Co-invasion of South African ecosystems by an Australian legume and its rhizobial symbionts

Journal of Biogeography

Volumn 40, Issue 7, 2013, Pages 1240-1251

  Ndlovu, Joice ^a   Richardson, David M ^a   Wilson, John R U ^a,b   Le Roux, Johannes J ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b SOUTH AFRICAN NATIONAL BIODIVERSITY INSTITUTE   (South Africa)

Author keywords

Acacia pycnantha; Australia; Biological invasions; Co introduction hypothesis; Generalist; Host jumping hypothesis; Mutualisms; Plant growth promoters; Rhizobia; South Africa

Indexed keywords

BACTERIUM; BIOLOGICAL INVASION; GENERALIST; HOME RANGE; HOST SPECIFICITY; HOST-SYMBIONT INTERACTION; INVASIVE SPECIES; LEGUME; MUTUALISM; NATIVE SPECIES; PHYLOGENETICS; PHYLOGENY; RHIZOBACTERIUM; TAXONOMY;

AUSTRALIA; SOUTH AFRICA;

ACACIA; ACACIA PYCNANTHA; BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM JAPONICUM; BURKHOLDERIA; BURKHOLDERIA CALEDONICA; BURKHOLDERIA GRAMINIS; BURKHOLDERIA PHYTOFIRMANS; RHIZOBIACEAE; RHIZOBIUM; RHIZOBIUM GALLICUM; RHIZOBIUM LUSITANUM; RHIZOBIUM TROPICI;

EID: 84880068945     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/jbi.12091     Document Type: Article

References (49)

1. Ardley, J.K., O'Hara, G.W., Reeve, W.G., Yates, R.J., Dilworth, M.J., Tiwari, R.P. & Howieson, J.G. (2009) Root nodule bacteria isolated from South African Lotononis bainesii, L. listii and L. solitudinis species of Methylobacterium that are unable to utilize methanol. Archives of Microbiology, 191, 311-318.
2. Birnbaum, C., Barret, L., Thrall, P.H. & Leishman, M.R. (2012) Mutualisms are not constraining cross-continental invasional success of Acacia species within Australia. Diversity and Distributions, 18, 962-976.
3. Bontemps, C., Elliott, G.N., Simon, M.F., dos Reis Junior, F.B., Gross, E., Lawton, R.C., Neto, N.E., Loureiro, M.F., de Faria, S.M., Sprent, J.I., James, E.K. & Young, J.P. (2010) Burkholderia species are ancient symbionts of legumes. Molecular Ecology, 19, 44-52.
4. Burdon, J.J., Gibson, H., Searle, S.D., Woods, M.J. & Brockwell, J. (1999) Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian Acacia: within-species interactions. Journal of Applied Ecology, 36, 398-408.
5. Chen, W.M., James, E.K., Chou, J.H., Sheu, S.Y., Yang, S.Z. & Sprent, J.I. (2005) Βeta-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytologist, 168, 661-675.
6. Compant, S., Nowak, J., Coenye, T., Clément, C. & Barka, E.A. (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiology Reviews, 32, 607-626.
7. Crisóstomo, J.A., Rodríguez-Echeverría, S. & Freitas, H. (2013) Co-introduction of exotic rhizobia to the rhizosphere of the invasive legume Acacia saligna, an intercontinental study. Applied Soil Ecology, 64, 118-126.
8. Daehler, C.C. (1998) The taxonomic distribution of invasive angiosperm plants: ecological insights and comparison to agricultural weeds. Biological Conservation, 84, 167-180.
9. Dashti, N., Zhang, F., Hynes, R. & Smith, D.L. (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant and Soil, 200, 205-213.
10. Elliot, G.N., Chen, W.M., Bontemps, C., Chou, J.H., Young, J.P.W., Sprent, J.I. & James, E.K. (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Annals of Botany, 100, 1403-1411.
11. Gaertner, M., Den Breeÿen, A., Hui, C. & Richardson, D.M. (2009) Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: a meta-analysis. Progress in Physical Geography, 33, 319-338.
12. García-Fraile, P., Rivaz, R., Willems, A., Peix, A., Martens, M., Martínez-Molina, E., Mateos, P.F. & Veláquez, E. (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. International Journal of Systematic and Evolutionary Microbiology, 57, 844-848.
13. Gu, C.T., Wang, E.T., Tian, C.F., Han, T.X., Chen, W.F., Sui, X.H. & Chen, W.X. (2008) Rhizobium miluonense sp. nov., a symbiotic bacterium isolated from Laspedeza root nodules. International Journal of Systematic and Evolutionary Microbiology, 58, 1364-1368.
14. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
15. Han, T.X., Wand, E.T., Wu, L.J., Chen, W.F., Gu, J.G., Gu, C.T., Tian, C.F. & Chen, W.X. (2008) Rhizobium multihospitum sp. nov., isolated from multiple legume species native of Xinjian, China. International Journal of Systematic and Evolutionary Microbiology, 58, 1693-1699.
16. Hoque, M.S., Broadhurst, L.M. & Thrall, P.H. (2011) Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across south-eastern Australia. International Journal of Systematic and Evolutionary Microbiology, 61, 299-309.
17. Le Maitre, D.C., Gaertner, M., Marchante, E., Ens, E.J., Holmes, P.M., Pauchard, A., O'Farrell, P.J., Rogers, A.M., Blanchard, R., Blignaut, J. & Richardson, D.M. (2011) Impacts of invasive Australian acacias: implications for management and restoration. Diversity and Distributions, 17, 1015-1029.
18. Le Roux, J.J., Brown, G.K., Byrne, M., Ndlovu, J., Richardson, D.M., Thompson, G.D. & Wilson, J.R.U. (2011) Phylogeographic consequences of different introduction histories of invasive Australian Acacia species and Paraserianthes lophantha (Fabaceae). Diversity and Distributions, 17, 861-887.
19. Marques, M.S., Pagano, M. & Scotti, M.R.M.M.L. (2001) Dual inoculation of a woody legume (Centrolobium tomentosum) with rhizobia and mycorrhizal fungi in south-eastern Brazil. Agroforestry Systems, 52, 107-117.
20. Menna, P. & Hungria, M. (2011) Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer. International Journal of Systematic and Evolutionary Microbiology, 61, 3052-3067.
21. Menna, P., Hungria, M., Barcellos, F.G., Bangel, E.V., Hess, P.N. & Martínez-Romero, E. (2006) Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Systematic and Applied Microbiology, 29, 315-332.
22. Moulin, L., Munive, A., Dreyfus, B. & Boivin-Masson, C. (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature, 411, 948-950.
23. Moulin, L., Béna, G., Boivin-Masson, C. & Stepkowski, T. (2004) Phylogenetic analysis of the symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Molecular Phylogenetics and Evolution, 30, 720-732.
24. Parker, M.A. (2001) Mutualism as a constraint on invasion success for legumes and rhizobia. Diversity and Distributions, 7, 125-136.
25. Parker, M.A., Malek, W. & Parker, I.M. (2006) Growth of an invasive legume is symbiont-limited in newly occupied habitats. Diversity and Distributions, 12, 563-571.
26. Parker, M.A., Wurtz, A.K. & Paynter, Q. (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biological Invasions, 9, 127-138.
27. Porter, S.S., Stanton, M.L. & Rice, K.J. (2011) Mutualisms and adaptive divergence: co-invasion of a heterogenous grassland by an exotic legume rhizobia symbiosis. PLoS ONE, 12, e27935.
28. Posoda, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
29. Reinhart, K.O. & Callaway, R.M. (2006) Soil biota and invasive plants. New Phytologist, 170, 445-457.
30. Richardson, D.M., Allsopp, N., D'Antonio, C.M., Milton, S.J. & Rejmánek, M. (2000) Plant invasions - the role of mutualisms. Biological Reviews, 75, 65-93.
31. Richardson, D.M., Carruthers, J., Hui, C., Impson, F.A.C., Robertson, M.P., Rouget, M., Le Roux, J.J. & Wilson, J.R.U. (2011) Human-mediated introductions of Australian acacias - a global experiment in biogeography. Diversity and Distributions, 17, 771-787.
32. Rodríguez, H. & Fraga, R. (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances, 17, 319-339.
33. Rodríguez-Echeverría, S. (2010) Rhizobial hitchhikers from Down Under: invasional meltdown in a plant-bacteria mutualism? Journal of Biogeography, 37, 1611-1622.
34. Rodríguez-Echeverría, S., Chrisóstomo, J.A., Nabais, C. & Freitas, H. (2009) Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biological Invasions, 11, 651-661.
35. Rodríguez-Echeverría, S., Le Roux, J.J., Chrisóstomo, J.A. & Ndlovu, J. (2011) Jack-of-all-trades and master of many? How does associated rhizobial diversity influence colonization success of Australian Acacia species. Diversity and Distributions, 17, 946-957.
36. Romdhane, S.B., Nasr, H., Samba-Mbanye, R., Neyra, M. & Ghorbal, M.H. (2005) Diversity of Acacia tortilis rhizobia as revealed by PCR/RFLP on crushed root nodules in Tunisia. Annals of Microbiology, 55, 249-258.
37. Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
38. Slabbert, E., Kongor, R.Y., Esler, K.J. & Jacobs, K. (2010) Microbial diversity and community structure in Fynbos soil. Molecular Ecology, 19, 1031-1041.
39. Swofford, D.L. (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA.
40. Sy, A., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., Prin, Y., Neyra, M., Gillis, M., Boivin-Masson, C. & Dreyfus, B. (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. Journal of Bacteriology, 183, 214-220.
41. Tan, Z.Y., Kan, F.L., Peng, G.X., Wang, E.T., Reinhold-Hurek, B. & Chen, W.X. (2001) Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China. International Journal of Systematic and Evolutionary Microbiology, 51, 909-914.
42. Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
43. Veena, K. & Poonam, S. (2011) Potential for enhancing lentil (Lens culinaris) productivity by co-inoculation with PSB, plant growth-promoting rhizobacteria and Rhizobium. The Indian Journal of Agricultural Sciences, 81, 932-934.
44. Versalovic, J., Schneider, M., de Bruijin, F.J. & Lupski, J.R. (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cellular Biology, 5, 25-40.
45. Vincent, J. (1970) A manual for the practical study of the root-nodule bacteria. IBP 32 Handbook No. 15. Blackwell, Oxford.
46. Wei, G., Chen, W., Zhu, W., Chen, C., Young, J.P.W. & Bontemps, C. (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiology Ecology, 68, 320-328.
47. Weir, B.S., Turner, S.J., Silvester, W.B., Park, D.C. & Young, J.M. (2004) Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Applied Environmental Microbiology, 70, 5980-5987.
48. Weisburg, W.G., Barns, S.M., Pelletier, D.A. & Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173, 697-703.
49. Wilkinson, H.H. & Parker, M.A. (1996) Symbiotic specialization and the potential for genotypic coexistence in a plant-bacterial mutualism. Oecologia, 108, 361-367.