Rhizobium alters inducible defenses in broad bean, Vicia faba

Edward Brian Mondor, Misty Cree Summers

.

DOI: 10.4236/oje.2011.13007                

Abstract

Conversion of inorganic nitrogen by mutualistic nitrogen-fixing bacteria is essential for plant growth and reproduction, as well as the development of chemical and mechanical defenses. It is unclear, however, how these bacteria alter co-occurring symbioses at higher trophic levels; e.g., extrafloral nectary (EFN) induction, in response to herbivory, to attract defensive mutualists. We hypothesized that plants colonized by nitrogen-fixing bacteria would mount a larger inducible, defensive response than plants lacking symbioses, as defensive traits are costly. We predicted that bean plants, Vicia faba L., harboring Rhizobium leguminosarum bv. viciae Frank would produce more EFNs upon leaf damage, than plants lacking the symbionts, as EFN induction in V. faba is resource-dependent. Here we report that V. faba colonized by R. leguminosarum produced similar numbers of EFNs as did plants without symbionts. Plants with symbionts, however, produced significantly fewer EFNs over 1 week in response to leaf damage, than those without leaf damage. As such, nitrogen-fixing bacteria may not always benefit the host plant, but rather, the utility of these bacteria may be dependent on the prevailing ecological conditions.

Keywords

Extrafloral Nectary; Inducible Defense; Mutualism; Phenotypic Plasticity; Rhizobia

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Chen, H.K. and Thornton, H.G. (1940) The structure of “ineffective” nodules and its influence on nitrogen fixation. Proceedings of the Royal Society of London—Bi- ology, 129, 208-229.
[2]	Graham, P.H. (1998) Symbiotic nitrogen fixation. In: Sylvia, D.M., Fuhrmann, J.J., Hartel, P.G. and Zuberer, D.A. Eds., Principles and applications of soil microbiology. Prentice Hall, Englewood Cliffs, NJ 325-347.
[3]	Arfaoui, A., Sifi, B., El Hassni, M., El Hadrami, I., Bou- dabbous, A. and Cherif, M. (2005) Biochemical analysis of chickpea protection against Fusarium wilt afforded by two Rhizobium isolates. Plant Pathology Journal, 4, 35- 42. doi:10.3923/ppj.2005.35.42
[4]	Mishra, R.P.N., Singh, R.K., Jaiswal, H.K., Kumar, V., and Maurya, S. (2006) Rhizobium-mediated induction of phe- nolics and plant growth promotion in rice (Oryza sativa L.). Current Microbiology, 52, 383-389. doi:10.1007/s00284-005-0296-3
[5]	Mutch, L.A. and Young J.P.W. (2004) Diversity and spe- cificity of Rhizobia leguminosarum biovar viciae on wild and cultivated legumes. Molecular Ecology, 13, 2435- 2444. doi:10.1111/j.1365-294X.2004.02259.x
[6]	Simms, E.L., Taylor, D.L., Povich, J., Shefferson, R.P., Sachs, J.L., Urbina, M. and Tausczik, Y. (2006) An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proceedings of the Royal Society of London—Biology, 273, 77-81.
[7]	Hirsch, A.M., Lum, M.R. and Downie, J.A. (2001) What makes the rhizobia-legume symbiosis so special? Plant Physiology, 127, 1484-1492. doi:10.1104/pp.010866
[8]	Ventorino, V., Chiurazzi, M., Aponte, M., Pepe, O. and Moschetti, G. (2007) Genetic diversity of a natural population of Rhizobium leguminosarum bv. viceae nodulating plants of Vicia faba in the Vesuvian area. Current Microbiology, 55, 512-517. doi:10.1007/s00284-007-9024-5
[9]	Carter, J.M., Gardner, W.K. and Gibson, A.H. (1994) Improved growth and yield of Faba beans (Vicia faba cv. Fiord) by inoculation with strains of Rhizobium leguminosarum biovar. viciae in acid soils in south west Victoria. Australian Journal of Agricultural Research, 45, 613-623. doi:10.1071/AR9940613
[10]	Koptur, S. (1992) Interactions between insects and plants mediated by extrafloral nectaries. In: Bernays, E. Ed., CRC Series on Insect/Plant Interactions, CRC Press, Bo- ca Raton, 4, 85-132.
[11]	Holldobler, B. and Wilson, E.O. (1990) The ants. Harvard University Press, Cambridge.
[12]	Ness, J.H. (2003) Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia, 134, 210-218.
[13]	Heil, M., Fiala, B., Baumann, B. and Linsenmair, K.E. (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology, 14, 749-757. doi:10.1046/j.1365-2435.2000.00480.x
[14]	Heil, M., Hilpert, A., Fiala, B. and Linsenmair, K.E. (2001) Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia, 126, 404-408. doi:10.1007/s004420000534
[15]	Doak, P., Wagner, D. and Watson A. (2007) Variable extrafloral nectary expression and its consequences in quaking aspen. Canadian Journal of Botany, 85, 1-9. doi:10.1139/b06-137
[16]	Stephenson, A.G. (1982) The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology, 63, 663-669. doi:10.2307/1936786
[17]	Mondor, E.B. and Addicott, J.F. (2003) Conspicuous extra-floral nectaries are inducible in Vicia faba. Ecology Letters, 6, 495-497. doi:10.1046/j.1461-0248.2003.00457.x
[18]	Katayama, N. and Suzuki, N. (2004) Role of extrafloral nectaries of Vicia faba in attraction of ants and herbivore exclusion by ants. Entomological Science, 7, 119-124. doi:10.1111/j.1479-8298.2004.00057.x
[19]	Bugg, R.L. and Ellis, R.T. (1990) Insects associated with cover crops in Massachusetts. Biology, Agriculture and Horticulture, 7, 47-68.
[20]	Mondor, E.B., Tremblay, M.N. and Messing, R.H. (2006) Extrafloral nectary phenotypic plasticity is damage- and resource-dependent in Vicia faba. Biology Letters, 2, 583- 585. doi:10.1098/rsbl.2006.0527
[21]	Rogers, W.E., Siemann, E. and Lankau, R. (2003) Damage induced production of extrafloral nectaries in native and invasive seedlings of Chinese tallow tree (Sapium sebiferum). American Midland Naturalist, 149, 413-417. doi:10.1674/0003-0031(2003)149[0413:DIPOEN]2.0.CO;2
[22]	Pulice, C.E. and Packer, A.A. (2008) Simulated herbivory induces extrafloral nectary production in Prunus avium. Functional Ecology, 22, 801-807. doi:10.1111/j.1365-2435.2008.01440.x
[23]	Bentley, B.L. (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics, 8, 407-427. doi:10.1146/annurev.es.08.110177.002203
[24]	Baldwin, I.T. (1998) Jasmonate-Induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the USA, 95, 8113-8118. doi:10.1073/pnas.95.14.8113
[25]	SAS Institute Inc. (2005) JMP start statistics, 3rd Edition. Brooks/Cole-Thomson, Belmont.
[26]	Burdon, J.J., Gibson, A.H., Searle, S.D., Woods, M.J. and 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. doi:10.1046/j.1365-2664.1999.00409.x
[27]	Denison, R.F. (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist, 156, 567-576. doi:10.1086/316994
[28]	Simms, E.L. and Taylor D.L. (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integrative and Comparative Biology, 42, 369-380. doi:10.1093/icb/42.2.369
[29]	Suzuki, S., Toshihiro, A., Kyung-Bum, L., Tadahiro, S., Chi-Te, L., Hiroki, M., Seiji, W., Taichiro, I. and Hiroshi O. (2007) Rhizobial factors required for stem nodule maturation and maintenance in Sesbania rostrata-Azorhi- zobium caulinodans ORS571 symbiosis. Applied and En- vironmental Microbiology, 73, 6650-6659. doi:10.1128/AEM.01514-07
[30]	Bascompte, J., Jordano, P., Melian, C.J. and Olesen, J.M. (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences of the USA, 100, 9383-9387. doi:10.1073/pnas.1633576100
[31]	Sprent, J.I., Sutherland, J.M. and de Faria, S.M. (1987) Some aspects of the biology of nitrogen-fixing organisms. Philosophical Transactions of the Royal Society—Bio- logical Sciences, 317, 111-129.
[32]	Kirizii, D.A., Vorobei, N.A. and Kots, S.Y. (2007) Relationships between nitrogen fixation and photosynthesis as the main components of the productivity in alfalfa. Russian Journal of Plant Physiology, 54, 589-594. doi:10.1134/S1021443707050032
[33]	Walters, D. and Heil, M. (2007) Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology, 71, 3-17. doi:10.1016/j.pmpp.2007.09.008
[34]	Zangerl, A.R., Hamilton, J.G., Miller, T.J., Crofts, A.R., Oxborough, K., Berenbaum, M.R. and de Lucia, E.H. (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences of the USA, 99, 1088-1091. doi:10.1073/pnas.022647099
[35]	Baldwin, I.T., Kessler, A. and Halitschke, R. (2002) Vo- latile signaling in plant-plant-herbivore interactions: What is real? Current Opinions in Plant Biology, 5, 351-354. doi:10.1016/S1369-5266(02)00263-7
[36]	Karban, R. (2008) Plant behaviour and communication. Ecology Letters, 11, 727-739. doi:10.1111/j.1461-0248.2008.01183.x
[37]	Djordjevic, M.A., Gabriel, D.W. and Rolfe, B.G. (1987) Rhizobium—The refined parasite of legumes. Annual Review of Phytopathology, 25, 145-168. doi:10.1146/annurev.py.25.090187.001045
[38]	Lodeiro, A.R., Lopez-Garcia, S.L., Althabegoiti, M.J., Mon- giardini, E.J., Perez-Gimenez, J. and Quelas, J.I. (2004) Parasitic traits and plant defenses in the rhizobia-legume symbiosis. Recent Research Developments in Plant Pathology, 3, 125-166.
[39]	Denison, R.F. and Kiers, E.T. (2004) Why are most rhizobia beneficial to their host plants, rather than parasitic? Microbes and Infection, 6, 1235-1239. doi:10.1016/j.micinf.2004.08.005
[40]	Laird, R.A. and Addicott, J.F. (2007) Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in Vicia faba. Oecologia, 152, 541-551. doi:10.1007/s00442-007-0676-4
[41]	Janos, D.P. (1980) Vesicular-arbuscular mycorrhizae af- fect lowland tropical rain forest plant growth. Ecology, 61, 151-162. doi:10.2307/1937165
[42]	Koide, R.T. , Shumway, D.L. and Mabon, S.A . (1994) Mycorrhizal fungi and reproduction of field populations of Abutilon theophrasti Medic. (Malvaceae). New Phytologist, 126, 123-130. doi:10.1111/j.1469-8137.1994.tb07537.x
[43]	Gange, A.C. and Smith, A.K. (2005) Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecological Entomology, 30, 600-606. doi:10.1111/j.0307-6946.2005.00732.x
[44]	Wolfe, B.E., Husband, B.C. and Klironomos, J.N. (2005) Effects of a belowground mutualism on an aboveground mutualism. Ecology Letters, 8, 218-223. doi:10.1111/j.1461-0248.2004.00716.x
[45]	Yamamuram N. (1996) Evolution of mutualistic symbiosis: A differential equation model. Population Ecology, 38, 211-218. doi:10.1007/BF02515729
[46]	Hoeksemam J.D. and Bruna, E.M. (2004) Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia, 125, 321-330.
[47]	Neuhauser, C. and Fargione, J.E. (2004) A mutualism- parasitism continuum model and its application to plant- mycorrhizae interactions. Ecological Modelling, 177, 337- 352. doi:10.1016/j.ecolmodel.2004.02.010
[48]	Paszkowski, U. (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Current Opinions in Plant Biology, 9, 364-370. doi:10.1016/j.pbi.2006.05.008