Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae?

Ecology

Volumn 94, Issue 9, 2013, Pages 2019-2029

  Duhamel, Marie ^a,b   Pel, Roel ^b   Ooms, Astra ^b   Bucking, Heike ^c   Jansa, Jan ^d   Ellers, Jacintha ^b   Van Straalen, Nico M ^b   Wouda, Tjalf ^b   Vandenkoornhuyse, Philippe ^a   Kiers, E Toby ^b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c SOUTH DAKOTA STATE UNIVERSITY   (United States)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Cooperation; Defense; Folsomia candida; Glomus sp.; Mutualism; Networks; Plantago lanceolata; Species interactions; Symbiosis

Indexed keywords

ABUNDANCE; ARBUSCULAR MYCORRHIZA; BIOMASS; COOPERATIVE BEHAVIOR; DEFENSE BEHAVIOR; DICOTYLEDON; EVOLUTIONARILY STABLE STRATEGY; FUNGUS; HOST PLANT; SECONDARY METABOLITE; SYMBIOSIS; TRITROPHIC INTERACTION;

ANIMAL; ARTICLE; FEEDING BEHAVIOR; FUNGUS HYPHAE; INSECT; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANTAGO; SYMBIOSIS;

ANIMALS; FEEDING BEHAVIOR; HYPHAE; INSECTS; MYCORRHIZAE; PLANTAGO; SYMBIOSIS;

EID: 84884824426     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/12-1943.1     Document Type: Article

References (80)

1. Afkhami, M. E., and J. A. Rudgers. 2009. Endophyte-mediated resistance to herbivores depends on herbivore identity in the wild grass Festuca subverticillata. Environmental Entomology 38:1086-1095.
2. Alkan, N., V. Gadkar, O. Yarden, and Y. Kapulnik. 2006. Analysis of quantitative interactions between two species of Arbuscular Mycorrhizal Fungi, Glomus mossae and G. intraradices, by real-time PCR. Applied and Environmental Microbiology 72:4192-4199. (Pubitemid 43894886)
3. Aly, A. H., A. Debbab, J. Kjer, and P. Proksch. 2010. Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Diversity 41:1-16.
4. Bago, B., P. E. Pfeffer, and Y. Shachar-Hill. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124:949-957.
5. Bakonyi, G., K. Posta, I. Kiss, M. Fabian, P. Nagy, and J. N. Nosek. 2002. Density-dependent regulation of arbuscular mycorrhiza by collembola. Functional Ecology 34:661-664. (Pubitemid 34463494)
6. Barto, E. K., M. Hilker, F. Mueller, B. K. Mohney, J. D. Weidenhamer, and M. C. Rillig. 2011. The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6:e27195.
7. Barton, K. E. 2007. Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. American Journal of Botany 94:56-66. (Pubitemid 46955054)
8. Bascompte, J. 2009. Mutualistic networks. Frontiers in Ecology and the Environment 7:429-436.
9. Biere, A., H. M. Marak, and J. M. M. van Damme. 2004. Plant chemical defense against herbivores and pathogens: generalized defense or trade offs? Oecologia 140:430-441. (Pubitemid 39147382)
10. Bollmann, J., M. Elmer, J. Wollecke, S. Raidl, and R. F. Huttl. 2010. Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiologia 53:107-114.
11. Bowers, M. D., S. K. Collinge, S. F. Gamble, and J. Schmitt. 1992. Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201-207.
12. Bowers, M. D., and G. M. Puttick. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. Journal of Chemical Ecology 14:319-334.
13. Cano, C., A. Bago, and Y. Dalpe. 2009. Glomus custos sp nov., isolated from a naturally heavy metal-polluted environment in southern Spain. Mycotaxon 109:499-515.
14. Darrow, K., and M. D. Bowers. 1997. Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochemical Systematics and Ecology 25:1-11. (Pubitemid 27098338)
15. Darrow, K., and M. D. Bowers. 1999. Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. Journal of Chemical Ecology 25: 1427-1440. (Pubitemid 29297860)
16. De Deyn, G. B., A. Biere, W. H. van der Putten, R. Wagenaar, and J. N. Klironomos. 2009. Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia 160:433-442.
17. Dinda, B., S. Debnath, and Y. Harigaya. 2007. Naturally occurring iridoids: a review. Part 1. Chemical and Pharmaceutical Bulletin 55:159-227.
18. Doner, L. W., and G. Becard. 1991. Solubilization of gellan gels by chelation of cations. Biotechnology Techniques 5:25-28.
19. Fajer, E. D., M. D. Bowers, and F. A. Bazzaz. 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. American Naturalist 140:707-723. (Pubitemid 23396619)
20. Fellbaum, C. R., E. W. Gachomoa, Y. Beesetty, S. Choudhari, G. D. Strahan, P. E. Pfeffer, E. T. Kiers, and H. Bucking. 2012. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences USA 109:2666-2671.
21. Field, B., F. Jordan, and A. Osbourn. 2006. Tansley review: First encounters-deployment of defence-related natural products by plants. New Phytologist 172:193-207. (Pubitemid 44414108)
22. Fleetwood, D. J., B. Scott, G. A. Lane, A. Tanaka, and R. D. Johnson. 2007. A complex ergovaline gene cluster in Epichloe endophytes of grasses. Applied and Environmental Microbiology 73:2571-2579. (Pubitemid 46668750)
23. Fontana, A., M. Reichelt, S. Hempel, J. Gershenzon, and S. B. Unsicker. 2009. The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. Journal of Chemical Ecology 35:833-843.
24. Fountain, M. T., and S. P. Hopkin. 2005. Folsomia candida (Collembola): a "standard" soil arthropod. Annual Review of Entomology 50:201-222. (Pubitemid 40162232)
25. Fuchs, A., and M. D. Bowers. 2004. Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. Journal of Chemical Ecology 30:1723-1724.
26. Gange, A. C. 2000. Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends in Ecology and Evolution 15:369-372.
27. Gange, A. C., and H. M. West. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytologist 128:79-87. (Pubitemid 2144908)
28. Giller, PS. 1996. The diversity of soil communities, the "poor man's tropical rainforest." Biodiversity and Conservation 5:135-168.
29. Harris, K. K., and R. E. J. Boerner. 1990. Effects of belowground grazing by Collembola on growth, mycorrhizal infection, and P uptake of Geranium-robertianum. Plant and Soil 129:203-210.
30. Hishi, T., R. Fujimaki, T. McGonigle, and H. Takeda. 2008. Relationships among fine roots, fungal hyphae and soil microarthropods among different soil microhabitats in a temperate coniferous forest of Chamaecyparis obtusa. European Journal of Soil Biology 44:473-477.
31. Hoagland, D. R., and D. I. Arnon. 1950. The water-culture method for growing plants without soil. Circular 347. University of California Agricultural Experiment Station, Berkeley, California, USA.
32. Johnson, D., M. Krsek, E. M. H. Wellington, A. W. Stott, L. Cole, R. D. Bardgett, D. J. Read, and J. R. Leake. 2005. Soil invertebrates disrupt carbon flow through fungal networks. Science 309:1047. (Pubitemid 41134457)
33. Jonas, J. L., G. W. T. Wilson, P. M. White, and A. Joern. 2007. Consumption of mycorrhizal and saprophytic fungi by Collembola in grassland soils. Soil Biology and Biochemistry 39:2594-2602. (Pubitemid 47077461)
34. Jørgensen, H. B., T. Johansson, B. Canback, K. Hedlund, and A. Tunlid. 2005. Selective foraging of fungi by collembolans in soil. Biology Letters 1:243-246. (Pubitemid 41374942)
35. Kempken, F., and M. Rohlfs. 2010. Fungal secondary metabolite biosynthesis-a chemical defence strategy against antagonistic animals? Fungal Ecology 3:107-114.
36. Kiers, E. T., et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882.
37. Kiers, E. T., T. M. Palmer, A. R. Ives, J. F. Bruno, and J. L. Bronstein. 2010. Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13:1459-1474.
38. Klironomos, J. N., and W. B. Kendrick. 1996. Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biology and Fertility of Soils 21:43-52.
39. Klironomos, J. N., and P. Moutoglis. 1999. Colonization of nonmycorrhizal plants by mycorrhizal neighbours as influenced by the collembolan, Folsomia candida. Biology and Fertility of Soils 29:277-281. (Pubitemid 29358157)
40. Klironomos, J. N., and M. Ursic. 1998. Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Nature 396:69-72.
41. Kuhn, J., E. M. Petterson, B. K. Feld, A. Burse, A. Termonia, J. M. Pasteels, and W. Boland. 2004. Selective transport systems mediate sequestration of plant glucosides in leaf beetles: a molecular basis for adaptation and evolution. Proceedings of the National Academy of Sciences USA 101: 13808-13813. (Pubitemid 39298489)
42. Larsen, J., A. Johansen, S. E. Larsen, L. H. Heckmann, I. Jakobsen, and P. H. Krogh. 2008. Population performance of collembolans feeding on soil fungi from different ecological niches. Soil Biology and Biochemistry 40:360-369. (Pubitemid 350087154)
43. Leake, J. R., D. Johnson, D. P. Donnelly, G. E. Muckle, L. Boddy, and D. J. Read. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany 82:1016-1045. (Pubitemid 39501011)
44. Maherali, H., and J. N. Klironomos. 2007. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746-1748. (Pubitemid 46988549)
45. Maier, W., H. Peipp, T. J. Schmid, V. Wray, and D. Strack. 1995. Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiology 109:465-470.
46. Marak, H. B., A. Biere, and J. M. M. Van Damme. 2000. Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. Journal of Evolutionary Biology 13: 985-996.
47. Marak, H. B., A. Biere, and J. M. M. van Damme. 2002. Two herbivore-deterrent iridoid glycosides reduce the in vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L. Chemoecology 12:185-192. (Pubitemid 36052877)
48. McGonigle, T. P., M. H. Miller, D. G. Evans, G. L. Fairchild, and J. A. Swan. 1990. A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist 115:495-501.
49. Mikkelsen, B. L., S. Rosendahl, and I. Jakobsen. 2008. Underground resource allocation between individual networks of mycorrhizal fungi. New Phytologist 180:890-898.
50. Moore, J. C., R. J. Snider, and L. S. Robertson. 1984. Effects of different management practices on Collembola and Acarina in corn production systems. the effects of no-tillage and Atrazine. Pedobiologia 26:143-152. (Pubitemid 16275805)
51. Palmer, T. M., D. F. Doak, M. L. Stanton, J. L. Bronstein, E. T. Kiers, T. P. Young, J. R. Goheen, and R. M. Pringle. 2010. Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proceedings of the National Academy Sciences USA 107:17234-17239.
52. Pardo, F., F. Perich, L. Villarroel, and R. Torres. 1993. Isolation of verbascoside, an antimicrobial constituent of Buddleja globosa leaves. Journal of Ethnopharmacology 39: 221-222. (Pubitemid 23272441)
53. Parniske, M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature 6:763-775.
54. Petersen, H., and M. Luxton. 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39:288-388.
55. Phillips, J. M., and D. S. Hayman. 1970. Improved procedures for clearing roots and staining parasitic and vesiculararbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55:158-161.
56. R Development Core Team. 2010. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
57. Rasmussen, L. S., C. Rank, and S. R. Jensen. 2006. Transfer of iridoid glycosides from host plant Galium verum to hemiparasitic Euphrasia stricta. Biochemical Systematics and Ecology 34:763-765. (Pubitemid 44108447)
58. Rillig, M. C., and D. L. Mummey. 2006. Mycorrhizas and soil structure. New Phytologist 171:41-53. (Pubitemid 43847063)
59. Rohlfs, M., M. Albert, N. P. Keller, and F. Kempken. 2007. Secondary chemicals protect mould from fungivory. Biology Letters 5:523-525.
60. Rohlfs, M., and A. C. L. Churchill. 2011. Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genetics and Biology 48:23-34.
61. Roze, V. L., A. Chanda, and J. E. Linz. 2011. Compartmentalization and molecular traffic in secondary metabolism: a new understanding of established cellular processes. Fungal Genetics and Biology 48:35-48.
62. Schadler, M., M. Roeder, I. Brand, and D. Matthies. 2005. Is palatability of a root-hemiparasitic plant influenced by its host? Oecologia 146:227-233. (Pubitemid 41547138)
63. Schenck, N. C., and G. S. Smith. 1985. 2 new dimorphic species in the endogonaceae-Glomus-ambisporum and Glomusheterosporum. Mycologia 4:566-574.
64. Schreiner, R. P., and G. J. Bethlenfalvay. 2003. Crop residue and Collembola interact to determine the growth of mycorrhizal pea plants. Biology and Fertility of Soils 39:1-8. (Pubitemid 37519254)
65. Sesterhenn, K., M. Distl, and M. Wink. 2007. Occurrence of iridoid glycosides in in vitro cultures and intact plants of Scrophularia nodosa L. Plant Cell Reports 26:365-371.
66. Smilauerova, M., and P. Smilauer. 2002. Morphological responses of plant roots to heterogeneity of soil resources. New Phytologist 154:703-715. (Pubitemid 34548638)
67. Staaden, S., A. Milcu, M. Rohlfs, and S. Scheu. 2010. Fungal toxins affect the fitness and stable isotope fractionation of Collembola. Soil Biology and Biochemistry 42:1766-1773.
68. Stockinger, H., C. Walker, and A. Schuessler. 2009. 'Glomus intraradices DAOM197198', a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytologist 183:1176-1187.
69. Stout, M. J., K. V. Workman, and S. S. Duffey. 1996. Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomologia Experimentalis et Applicata 79:255-271.
70. Strack, D., T. Fester, B. Hause, W. Schliemann, and M. H. Walter. 2003. Arbuscular mycorrhiza: biological, chemical, and molecular aspects. Journal of Chemical Ecology 29: 1955-1979. (Pubitemid 37158972)
71. Tanaka, A., D. Takemoto, T. Chujo, and B. Scott. 2012. Fungal endophytes of grasses. Current Opinion in Plant Biology 15:462-468.
72. Thonar, C., A. Erb, and J. Jansa. 2012. Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities, marker design, verification, calibration and field validation. Molecular Ecology Resources 12:219-232.
73. Vandenkoornhuyse, P., R. Husband, T. J. Daniell, I. J. Watson, J. M. Duck, A. H. Fitter, and J. P. W. Young. 2002. Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Molecular Ecology 11:1555-1564.
74. Vandenkoornhuyse, P., S. Mahe, P. Ineson, P. Staddon, N. Ostle, J. B. Cliquet, A. J. Francez, A. H. Fitter, and J. P. W. Young. 2007. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proceedings of the National Academy of Sciences USA 104:16970-16975. (Pubitemid 350210974)
75. van der Heijden, M. G. A., R. D. Bardgett, and N. M. van Straalen. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11:296-310. (Pubitemid 351172045)
76. Verbruggen, E., C. El Mouden, J. Jansa, G. Akkermans, H. Bucking, S. A. West, and E. T. Kiers. 2012. Spatial structure and inter-specific cooperation: theory and an empirical test using the mycorrhizal mutualism. American Naturalist 179: E133-E146.
77. Wurst, S., D. Dugassa-Gobena, R. Langel, M. Bonkowski, and S. Scheu. 2004. Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid performance. New Phytologist 163:169-176. (Pubitemid 38826184)
78. Wurst, S., W. Roel, A. Biere, and W. H. Putten. 2010. Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata. Plant and Soil 329:117-126.
79. Wurst, S., N. M. Van Dam, F. Monroy, A. Biere, and W. H. van der Putten. 2008. Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. Journal of Chemical Ecology 34:1360-1367.
80. Yue, Q., C. J. Miller, J. F. White, and M. D. Richardson. 2000. Isolation and characterization of fungal inhibitors from Epichloe festucae. Journal of Agricultural and Food Chemistry 48:4687-4692.