Abstract
Individual plants typically interact with multiple mutualists and enemies simultaneously. Plant roots encounter both arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi, while the leaves are exposed to herbivores. AMF are usually beneficial symbionts, while the functional role of DSE is largely unknown. Leaf herbivory may have a negative effect on root symbiotic fungi due to decreased carbon availability. However, evidence for this is ambiguous and no inoculation-based experiment on joint effects of herbivory on AM and DSE has been done to date. We investigated how artificial defoliation impacts root colonization by AM (Glomus intraradices) and DSE (Phialocephala fortinii) fungi and growth of Medicago sativa host in a factorial laboratory experiment. Defoliation affected fungi differentially, causing a decrease in arbuscular colonization and a slight increase in DSE-type colonization. However, the presence of one fungal species had no effect on colonization by the other or on plant growth. Defoliation reduced plant biomass, with this effect independent of the fungal treatments. Inoculation by either fungal species reduced root/shoot ratios, with this effect independent of the defoliation treatments. These results suggest AM colonization is limited by host carbon availability, while DSE may benefit from root dieback or exudation associated with defoliation. Reductions in root allocation associated with fungal inoculation combined with a lack of effect of fungi on plant biomass suggest DSE and AMF may be functional equivalent to the plant within this study. Combined, our results indicate different controls of colonization, but no apparent functional consequences between AM and DSE association in plant roots in this experimental setup.
Similar content being viewed by others
References
Ba L, Ning J, Wang D, Facelli E, Facelli JM, Yang Y, Zhang L (2012) The relationship between the diversity of arbuscular mycorrhizal fungi and grazing in a meadow steppe. Plant Soil 352:143–156
Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753
Bécard G, Kosuta S, Tamasloukht M, Séjalon-Delmas N, Roux C (2004) Partner communication in the arbuscular mycorrhizal interaction. Can J Bot 8:1186–1197
Borowicz VA (2013) The impact of arbuscular mycorrhizal fungi on plant growth following herbivory: a search for pattern. Acta Oecol 52:1–9
Cahill JF, McNickle GG (2011) The behavioral ecology of nutrient foraging by plants. Annu Rev Ecol Syst 42:289–311
Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark septate, root endophytes. Mycologia 92:230–232
Daft MJ, El Giahmi AA (1978) Effects of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts. New Phytol 80:365–372
De Deyn GB, Quirk H, Oakley S, Ostle NJ, Bardgett RD (2011) Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences 8:1131–1139
Denef K, Roobroeck D, Wadu MCWM, Lootens P, Boeckx P (2009) Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils. Soil Biol Biochem 41:144–153
Douds DD (2002) Increased spore production by Glomus intraradices in the split-plate monoxenic culture system by repeated harvest, gel replacement, and resupply of glucose to the mycorrhiza. Mycorrhiza 12:163–167
Garcia I, Maedoza R, Pomar MC (2012) Arbuscular mycorrhizal symbiosis and dark septate endophytes under contrasting grazing modes in the Magellanic steppe of Tierra del Fuego. Agr Ecosyst Environ 155:194–201
Gehring CA, Whitman TG (1994) Interactions between above ground herbivores and the mycorrhizal mutualists of plants. TREE 9:251–255
Gehring CA, Whitman TG (2002) Mycorrhizae–herbivore interactions: population and community consequences. In: van der Heijden M, Sanders I (eds) Mycorrhizal ecology. Springer, Berlin, pp 295–320
Guitian R, Bardgett RD (2000) Plant and soil microbial responses to defoliation in temperate semi-natural grassland. Plant Soil 220:271–277
Hamilton EW III, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873
Idjo M, Schtickzelle N, Cranenbrouck S, Declerck S (2010) Do arbuscular mycorrhizal fungi with contrasting life-history strategies differ in their responses to repeated defoliation? FEMS Microbiol Ecol 72:114–122
Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83
Jakobsen I, Smith SE, Smith FA (2002) Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In: van der Heijden M, Sanders I (eds) Mycorrhizal ecology. Springer, Berlin, pp 75–91
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585
Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root colonizing fungi. New Phytol 140:295–310
Klironomos JN, McCune J, Moutoglis P (2004) Species of arbuscular mycorrhizal fungi affect mycorrhizal responses to simulated herbivory. Appl Soil Ecol 26:133–141
Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions. Ecol Lett 8:61–69
Lamb EG, Cahill JF (2008) When competition does not matter: grassland diversity and community composition. Am Nat 171:777–787
Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189
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
Medina-Roldán E, Arredondo JT, Huber-Sannwald E, Chapa-Vargas L, Olalde-Portugal V (2008) Grazing effects on fungal root symbionts and carbon and nitrogen storage in a shortgrass steppe in Central Mexico. J Arid Env 72:546–556
Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793
Phillips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Pietikäinen A, Kytoviita M-M, Vuoti U (2005) Mycorrhiza and seedling establishment in a subarctic meadow: effects of fertilization and defoliation. J Veg Sci 16:175–182
Piippo S, Markkola AM, Härmä E, Tuomi J (2011) Do compensatory shoot growth and mycorrhizal symbionts act as competing above- and below-ground sinks after simulated grazing? Plant Ecol 212:33–42
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315
Reininger V, Grünig CR, Sieber TN (2012) Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Env Microbiol 14:1064–1076
Ruotsalainen AL, Eskelinen A (2011) Root fungal symbionts interact with mammalian herbivory, soil nutrient availability and specific habitat conditions. Oecol 166:807–817
Ruotsalainen AL, Vare H, Vestberg M (2002) Seasonality of root fungal colonization in low-alpine herbs. Mycorrhiza 12:29–36
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Tellenbach C, Grünig CR, Sieber TN (2011) Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Env Microbiol 13:2508–2517
Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K et al (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769
Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11
Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect their allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990–2010. Mycorrhiza 22:227–235
Zhang Q, Zhang L, Weiner J, Tang J, Chen X (2011) Arbuscular mycorrhizal fungi alter plant allometry and biomass–density relationships. Ann Bot 107:407–413
Acknowledgments
We are grateful for Prof. Randolph Currah and for Dr. Melissa Piercey for their expertise with the fungal inocula. MSc Karoliina Huusko is thanked for microscopy and other technical assistance. The project was financed by the Academy of Finland, project no. 133889 (KS) and no. 122092 (ALR) and Kone Foundation (KS).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Saravesi, K., Ruotsalainen, A.L. & Cahill, J.F. Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa . Mycorrhiza 24, 239–245 (2014). https://doi.org/10.1007/s00572-013-0536-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-013-0536-5