PM, Grasso DH, Crespi M, Aguilar OM (2005) GuaB activity is required in Rhizobium tropici during the early stages of nodulation of determinate nodules but is dispensable for the Sinorhizobium meliloti-alfalfa symbiotic interaction. Mol Plant-Microbe Inter 18:742–750

    Article  CAS  Google Scholar 

  • de Faria SM, de Lima HC, Olivares FL, Melo RB, Xavier RP (1999) Nodulação em espécies florestais, especificidade hospedeira e implicações na sistemática de leguminosae. In: Siqueira JO, Moreira FMS, Lopes AS, Guiherme LRG, Faquin V, Furtinia Neto AE, Carvalho JG (eds) Soil Fertility, Soil Biology, and Plant Nutrition Interrelationships. Soc Brasil Ciên Univ Fed Lavras. pp. 667–686

  • Dos Reis FB Jr, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, Loureiro MF, de Queiroz LP, Scotti MR, Chen W-M, Norén A, Rubio MC, de Faria SM, Bontemps C, Goi SR, Young JP, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946

    Article  PubMed  Google Scholar 

  • Elliott GN, Chen W-M, Bontemps C, Chou J-H, Young JPW, Sprent JI, James EK (2007a) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot 100:1403–1411

    Article  PubMed  CAS  Google Scholar 

  • Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu SY, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, de Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007b) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180

    Article  CAS  Google Scholar 

  • Estévez J, Soria Díaz ME, Fernández de Córdoba F, Móron B, Manyan H, Gil A, Thomas-Oates J, van Brussel AAN, Dardanelli MS, Sousa C, Megías M (2009) Different and new Nod factors produced by Rhizobium tropici CIAT899 following Na+ stress. FEMS Microbiol Lett 293:220–231

    Article  PubMed  Google Scholar 

  • Estrada-de los Santos P, Vacaseydel-Aceves NB, Martínez-Aquilar L, Cruz-Hernández MA, Mendoza-Herrera A, Caballero-Mellado J (2011) Cupriavidus and Burkholderia species associated with agricultural plants that grow in alkaline soils. J Microbiol 49:867–876

    Article  PubMed  Google Scholar 

  • Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM (2008) Rhizobium common nod genes are required for biofilm formation Mol. Microbiology 67:504–515

    CAS  Google Scholar 

  • Garau G, Yates RJ, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem 41:125–134

    Article  CAS  Google Scholar 

  • Graham PH, Viteri SE, Mackie F, Vargas AAT, Palacios A (1982) Variation in acid soil tolerance among strains of Rhizobium phaseoli. Field Crops Res 5:121–128

    Article  Google Scholar 

  • Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martínez E, Arons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:189–207

    Article  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de los Santos P, Gross E, dos Reis Junior FB, Sprent JI, Young JPW, James EK (2011) Legume nodulating β-proteobacteria: diversity, host range and future prospects. Mol Plant-Microbe Inter 24:1276–1288

    Article  CAS  Google Scholar 

  • Hernandez-Lucas L, Segovia L, Martinez-Romero E, Pueppke SG (1995) Phylogenetic relationships and host range of Rhizobium spp. that nodulate Phaseolus vulgaris L. Appl Environ Microbiol 61:2775–2779

    PubMed  CAS  Google Scholar 

  • Herridge DF, Roughley RJ (1976) Influence of temperature and Rhizobium strain on nodulation and growth of two tropical legumes. Trop Grass 10:21–23

    Google Scholar 

  • Hirsch AM (1992) Tansley review No. 40. Developmental biology of legume nodulation. New Phytol 122:211–237

    Article  Google Scholar 

  • Hugenholtz P, Cunningham MA, Hendrlkz JK, Fuerst JA (1995) Desiccation resistance of bacteria isolated from an air-handling system biofilm determined using a simple quantitative membrane filter method. Lett Appl Micro 21:41–46

    Article  Google Scholar 

  • Iturriaga G, Suárez R, Nova-Franco B (2009) Trehalose metabolism: from osmoprotection to signaling. Int J Mol Sci 10:3793–3810

    Article  PubMed  CAS  Google Scholar 

  • Lee HK, LaRue TA (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv Sparkle. Plant Physiol 100:1759–1763

    Article  PubMed  CAS  Google Scholar 

  • Lima AS, Nobrega RSA, Barberi A, da Silva K, Ferreira DF, Moreira FMS (2009) Nitrogen-fixing bacteria communities occurring in soils under different uses in the Western Amazon Region as indicated by nodulation of siratro (Macroptilium atropurpureum). Plant Soil 319:127–145

    Article  CAS  Google Scholar 

  • Martínez-Romero E, Segovia L, Mercant FM, Franco AA, Graham P, Pardon MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Evol Microbiol 41:417–426

    Google Scholar 

  • Mathew JA, Tan YP, Srinivasa Rao PS, Lim TM, Leung KY (2001) Edwardisella tarda mutants defective in siderophore production, motility, serum resistance and catalase activity. Microbiology 149:449–457

    Google Scholar 

  • Michiels J, Verreth C, Vanderleyden J (1994) Effect of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212

    PubMed  CAS  Google Scholar 

  • Mietzner TA, Morse SA (1994) The role of iron-binding proteins in the survival of pathogenic bacteria. Annu Rev Nutr 14:471–493

    Article  PubMed  CAS  Google Scholar 

  • Mishra RP, Tisseyre P, Melkonian R, Chaintreuil C, Miché L, Klonowska A, Gonzalez S, Bena G, Laguerre G, Moulin L (2012) Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol 79:487–503

    Article  PubMed  CAS  Google Scholar 

  • Móron B, SoriaDíaz ME, Ault J, Verroios G, Noreen S, Rodríguez-Navarro DN, Gil-Serrano A, Thomas-Oates J, Megías M, Sousa C (2005) Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem Biol 12:1020–1040

    Article  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of proteobacteria. Nature 411:948–950

    Article  PubMed  CAS  Google Scholar 

  • Muofhe ML, Dakora FD (1998) Bradyrhizobium species isolated from indigenous legumes of the Western Cape exhibit high tolerance of low pH. In: Elmerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer Academic Publishers, Dordrecht, p 519

    Google Scholar 

  • Ohashi Y, Saneoka H, Fujita K (2000) Effect of water stress of growth, photosynthesis, and photoassimilate translocation in soybean and tropical pasture legume siratro. Soil Sci Plant Nutr 46:417–425

    CAS  Google Scholar 

  • Perin L, Martinez-Aquilar L, Paredes-Valdez G, Baldani JI, Estrada-de Los Santos P, Reis VM, Cabellero-Mellado J (2006) Burkholderia silvatlantica sp. nov., a bacterium associated with field-grown sugarcane and maize. Int J Syst Evol Microbiol 56:1931–1937

    Article  PubMed  CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorous soil in connection with the vital activity of some microbial species. Microbiol (Mikrobiol) 17:362–370

    CAS  Google Scholar 

  • Pinto FGS, Chueire LMO, Vasconcelos ATR, Nicolás MF, Almeida LGP, Souza RC, Menna P, Barcellos FG, Megías N, Hungria M (2009) Novel genes related to nodulation, secretion systems, and surface structures revealed by a genome draft of Rhizobium tropici strain PRF 81. Funct Integr Genom 9:263–270

    Article  CAS  Google Scholar 

  • Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Inter 12:293–318

    Article  CAS  Google Scholar 

  • Riccillo PM, Collavino MM, Grasso DH, England R, de Bruijn FJ, Aguilar OM (2000) A guaB mutant strain of Rhizobium tropici CIAT899 pleiotropically defective in thermal tolerance and symbiosis. Mol Plant-Microbe Inter 13:1228–1236

    Article  CAS  Google Scholar 

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  PubMed  Google Scholar 

  • Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21

    Article  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  PubMed  CAS  Google Scholar 

  • Sheriff DW, Ludlow MM (1984) Physiological reactions to an imposed drought by Macroptilium atropurpureum and Cenchrus ciliaris in a mixed sward. Aust J Plant Physiol 11:23–34

    Article  Google Scholar 

  • Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 186:934–946

    Google Scholar 

  • Streeter JG, Gomez ML (2006) Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. Appl Environ Microbiol 72:4250–4255

    Article  PubMed  CAS  Google Scholar 

  • Suárez-Moreno AR, Cabellero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266

    Article  PubMed  Google Scholar 

  • Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hiratsuka Y, Yoshinaga A, Arima S, Agarie S, Sakai T, Inada S, Jikumaru Y, Kamiya Y, Uchiumi T, Abe M, Hashiguchi M, Akashi T, Sato S, Kaneko T, Tabata S, Hirsch AM (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the R/FR ratio through JA signaling. Proc Natl Acad Sci USA 108:16837–16842

    Article  PubMed  CAS  Google Scholar 

  • Van Brussel AAN, Tak T, Wetselaar A, Pees E, Wijffelman CA (1982) Small Leguminosae as test plants for nodulation of Rhizobium leguminosarum and other rhizobia an agrobacteria harbouring a leguminosarum sym-plasmid. Plant Sci Lett 27:317–325

    Article  Google Scholar 

  • Vandamme P, Goris J, Chen W-M, de Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512

    Article  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Blackwell Scientific Publications, London

    Google Scholar 

  • Weisskofp L, Heller S, Eberl L (2011) Burkholderia species are major inhabitants of white lupin cluster roots. Appl Environ Microbiol 77:7715–7720

    Article  Google Scholar 

  • Xie J, Knight D, Legget M (2009) Comparison of media used to evaluate Rhizobium leguminosarum biovar viciae for phosphate-solubilizing ability. Can J Microbiol 55:910–915

    Article  PubMed  CAS  Google Scholar 

  • Yao W, Byrne R (2001) Spectrophotometric determination of freshwater pH using bromocresol purple and phenol red. Environ Sci Technol 35:1197–1201

    Article  PubMed  CAS  Google Scholar 

  • Yeung S-L, Cheng C, Lui TKO, Tsang JSH, Chan W-T, Lim BL (2009) Purple acid phosphastase-like sequences in prokaryotic genomes and the characterization of an atypical purple alkaline phosphatase from Burkholderia cenocepacia J2315. Gene 440:1–8

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported in part by a grant (IOB-0537497) from the National Science Foundation (USA) to GW and AMH and a Shanbrom Family Foundation grant to AMH. A University of California Office of The President, President’s Postdoctoral Fellowship, supported AA. We thank the National Germplasm Collection of the USDA-ARS for seeds of various cowpea varieties that were tested and the Joint Genome Institute/Department of Energy for the annotation platform. LMU’s Seaver College of Science and Engineering M.A.N.E. laboratory is thanked for the use of the confocal microscope.

Liamara Perin and Veronica M. Reis of EMBRAPA are acknowledged for their previous research on Burkholderia species and for providing helpful information regarding B. silvatlantica SRMrh20T. J. Peter Young is thanked for providing the B. tuberum/gfp strain. Members of the Hirsch laboratory, especially Drs. Drora Kaplan and Nisha Tak are thanked for reviewing the manuscript.

This paper is dedicated to the memory of Jesus Cabellero-Mellado, one of the pioneers in the study of the plant-associated Burkholderia species.

Author information

Authors and Affiliations

  1. Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, CA, 90095, USA

    Annette A. Angus, Maya Shehayeb, Reza Hessabi, Nancy A. Fujishige, Stephanie Kano, Nannie Song, Paul Yang & Ann M. Hirsch

  2. Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, CA, 90095, USA

    Andrew Lee

  3. Molecular Biology Institute, University of California, Los Angeles, CA, 90095, USA

    Ann M. Hirsch

  4. Biology Department, Loyola Marymount University, Los Angeles, CA, 90045, USA

    Michelle R. Lum

  5. Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Shailaja Yerrapragada

  6. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala, México, DF, 11340, Mexico

    Paulina Estrada de los Santos

  7. Embrapa Agrobiologia, Seropédica, 23890-000, RJ, Brazil

    Sergio M. de Faria

  8. Chemistry Department, Tshwane University of Technology, Arcadia Campus, 175 Nelson Mandela, Drive Private Bag X680, Pretoria, 0001, South Africa

    Felix D. Dakora

  9. Department of Genetics, Washington University School of Medicine, St. Louis, MO, 63110, USA

    George Weinstock

  10. University of California-Los Angeles (UCLA), 621 Charles E. Young Drive South, Los Angeles, CA, 90095-1606, USA

    Ann M. Hirsch

Authors
  1. Annette A. Angus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michelle R. Lum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maya Shehayeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Reza Hessabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nancy A. Fujishige
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shailaja Yerrapragada
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Stephanie Kano
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nannie Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Paul Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Paulina Estrada de los Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sergio M. de Faria
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Felix D. Dakora
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. George Weinstock
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Ann M. Hirsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ann M. Hirsch.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1

Burkholderia tuberum STM678T-inoculated plants nodulate under water-stressed conditions. Dishpans containing siratro plants inoculated (a and c) with B. tuberum STM678T or left uninoculated (b). Dishpans a) and b) were watered with ¼ strength Hoagland’s medium minus N twice weekly whereas dishpan c was watered every other week. (JPEG 398 kb)

Supplementary Figure 2

Burkholderia species vary in ability to solubilize inorganic phosphate depending on the supplied carbon source. (a) When either sucrose or glucose was supplied as the sole carbon source in the preparation of PVK medium, a difference in the ability to solubilize inorganic phosphate was observed on agar plates. (b) Measurements indicate the zone of clearance (if any) calculated by measuring the surrounding halo to equal starting OD values of bacteria. Error bars indicate standard error. (JPEG 242 kb)

Supplementary Figure 3

Burkholderia species secrete siderophores. (a) Iron acquisition via siderophore secretion was detected 5 dpi using chrome azurol S (CAS) overlay agar assay plates for each of the Burkholderia species studied. The presence of the yellow/orange halo around the spot of bacterial growth indicates the presence of iron-binding siderophores being secreted into the surrounding media. (b) Measurements indicate the zone of each halo, calculated by taking the ratio of the surrounding halo to that of the bacterial growth. Error bars indicate standard error. (JPEG 7 kb)

High resolution image (TIFF 1429 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angus, A.A., Lee, A., Lum, M.R. et al. Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a nodulating and plant growth promoting beta-proteobacterium, are influenced by environmental factors. Plant Soil 369, 543–562 (2013). https://doi.org/10.1007/s11104-013-1590-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1590-7

Keywords

Search

Navigation