, Volume 172, Issue 3, pp 833–846 | Cite as

Induced plant defense via volatile production is dependent on rhizobial symbiosis

  • Daniel J. BallhornEmail author
  • Stefanie Kautz
  • Martin Schädler
Plant-Animal Interactions - Original Research


Nitrogen-fixing rhizobia can substantially influence plant–herbivore interactions by altering plant chemical composition and food quality. However, the effects of rhizobia on plant volatiles, which serve as indirect and direct defenses against arthropod herbivores and as signals in defense-associated plant–plant and within-plant signaling, are still unstudied. We measured the release of jasmonic acid (JA)-induced volatiles of rhizobia-colonized and rhizobia-free lima bean plants (Fabaceae: Phaseolus lunatus L.) and tested effects of their respective bouquets of volatile organic compounds (VOCs) on a specialist insect herbivore (Mexican bean beetle; Coccinellidae: Epilachna varivestis Mulsant) in olfactometer choice trials. In a further experiment, we showed that VOC induction by JA reflects the plant responses to mechanical wounding and insect herbivory. Following induction with JA, rhizobia-colonized plants released significantly higher amounts of the shikimic acid-derived compounds, whereas the emission of compounds produced via the octadecanoid, mevalonate and non-mevalonate pathways was reduced. These changes affected the choice behavior of beetles as the preference of non-induced plants was much more pronounced for plants that were colonized by rhizobia. We showed that indole likely represents the causing agent for the observed repellent effects of jasmonic acid-induced VOCs of rhizobia-colonized lima bean plants. Our study demonstrates a rhizobia-triggered efficacy of induced plant defense via volatiles. Due to these findings, we interpret rhizobia as an integral part of legume defenses against herbivores.


Above–belowground interactions Legumes Nitrogen fixation Phaseolus lunatus Volatile organic compounds 



S. K. was supported by a postdoctoral fellowship (grant LPDS 2009-29) from the German Academy of Sciences Leopoldina. Startup funds to D. J. B. from Portland State University are gratefully acknowledged. We thank Sascha Eilmus for providing the rhizobial strain used in this study.

Supplementary material

442_2012_2539_MOESM1_ESM.docx (14 kb)
Supplementary Table S1 (DOCX 13 kb)


  1. Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397. doi: 10.1016/j.cub.2010.02.052 CrossRefGoogle Scholar
  2. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect of lima bean (Phaseolus lunatus). J Ecol 96:743–745. doi: 10.1111/j.1365-2745.2008.01404.x CrossRefGoogle Scholar
  3. Ballhorn DJ, Kautz S, Heil M, Hegeman AD (2009a) Analyzing plant defenses in nature. Plant Signal Behav 4:743–745PubMedCrossRefGoogle Scholar
  4. Ballhorn DJ, Kautz S, Heil M, Hegeman AD (2009b) Cyanogenesis of wild lima bean (Phaseolus lunatus L.) is an efficient and direct defense in nature. PLoS ONE e5450. doi: 10.1371/journal.pone.0005450
  5. Ballhorn DJ, Reisdorff C, Pfanz H (2011a) Quantitative effects of enhanced CO2 on jasmonic acid induced plant volatiles of lima bean (Phaseolus lunatus L.). J Appl Bot Food Qual 84:65–71Google Scholar
  6. Ballhorn DJ, Kautz S, Jensen M, Schmitt I, Heil M, Hegeman AD (2011b) Genetic and environmental interactions determine plant defences against herbivores. J Ecol 99:313–326. doi: 10.1111/j.1365-2745.2010.01747.x CrossRefGoogle Scholar
  7. Bazzaz FA, Chiariello NR, Coley FD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67. doi: 10.2307/1310178 CrossRefGoogle Scholar
  8. Bonte D, de Roissart A, Vandegehuchte ML, Ballhorn DJ, de la Peña E (2010) Local adaptation of aboveground herbivores towards plant phenotypes induced by soil biota. PLoS ONE 5:e11174. doi: 10.1371/journal.pone.0011174 PubMedCrossRefGoogle Scholar
  9. Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility—a critical assessment. Plant Soil 174:143–180. doi: 10.1007/BF00032245 CrossRefGoogle Scholar
  10. Brown GC, Prochaska GL, Hildebrand DF, Nordin GL, Jackson DM (1995) Green leaf volatiles inhibit conidial germination of the entomopathogen Pandora neoaphidis (Entomophthorales: Entomophthoraceae). Environ Entomol 24:1637–1643Google Scholar
  11. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72:1605–1611. doi: 10.1016/j.phytochem.2011.04.011 PubMedCrossRefGoogle Scholar
  12. Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368. doi: 10.2307/3544308 CrossRefGoogle Scholar
  13. Chen Y, Schmelz EA, Wäckers F, Ruberson JR (2008) Cotton plant, Gossypium hirsutum L., defense in response to nitrogen fertilization. J Chem Ecol 34:1553–1564. doi: 10.1007/s10886-008-9560-x PubMedCrossRefGoogle Scholar
  14. Cipollini ML, Paulke E, Cipollini DF (2002) Effect of nitrogen and water treatment on leaf chemistry in horsenettle (Solanum carolinense), and relationship to herbivory by flea beetles (Epitrix spp.) and tobacco hornworm (Manduca sexta). J Chem Ecol 28:2377–2398. doi: 10.1023/A:1021494315786 PubMedCrossRefGoogle Scholar
  15. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedjel JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi: 10.1093/nar/gkn879 PubMedCrossRefGoogle Scholar
  16. Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228. doi: 10.1111/j.2006.0030-1299.14928.x CrossRefGoogle Scholar
  17. Corby HDL (1981) The systematic value of leguminous root nodules. In: Polhill RM, Raven PH (eds) Advances in legume systematics, parts 1 and 2. Proceedings of the International Legume Conference, Kew, Surrey, England, vol 2, pp 657–670Google Scholar
  18. D’Alessandro M, Held M, Triponez Y, Turlings TC (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32:2733–2748. doi: 10.1007/s10886-006-9196-7 PubMedCrossRefGoogle Scholar
  19. D’Alessandro M, Brunner V, Von Merey G, Turlings TC (2009) Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J Chem Ecol 35:999–1008. doi: 10.1007/s10886-009-9692-7 PubMedCrossRefGoogle Scholar
  20. D’Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49:194–207. doi: 10.1111/j.1365-313X.2006.02946.x PubMedCrossRefGoogle Scholar
  21. Dean JM, Mescher MC, De Moraes CM (2009) Plant–rhizobia mutualism influences aphid abundance on soybean. Plant Soil 323:187–196. doi: 10.1007/s11104-009-9924-1 CrossRefGoogle Scholar
  22. Digilio MC, Corrado G, Sasso R, Coppola V, Iodice L, Pasquariello M, Bossi S, Maffei ME, Coppola M, Pennacchio F, Rao R, Guerrieri E (2010) Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato. New Phytol 187:1089–1101. doi: 10.1111/j.1469-8137.2010.03314.x PubMedCrossRefGoogle Scholar
  23. Donath J, Boland W (1995) Biosynthesis of acyclic homoterpenes: enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry 39:785–790. doi: 10.1016/0031-9422(95)00082-I CrossRefGoogle Scholar
  24. Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102:933–938. doi: 10.1073/pnas.0407360102 PubMedCrossRefGoogle Scholar
  25. Eilmus S (2009) Diversität und Funktionen der mit der Ameisengattung Pseudomyrmex (Lund, 1831) assoziierten Bakterien. PhD thesis, Universität Duisburg-Essen, Essen, GermanyGoogle Scholar
  26. Fischer K, Fiedler K (2000) Response of the copper butterfly Lycaena tityrus to increased leaf nitrogen in natural food plants: evidence against the nitrogen limitation hypothesis. Oecologia 124:235–241. doi: 10.1007/s004420000365 CrossRefGoogle Scholar
  27. Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP et al (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699. doi: 10.1126/science.277.5326.696 PubMedCrossRefGoogle Scholar
  28. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498. doi: 10.1111/j.1461-0248.2007.01043.x PubMedCrossRefGoogle Scholar
  29. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–734. doi: 10.1111/j.1469-8137.2008.02599.x PubMedCrossRefGoogle Scholar
  30. Fukushima J, Kainoh Y, Honda H, Takabayashi J (2002) Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. J Chem Ecol 28:579–586. doi: 10.1023/A:1014548213671 PubMedCrossRefGoogle Scholar
  31. Gange AC, Brown VK, Aplin DM (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol Lett 6:1051–1055. doi: 10.1046/j.1461-0248.2003.00540.x CrossRefGoogle Scholar
  32. Gouinguené SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307. doi: 10.1104/pp.001941 PubMedCrossRefGoogle Scholar
  33. Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756. doi: 10.1111/j.0307-6946.2004.00644.x CrossRefGoogle Scholar
  34. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95. doi: 10.1046/j.1461-0248.2001.00192.x CrossRefGoogle Scholar
  35. Hampel D, Mosandl A, Wüst M (2005) Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66:305–311. doi: 10.1016/j.phytochem.2004.12.010 PubMedCrossRefGoogle Scholar
  36. Heil M (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J Chem Ecol 30:1289–1295. doi: 10.1023/B:JOEC.0000030299.59863.69 PubMedCrossRefGoogle Scholar
  37. Heil M, Silva Bueno JC (2007) Herbivore-induced volatiles as rapid signals in systemic plant responses. Plant Signal Behav 2:191–193PubMedCrossRefGoogle Scholar
  38. Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617. doi: 10.1016/j.tplants.2006.10.007 PubMedCrossRefGoogle Scholar
  39. Huelsenbeck JP, Ronquist F (2001) MR BAYES, Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi: 10.1093/bioinformatics/17.8.754 PubMedCrossRefGoogle Scholar
  40. Johnson ND, Bentley BL (1991) Symbiotic N2-fixation and the element of plant resistance to herbivores: lupine alkaloids and tolerance to defoliation. In: Barbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant–herbivore interactions. Wiley, New York, pp 45–63Google Scholar
  41. Karban R (2011) Evolutionary ecology of plant defences. The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347. doi: 10.1111/j.1365-2435.2011.01838.x CrossRefGoogle Scholar
  42. Katayama N, Nishida T, Zhang ZQ, Ohgushi T (2010) Belowground microbial symbiont enhances plant susceptibility to a spider mite through change in soybean leaf quality. Popul Ecol 52:499–506. doi: 10.1007/s10144-010-0207-8 CrossRefGoogle Scholar
  43. Katayama N, Zhang ZQ, Ohgushi T (2011) Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol Entomol 36:43–51. doi: 10.1111/j.1365-2311.2010.01242.x CrossRefGoogle Scholar
  44. Kautz S, Lumbsch HT, Ward PS, Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63:839–853. doi: 10.1111/j.1558-5646.2008.00594.x PubMedCrossRefGoogle Scholar
  45. Kempel A, Brandl R, Schädler M (2009) Symbiotic soil microorganisms as players in aboveground plant–herbivore interactions—the role of rhizobia. Oikos 118:634–640. doi: 10.1111/j.1600-0706.2009.17418.x Google Scholar
  46. Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300. doi: 10.1111/j.1365-2435.2009.01647.x CrossRefGoogle Scholar
  47. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defences. Ecology 83:176–190. doi: 10.2307/2680130 CrossRefGoogle Scholar
  48. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097. doi: 10.1890/08-1555.1 PubMedCrossRefGoogle Scholar
  49. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628. doi: 10.1111/j.1365-2745.2006.01120.x CrossRefGoogle Scholar
  50. Lange K (1999) Numerical analysis for statisticians. Springer, New YorkGoogle Scholar
  51. Leitner M, Kaiser R, Rasmussen MO, Driguez H, Boland W, Mithöfer A (2008) Microbial oligosaccharides differentially induce volatiles and signalling components in Medicago truncatula. Phytochemistry 69:2029–2040. doi: 10.1016/j.phytochem.2008.04.019 PubMedCrossRefGoogle Scholar
  52. Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101. doi: 10.1007/s00572-009-0264-z PubMedCrossRefGoogle Scholar
  53. Lerdau M, Coley PD (2002) Benefits of the carbon-nutrient balance hypothesis. Oikos 98:534–536. doi: 10.1034/j.1600-0706.2002.980318.x CrossRefGoogle Scholar
  54. Lou YG, Baldwin IT (2004) Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses to Nicotiana attenuata. Plant Physiol 135:496–506. doi: 10.1104/pp.104.040360 PubMedCrossRefGoogle Scholar
  55. Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236. doi: 10.1126/science.304.5668.234 PubMedCrossRefGoogle Scholar
  56. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280. doi: 10.1016/j.pbi.2006.03.002 PubMedCrossRefGoogle Scholar
  57. Mithöfer A, Maitrejean M, Boland W (2005a) Structural and biological diversity of cyclic octadecanoids, jasmonates, and mimetics. J Plant Growth Regul 23:170–178. doi: 10.1007/s00344-004-0034-2 Google Scholar
  58. Mithöfer A, Wanner G, Boland W (2005b) Effects of feeding Spodoptera littoralis on Lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168. doi: 10.1104/pp.104.054460 PubMedCrossRefGoogle Scholar
  59. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67. doi: 10.1080/10635150490264699 PubMedCrossRefGoogle Scholar
  60. Oono R, Denison RF (2010) Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol 154:1541–1548. doi: 10.1104/pp.110.163436 PubMedCrossRefGoogle Scholar
  61. Ormeño E, Torres R, Mayo J, Rivas R, Peix A, Velázquez E, Zúniga D (2007) Phaseolus lunatus is nodulated by a phosphate solubilizing strain of Sinorhizobium meliloti in a Peruvian soil. In: Velázquez E, Rodriguez-Barrueco C (eds) Development in plant and soil sciences. Springer, The Netherlands, pp 243–247Google Scholar
  62. Ormeño-Orillo E, Vinuesa P, Zúñiga-Dávila D, Martinez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262. doi: 10.1016/j.syapm.2005.09.002 CrossRefGoogle Scholar
  63. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398PubMedCrossRefGoogle Scholar
  64. Paetzold H, Garms S, Bartram S, Wieczorek J, Urós-Gracia E-M, Rodríguez-Concepción M, Boland W, Strack D, Hause B, Walter MH (2010) The isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol Plant 5:904–916. doi: 10.1093/mp/ssq032 CrossRefGoogle Scholar
  65. Paré PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167. doi: 0046-225X/95/1637-1643 PubMedGoogle Scholar
  66. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514. doi: 10.1016/j.tplants.2010.05.007 PubMedCrossRefGoogle Scholar
  67. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. doi: 10.1016/j.pbi.2007.05.004 PubMedCrossRefGoogle Scholar
  68. Rodriguez-Saona C, Thaler JS (2005) The jasmonate pathway alters herbivore feeding behavior: consequences for plant defences. Entomol Exp Appl 115:125–134. doi: 10.1111/j.1570-7458.2005.00277.x CrossRefGoogle Scholar
  69. Rostás M, Turlings TCJ (2008) Induction of systemic acquired resistance in Zea mays also enhances the plant’s attractiveness to parasitoids. Biol Control 46:178–186. doi: 10.1016/j.biocontrol.2008.04.012 CrossRefGoogle Scholar
  70. Schädler M, Roeder M, Brandl R, Matthies D (2007) Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore. Glob Change Biol 13:1005–1015. doi: 10.1111/j.1365-2486.2007.01319.x CrossRefGoogle Scholar
  71. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499. doi: 10.1104/pp.104.047019 PubMedCrossRefGoogle Scholar
  72. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306. doi: 10.1104/pp.103.024174 PubMedCrossRefGoogle Scholar
  73. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA 103:16672–16676. doi: 10.1073/pnas.0607780103 PubMedCrossRefGoogle Scholar
  74. Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721. doi: 10.1038/385718a0 CrossRefGoogle Scholar
  75. Simon J, Gleadow RM, Woodrow IE (2010) Allocation of nitrogen to chemical defence and plant functional traits is constrained by soil N. Tree Physiol 30:1111–1117. doi: 10.1093/treephys/tpq049 PubMedCrossRefGoogle Scholar
  76. Sprent JI (2001) Nodulation in legumes. Kew Royal Botanical Gardens, KewGoogle Scholar
  77. Sprent JI, Sprent P (1990) Nitrogen-fixing organisms: pure and applied aspects. Chapman and Hall, LondonCrossRefGoogle Scholar
  78. Thamer S, Schädler M, Bonte D, Ballhorn DJ (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209–219. doi: 10.1007/s11104-010-0635-4 CrossRefGoogle Scholar
  79. Thies JE, Singleton PW, Bohlool BB (1991) Influence of the size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl Environ Microbiol 57:19–28PubMedGoogle Scholar
  80. Triplett EW, Heitholt JJ, Evensen KB, Blevins DG (1981) Increase in internode length of Phaseolus lunatus L. caused by inoculation with a nitrate reductase-deficient strain of Rhizobium sp. Plant Physiol 67:1–4. doi: 10.1104/pp.67.1.1 PubMedCrossRefGoogle Scholar
  81. Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427. doi: 10.1016/j.pbi.2006.05.010 PubMedCrossRefGoogle Scholar
  82. Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152. doi: 10.1007/s004250050466 CrossRefGoogle Scholar
  83. Van Brussel AAN (1977) The wall of Rhizobium leguminosarum in bacteroid and free-living forms. J Gen Microbiol 101:51–56. doi: 10.1099/00221287-101-1-51 CrossRefGoogle Scholar
  84. Van der Putten WHL, Vet JH, Wäckers F (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554. doi: 10.1016/S0169-5347(01)02265-0 CrossRefGoogle Scholar
  85. von Dahl CC, Baldwin IT (2004) Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuata. Physiol Plant 120:474–481. doi: 10.1080/07357900801975272 CrossRefGoogle Scholar
  86. Walters D (2011) Plant defense: warding off attack by pathogens, herbivores, and parasitic plants. Wiley, OxfordGoogle Scholar
  87. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, PrincetonGoogle Scholar
  88. Winter TR, Rostás M (2010) Nitrogen deficiency affects bottom-up cascade without disrupting indirect plant defense. J Chem Ecol 36:642–651. doi: 10.1007/s10886-010-9797-z PubMedCrossRefGoogle Scholar
  89. Zilli JE, Ribeiro KG, Campo RJ, Hungria M (2009) Influence of fungicide seed treatment on soybean nodulation and grain yield. Rev Bras Ciênc Solo 33:917–923. doi: 10.1590/S0100-06832009000400016 CrossRefGoogle Scholar
  90. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at AustinGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Daniel J. Ballhorn
    • 1
    Email author
  • Stefanie Kautz
    • 2
  • Martin Schädler
    • 3
  1. 1.Department of BiologyPortland State UniversityPortlandUSA
  2. 2.Department of ZoologyField Museum of Natural HistoryChicagoUSA
  3. 3.Department Community EcologyHelmholtz-Centre for Environmental Research-UFZHalleGermany

Personalised recommendations