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Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L.

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Abstract

Allelochemicals defend plants against herbivore and pathogen attack aboveground and belowground. Whether such plant defenses incur ecological costs by reducing benefits from plant mutualistic symbionts is largely unknown. We explored a potential trade-off between inherent plant chemical defense and belowground mutualism with arbuscular mycorrhizal fungi (AMF) in Plantago lanceolata L., using plant genotypes from lines selected for low and high constitutive levels of the iridoid glycosides (IG) aucubin and catalpol. As selection was based on IG concentrations in leaves, we first examined whether IG concentrations covaried in roots. Root and leaf IG concentrations were strongly positively correlated among genotypes, indicating genetic interdependence of leaf and root defense. We then found that root AMF arbuscule colonization was negatively correlated with root aucubin concentration. This negative correlation was observed both in plants grown with monocultures of Glomus intraradices and in plants colonized from whole-field soil inoculum. Overall, AMF did not affect total biomass of plants; an enhancement of initial shoot biomass was offset by a lower root biomass and reduced regrowth after defoliation. Although the precise effects of AMF on plant biomass varied among genotypes, plants with high IG levels and low AMF arbuscule colonization in roots did not produce less biomass than plants with low IG and high AMF arbuscule colonization. Therefore, although an apparent trade-off was observed between high root chemical defense and AMF arbuscule colonization, this did not negatively affect the growth responses of the plants to AMF. Interestingly, AMF induced an increase in root aucubin concentration in the high root IG genotype of P. lanceolata. We conclude that AMF does not necessarily stimulate plant growth, that direct plant defense by secondary metabolites does not necessarily reduce potential benefits from AMF, and that AMF can enhance concentrations of root chemical defenses, but that these responses are plant genotype-dependent.

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References

  • Adler LS, Schmitt J, Bowers MD (1995) Genetic-variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85

    Article  Google Scholar 

  • Ayres RL, Gange AC, Aplin DM (2006) Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size, and size inequality, of Plantago lanceolata L. J Ecol 94:285–294

    Article  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    Article  PubMed  CAS  Google Scholar 

  • Bennett AE, Bever JD (2007) Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218

    Article  PubMed  Google Scholar 

  • Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am Nat 167:141–152

    Article  PubMed  Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc London B 269:2595–2601

    Article  Google Scholar 

  • Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 11:617–624

    Article  Google Scholar 

  • Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J Ecol 94:893–904

    Article  CAS  Google Scholar 

  • Biere A, Marak HB, van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441

    Article  PubMed  Google Scholar 

  • Bowers MD (1991) Iridoid glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic, New York, pp 297–325

    Google Scholar 

  • Brundrett MC, Piche Y, Peterson RL (1984) A new method for observing the morphology of vesicular arbuscular mycorrhizae. Can J Bot 62:2128–2134

    Article  Google Scholar 

  • Croteau R (1987) Biosynthesis and catabolism of monoterpenoids. Chem Rev 87:929–954

    Article  CAS  Google Scholar 

  • Darrow K, Bowers MD (1999) Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. J Chem Ecol 25:1427–1440

    Article  CAS  Google Scholar 

  • Fajer ED, Bowers MD, Bazzaz FA (1992) The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am Nat 140:707–723

    Article  Google Scholar 

  • Fester T, Wray V, Nimtz M, Strack D (2005) Is stimulation of carotenoid biosynthesis in arbuscular mycorrhizal roots a general phenomenon? Phytochemistry 66:1781–1786

    Article  PubMed  CAS  Google Scholar 

  • Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741

    Article  PubMed  CAS  Google Scholar 

  • Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar feeding insects in Plantago lanceolata L. New Phytol 128:79–87

    Article  Google Scholar 

  • Gange AC, Brown VK (2002) Actions and interactions of soil invertebrates and arbuscular mycorrhizal fungi in affecting the structure of plant communities. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Ecological studies 157. Springer, Berlin, pp 321–344

    Google Scholar 

  • Gange AC, Bower E, Brown VK (2002) Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia 131:103–112

    Article  Google Scholar 

  • Goverde M, van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (2000) Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125:362–369

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hol WHG, Macel M, van Veen JA, van der Meijden E (2004) Root damage and aboveground herbivory change concentration and composition of pyrrolizidine alkaloids of Senecio jacobaea. Basic Appl Ecol 5:253–260

    Article  CAS  Google Scholar 

  • Jensen SR (1991) Plant iridoids, their biosynthesis and distribution in angiosperms. In: Harborne JB, Tomas-Barberan FA (eds) Ecological chemistry and biochemistry of plant terpenoids. Clarendon Press, Oxford, pp 133–158

    Google Scholar 

  • Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecol Lett 8:61–69

    Article  Google Scholar 

  • Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595

    Article  Google Scholar 

  • Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 109:465–470

    Article  PubMed  CAS  Google Scholar 

  • Marak HB, Biere A, van Damme JMM (2000) Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J Evol Biol 13:985–996

    Article  CAS  Google Scholar 

  • Marak HB, Biere A, van Damme JMM (2002a) Two herbivore-deterrent iridoid glycosides reduce the in-vitro growth of a specialist but not a generalist pathogenic fungus of Plantago lanceolata L. Chemoecology 12:185–192

    Article  CAS  Google Scholar 

  • Marak HB, Biere A, van Damme JMM (2002b) Systemic, genotype-specific induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (Rob.) Niessel. J Chem Ecol 28:2429–2448

    Article  PubMed  CAS  Google Scholar 

  • Marak HB, Biere A, van Damme JMM (2003) Fitness costs of chemical defense in Plantago lanceolata L.: effects of nutrient and competition stress. Evolution 57:2519–2530

    PubMed  CAS  Google Scholar 

  • Matyssek R, Agerer R, Ernst D, Munch JC, Osswald W, Pretzsch H, Priesack E, Schnyder H, Treutter D (2005) The plant’s capacity in regulating resource demand. Plant Biol 7:560–580

    Article  PubMed  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Mugnier J, Mosse B (1987) Vesicular-arbuscular mycorrhizal infection in transformed root-inducing T-DNA roots grown axenically. Phytopathology 77:1045–1050

    Article  Google Scholar 

  • Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790

    Article  Google Scholar 

  • Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172:35–46

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • Rønsted N, Franzyk H, Molgaard P, Jaroszewski JW, Jensen SR (2003) Chemotaxonomy and evolution of Plantago L. Plant Syst Evol 242:63–82

    Article  Google Scholar 

  • Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiol 108:7–15

    PubMed  CAS  Google Scholar 

  • Simms EL (1992) Costs of plant resistance to herbivory. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, Chicago, pp 393–425

    Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Staddon PL, Fitter AH (2001) The differential vitality of intraradical mycorrhizal structures and its implications. Soil Biol Biochem 33:129–132

    Article  CAS  Google Scholar 

  • Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300:1138–1140

    Article  PubMed  CAS  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganisation in arbuscular mycorrhizal roots. New Phytol 172:22–34

    Article  PubMed  CAS  Google Scholar 

  • Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol 29:1955–1979

    Article  PubMed  CAS  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Toth R, Toth D, Starke D (1990) Vesicular-arbuscular mycorrhizal colonization in Zea mays affected by breeding for resistance to fungal pathogens. Can J Bot 68:1039–1044

    Google Scholar 

  • van der Putten WH (2003) Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280

    Article  Google Scholar 

  • van der Putten WH, Mortimer SR, Hedlund K, van Dijk C, Brown VK, Leps J, Rodriguez-Barrueco C, Roy J, Len TAD, Gormsen D, Korthals GW, Lavorel S, Regina IS, Smilauer P (2000) Plant species diversity as a driver of early succession in abandoned fields: a multi-site approach. Oecologia 124:91–99

    Article  Google Scholar 

  • van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Article  Google Scholar 

  • Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    Article  CAS  Google Scholar 

  • Wurst S, van der Putten WH (2007) Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores. Basic Appl Ecol 8:491–499

    Article  Google Scholar 

Download references

Acknowledgments

We thank Hafiz Maherali, Lewis Melville and Nora Magyara for their support and Richard Bardgett for useful suggestions on an earlier manuscript draft. The research was funded by Netherlands Organization for Scientific Research (NWO; Talent Postdoctoral Scholarship nr. S86-196) and the Natural Sciences and Engineering Research Council of Canada. Publication 4491 Netherlands Institute of Ecology (NIOO-KNAW). We declare that the experiments comply with the current laws of the country in which they were performed.

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Correspondence to Gerlinde Barbra De Deyn.

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Communicated by Julia Koricheva.

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De Deyn, G.B., Biere, A., van der Putten, W.H. et al. Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L.. Oecologia 160, 433–442 (2009). https://doi.org/10.1007/s00442-009-1312-2

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