Plant and Soil

, Volume 367, Issue 1–2, pp 363–377 | Cite as

Phenotypic and genotypic characterisation of root nodule bacteria nodulating Millettia pinnata (L.) Panigrahi, a biodiesel tree

  • Ni Luh Arpiwi
  • Guijun Yan
  • Elizabeth L. Barbour
  • Julie A. Plummer
  • Elizabeth Watkin
Regular Article

Abstract

Aims

Milletia pinnata is a leguminous tropical tree that produces seed oil suitable for biodiesel and is targeted to be planted on marginal land associated with nitrogen poor soil. This study aimed to identify effective rhizobia species for M. pinnata.

Methods

Soil samples were collected from M. pinnata grown in Kununurra, Australia. Rhizobia were trapped, characterised and sequenced for 16S rRNA, atpD, dnaK and recA genes.

Results

Forty isolates tolerated pH 7 – 9, temperatures 29 – 37 °C, salinity below 1 % NaCl, and had optimal growth on mannitol, arabinose or glutamate as a single carbon source, a few grew on sucrose and none grew on lactose. Inoculation of isolates increased shoot dry weight of M. pinnata’s seedlings in nitrogen minus media. Slow-growing isolates were closely related to Bradyrhizobium yuanmingense, Bradyrhizobium sp. DOA10, Bradyrhizobium sp. ORS305 and B. liaoningense LMG 18230T. The fast-growing isolates related to Rhizobium sp. 8211, R. miluonense CCBAU 41251T, R miluonense CC-B-L1, Rhizobium sp. CCBAU 51330 and Rhizobium sp. 43015

Conclusions

Millettia pinnata was effectively nodulated by slow-growing isolates related to Bradyrhizobium yuanmingense, Bradyrhizobium sp. DOA10 Bradyrhizobium sp. ORS305, B. liaoningense LMG 18230T and fast-growing isolates related Rhizobium sp. 8211, R. miluonense, Rhizobium sp. CCBAU 51330 and Rhizobium sp. 43015

Keywords

Bradyrhizobium Housekeeping genes Pongamia Rhizobia Rhizobium 16S rRNA gene 

Notes

Acknowledgements

We would like to thank the following organizations and people: Department of Higher Education, Republic of Indonesia (for the PhD scholarship for NLA), Forest Products Commission of Western Australia, the Centre for Legumes in Mediterranean Agriculture and the School of Plant Biology at the University of Western Australia for funding the research. Thanks to Len J Norris for field assistance and set up for the rhizobia trapping experiment and to Ms Frances Brigg at SABC, Murdoch University for help in sequencing. We also thank Dr Jason Terpolillli from Centre for Rhizobium Studies, Murdoch University and Associate Professor Susan Barker from School of Plant Biology the University of Western Australia for their advice on the manuscript.

References

  1. Appunu C, N’Zoue A, Moulin L, Depret G, Laguerre G (2009) Vigna mungo, V. radiata and V. unguiculata plants sampled in different agronomical–ecological–climatic regions of India are nodulated by Bradyrhizobium yuanmingense. Syst Appl Microbiol 32:460–470PubMedCrossRefGoogle Scholar
  2. Arpiwi NL, Yan G, Barbour EL, Plummer JA (2012) Genetic diversity, seed traits and salinity tolerance of Millettia pinnata (L.) Panigrahi, a biodiesel tree. Genet Resour Crop Evol. doi: 10.1007/s10722-012-9866-y
  3. Australian Bureau of Meteorology (2012) Climate data online http://www.bom.gov.au/climate/data/. Assessed 2 July 2012
  4. Brown CM, Dilworth MJ (1975) Ammonia assimilation by Rhizobium cultures and bacteroids. J Gen Microbiol 86:39–48PubMedCrossRefGoogle Scholar
  5. Chatel DL, Parker CA (1973) Survival of field-grown rhizobia over the dry summer period in Western Australia. Soil Biol Biochem 5:415–423CrossRefGoogle Scholar
  6. Craig GF, Atkins CA, Bell DT (1991) Effect of salinity on growth of four strains of Rhizobium and their infectivity and effectiveness on two species of Acacia. Plant Soil 133:253–262CrossRefGoogle Scholar
  7. Elbanna K, Elbadry M, Gamal-Eldin H (2009) Genotypic and phenotypic characterization of rhizobia that nodulate snap bean (Phaseolus vulgaris L.) in Egyptian soils. Syst Appl Microbiol 32:522–530PubMedCrossRefGoogle Scholar
  8. Fterich A, Mahdhi M, Caviedes MA, Pajuelo E, Rivas R, Rodriguez-Llorente ID, Mars M (2011) Characterization of root-nodulating bacteria associated to Prosopis farcta growing in the arid regions of Tunisia. Arch Microbiol 193:385–397PubMedCrossRefGoogle Scholar
  9. Graham PH (1992) Stress tolerance in Rhzobium and Bradyrhizobium, and nodulation under adverse soil conditions. Review. Can J Microbiol 38:475–484CrossRefGoogle Scholar
  10. Gueye F, Moulin L, Sylla S, Ndoye I, Bena G (2009) Genetic diversity and distribution of Bradyrhizobium and Azorhizobium strains associated with herb legume Zornia glochidiata sampled from across Sinegal. Syst Appl Microbiol 32:387–399PubMedCrossRefGoogle Scholar
  11. Gui MM, Lee KT, Bhatia S (2008) Feasibility of edible oil vs. non-edible oil vs. waste edible oil as biodiesel feedstock. Energy 33:1646–1653CrossRefGoogle Scholar
  12. Howieson JG, Ewing MA, D’Antuono MF (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105:179–188CrossRefGoogle Scholar
  13. Kumar S, Radhamani J, Singh AK, Varaprasad KS (2007) Germination and seed storage behaviour in Pongamia pinnata L. Scientific correspondence. Curr Sci 93:910–911Google Scholar
  14. Lane DJ (1991) 16S/23S rRNA sequencing. In: Strackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, pp 115–175Google Scholar
  15. Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Review. Cell Press 17:458–466Google Scholar
  16. Menna P, Barcellos FG, Hungria M (2009) Phylogeny and taxonomy of a diverse collection of Bradyhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int J Syst Evol Microbiol 59:2934–2950PubMedCrossRefGoogle Scholar
  17. Mohamed SH, Smouni A, Neyra M, Kharchaf D, Filali-Maltouf A (2000) Phenotypic characteristics of root-nodulating bacteria isolated from Acacia spp. grown in Libya. Plant Soil 224:171–183CrossRefGoogle Scholar
  18. Mukta N, Sreevalli Y (2010) Propagation techniques, evaluation and improvement of biodiesel plant, Pongamia pinnata (L.) Pierre – A review. Ind Crops Prod 31:1–12CrossRefGoogle Scholar
  19. Munoz V, Ibanez F, Tonelli ML, Valetti L, Anzuay MS, Fabra A (2011) Phenotypic and phylogenetic characterization of native peanut Bradyrhizobium isolates obtained from Córdoba, Argentina. Syst Appl Microbiol 34:446–452PubMedCrossRefGoogle Scholar
  20. Murphy HT, O’Connell DA, Seaton G, Raison RJ, Rodriguez LC, Braid AL, Kriticos DJ, Jovanovic T, Abadi A, Betar M, Brodie H, Lamont M, McKay M, Muirhead G, Plummer J, Arpiwi NL, Ruddle B, Saxena S, Scott PT, Stucley C, Thistlethwaite B, Wheaton B, Wylie P, Gresshoff PM (2012) A common view of the opportunities, challenges and research actions for Pongamia in Australia. Bioenerg Res 5:778–800CrossRefGoogle Scholar
  21. Ormeno-Orrillo E, Vinuesa P, Zuniga-Davila D, Martınez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262PubMedCrossRefGoogle Scholar
  22. Rahmani HA, Räsänen LA, Afshari M, Lindström K (2011) Genetic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in soils of Iran. Appl Soil Ecol 48:287–293Google Scholar
  23. Rajendhran J, Gunasekaran P (2011) Microbial phylogeny and diversity: small subunit ribosomal RNA sequence analysis and beyond. Microbiol Res 166:99–110PubMedCrossRefGoogle Scholar
  24. Ramırez-Bahena MH, Peix A, Rivas R, Camacho M, Rodrıguez-Navarro DN, Mateos PF, Martınez-Molina E, Willems A, Velazquez E (2009) Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol 59:1929–1934PubMedCrossRefGoogle Scholar
  25. Risal CP, Yokoyama T, Ohkama-Ohtsu N, Djedidi S, Sekimoto H (2010) Genetic diversity of native soybean bradyrhizobia from different topographical regions along the southern slopes of Himalayan Mountains in Nepal. Syst Appl Microbiol 33:416–425PubMedCrossRefGoogle Scholar
  26. Rivas R, Martens M, de Lajudie P, Willems A (2009) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32:101–110PubMedCrossRefGoogle Scholar
  27. Sahgal M, Johri BN (2003) The changing face of rhizobial systematics. Review article. Curr Sci 84:43–48Google Scholar
  28. Sarr PS, Yamakawa T, Fujimoto S, Saeki Y, Thao HTB, Myint AK (2009) Phylogenetic diversity and symbiotic effectiveness of root-nodulating bacteria associated with cowpea in the south-west area of Japan. Microb Environ 24:105–112CrossRefGoogle Scholar
  29. Scott PT, Pregelj L, Chen N, Hadler JS, Djordjevic MA, Gresshoff PM (2008) Pongamia pinnata: an untapped resource for the biofuels industry of the future. Bioenerg Res 1:2–11CrossRefGoogle Scholar
  30. Stepkowski T, Moulin L, Krzyzanska A, McInnes A, Law IJ, Howieson J (2005) European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl Environ Microbiol 71:7041–7052PubMedCrossRefGoogle Scholar
  31. Stepkowski T, Watkin E, McInnes A, Gurda D, Gracz J, Steenkamp ET (2012) Distinct Bradyrhizobium communities nodulate legumes native to temperate and tropical monsoon Australia. Mol Phylogenet Evol 63:265–277PubMedCrossRefGoogle Scholar
  32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  33. Tennakoon KU, Pate JS (1996) Heterotrophic gain of carbon from hosts by the xylem-tapping root hemiparasite Olax phyllanthi (Olacaceae). Oecologia 105:369–376CrossRefGoogle Scholar
  34. Tennakoon KU, Pate JS, Stewart GR (1997) Haustorium-related uptake and metabolism of host xylem solutes by the root hemiparasitic shrub Santalum acuminatum (R. Br.) A. DC. (Santalaceae). Ann Bot 80:257–264CrossRefGoogle Scholar
  35. Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martinez-Romero E (2005) Bradyrhizobium canariense sp. nov., and acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575PubMedCrossRefGoogle Scholar
  36. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14CrossRefGoogle Scholar
  37. Willems A, Coopman R, Gillis M (2001) Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA–DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51:623–632PubMedGoogle Scholar
  38. Yao ZY, Kan FL, Wang ET, Wei GH, Chen WX (2002) Characterization of rhizobia that nodulate legume species of genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int J Syst Evol Microbiol 52:2219–2230PubMedCrossRefGoogle Scholar
  39. Yates RJ, Howieson JG, Nandasena KG, O’Hara GW (2004) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 36:1319–1329CrossRefGoogle Scholar
  40. Yates RJ, Howieson JG, Reeve WG, Nandasena KG, Law IJ, Brau L, Ardley JK, Nistelberger HM, Real D, O’Hara GW (2007) Lotononis angolensis forms nitrogen fixing, lupinoid nodules with phylogenetically unique, fast-growing, pink-pigmented bacteria, which do not nodulate L. bainesii or L. listii. Soil Biol Biochem 39:1680–1688CrossRefGoogle Scholar
  41. Zhang YF, Wang ET, Tian CF, Wang FQ, Han LL, Chen WF, Chen WX (2008) Bradyrhizobium elkanii, Bradyrhizobium yuanmingense, Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China. FEMS Microbiol Lett 285:146–154PubMedCrossRefGoogle Scholar
  42. Zhang S, Xie F, Yang J, Li Y (2011) Phylogeny of bradyrhizobia from Chinese cowpea miscellany inferred from 16S rRNA, atpD, glnII and 16S-23S intergenic spacer sequences. Can J Microbiol 57:316–327PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Ni Luh Arpiwi
    • 1
    • 3
  • Guijun Yan
    • 1
    • 2
  • Elizabeth L. Barbour
    • 1
    • 4
  • Julie A. Plummer
    • 1
    • 2
  • Elizabeth Watkin
    • 5
  1. 1.School of Plant Biology, Faculty of Natural and Agricultural SciencesUniversity of Western AustraliaCrawleyAustralia
  2. 2.Institute of AgricultureUniversity of Western AustraliaCrawleyAustralia
  3. 3.Biology Department, Faculty of Natural and Basic SciencesUdayana UniversityBaliIndonesia
  4. 4.Forest Products Commission of Western AustraliaRivervaleAustralia
  5. 5.School of Biomedical Science, Faculty of Health SciencesCurtin UniversityBentleyAustralia

Personalised recommendations