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

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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

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References

  • 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 32:460–470

    Article  PubMed  CAS  Google Scholar 

  • 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

  • Australian Bureau of Meteorology (2012) Climate data online http://www.bom.gov.au/climate/data/. Assessed 2 July 2012

  • Brown CM, Dilworth MJ (1975) Ammonia assimilation by Rhizobium cultures and bacteroids. J Gen Microbiol 86:39–48

    Article  PubMed  CAS  Google Scholar 

  • Chatel DL, Parker CA (1973) Survival of field-grown rhizobia over the dry summer period in Western Australia. Soil Biol Biochem 5:415–423

    Article  Google Scholar 

  • 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 133:253–262

    Article  CAS  Google Scholar 

  • 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 32:522–530

    Article  PubMed  CAS  Google Scholar 

  • 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 193:385–397

    Article  PubMed  CAS  Google Scholar 

  • Graham PH (1992) Stress tolerance in Rhzobium and Bradyrhizobium, and nodulation under adverse soil conditions. Review. Can J Microbiol 38:475–484

    Article  CAS  Google Scholar 

  • 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 32:387–399

    Article  PubMed  CAS  Google Scholar 

  • Gui MM, Lee KT, Bhatia S (2008) Feasibility of edible oil vs. non-edible oil vs. waste edible oil as biodiesel feedstock. Energy 33:1646–1653

    Article  CAS  Google Scholar 

  • Howieson JG, Ewing MA, D’Antuono MF (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105:179–188

    Article  CAS  Google Scholar 

  • Kumar S, Radhamani J, Singh AK, Varaprasad KS (2007) Germination and seed storage behaviour in Pongamia pinnata L. Scientific correspondence. Curr Sci 93:910–911

    Google Scholar 

  • 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 115–175

    Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Review. Cell Press 17:458–466

    CAS  Google Scholar 

  • 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 59:2934–2950

    Article  PubMed  CAS  Google Scholar 

  • 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 224:171–183

    Article  CAS  Google Scholar 

  • Mukta N, Sreevalli Y (2010) Propagation techniques, evaluation and improvement of biodiesel plant, Pongamia pinnata (L.) Pierre – A review. Ind Crops Prod 31:1–12

    Article  Google Scholar 

  • 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 34:446–452

    Article  PubMed  Google Scholar 

  • 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 5:778–800

    Article  Google Scholar 

  • 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 29:253–262

    Article  PubMed  CAS  Google Scholar 

  • 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 48:287–293

    Google Scholar 

  • Rajendhran J, Gunasekaran P (2011) Microbial phylogeny and diversity: small subunit ribosomal RNA sequence analysis and beyond. Microbiol Res 166:99–110

    Article  PubMed  CAS  Google Scholar 

  • 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 59:1929–1934

    Article  PubMed  Google Scholar 

  • 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 33:416–425

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Martens M, de Lajudie P, Willems A (2009) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32:101–110

    Article  PubMed  CAS  Google Scholar 

  • Sahgal M, Johri BN (2003) The changing face of rhizobial systematics. Review article. Curr Sci 84:43–48

    Google Scholar 

  • 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 24:105–112

    Article  Google Scholar 

  • 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 1:2–11

    Article  Google Scholar 

  • 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 71:7041–7052

    Article  PubMed  CAS  Google Scholar 

  • 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 63:265–277

    Article  PubMed  Google Scholar 

  • 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 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tennakoon KU, Pate JS (1996) Heterotrophic gain of carbon from hosts by the xylem-tapping root hemiparasite Olax phyllanthi (Olacaceae). Oecologia 105:369–376

    Article  Google Scholar 

  • 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 80:257–264

    Article  CAS  Google Scholar 

  • 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 55:569–575

    Article  PubMed  CAS  Google Scholar 

  • Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  • 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 51:623–632

    PubMed  CAS  Google Scholar 

  • 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 52:2219–2230

    Article  PubMed  CAS  Google Scholar 

  • 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 36:1319–1329

    Article  CAS  Google Scholar 

  • 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 39:1680–1688

    Article  CAS  Google Scholar 

  • 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 285:146–154

    Article  PubMed  CAS  Google Scholar 

  • 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 57:316–327

    Article  PubMed  CAS  Google Scholar 

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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.

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Correspondence to Elizabeth Watkin.

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Responsible Editor: Euan K. James.

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Arpiwi, N.L., Yan, G., Barbour, E.L. et al. Phenotypic and genotypic characterisation of root nodule bacteria nodulating Millettia pinnata (L.) Panigrahi, a biodiesel tree. Plant Soil 367, 363–377 (2013). https://doi.org/10.1007/s11104-012-1472-4

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