Abstract
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.
Similar content being viewed by others
References
Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397. doi:10.1016/j.cub.2010.02.052
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
Ballhorn DJ, Kautz S, Heil M, Hegeman AD (2009a) Analyzing plant defenses in nature. Plant Signal Behav 4:743–745
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
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 84:65–71
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
Bazzaz FA, Chiariello NR, Coley FD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67. doi:10.2307/1310178
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
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
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 24:1637–1643
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
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
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
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
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
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
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 657–670
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
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
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
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
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
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
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
Eilmus S (2009) Diversität und Funktionen der mit der Ameisengattung Pseudomyrmex (Lund, 1831) assoziierten Bakterien. PhD thesis, Universität Duisburg-Essen, Essen, Germany
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
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
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
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
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
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
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
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
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
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
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
Heil M, Silva Bueno JC (2007) Herbivore-induced volatiles as rapid signals in systemic plant responses. Plant Signal Behav 2:191–193
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
Huelsenbeck JP, Ronquist F (2001) MR BAYES, Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754
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 45–63
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
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
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
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
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
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
Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defences. Ecology 83:176–190. doi:10.2307/2680130
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
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
Lange K (1999) Numerical analysis for statisticians. Springer, New York
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
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
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
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
Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236. doi:10.1126/science.304.5668.234
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
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
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
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
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
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 243–247
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
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 41:391–398
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
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
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
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
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
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
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
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
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
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
Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721. doi:10.1038/385718a0
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
Sprent JI (2001) Nodulation in legumes. Kew Royal Botanical Gardens, Kew
Sprent JI, Sprent P (1990) Nitrogen-fixing organisms: pure and applied aspects. Chapman and Hall, London
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
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 57:19–28
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
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
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
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
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
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
Walters D (2011) Plant defense: warding off attack by pathogens, herbivores, and parasitic plants. Wiley, Oxford
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton
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
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
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 Austin
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Roland Brandl.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ballhorn, D.J., Kautz, S. & Schädler, M. Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172, 833–846 (2013). https://doi.org/10.1007/s00442-012-2539-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-012-2539-x