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The effects of fungal root endophytes on plant growth: a meta-analysis

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Abstract

Fungal root endophytes are plant associates that colonize root tissue internally without causing any obvious harm to their host. Although ubiquitous, this relationship is not well understood. Our objectives were to determine the effects of fungal root endophyte inoculation on plant biomass and nitrogen concentration by conducting an extensive meta-analysis. We also explored the effects of experimental conditions on the host–endophyte relationship. We performed analyses weighted with non-parametric variance on plant response to root endophytes from the Ascomycetes (excluding the Clavacipitaceae), including categorical analyses of 21 experimental factors, ranging from the identity of the host and the endophyte, to the composition of the growing medium. The response of total biomass to endophyte inoculation was 18 % lower than non-inoculated controls, while individually, root biomass, shoot biomass, and nitrogen concentration responses to endophyte inoculation were neutral. The identities of both the host and the endophyte had an influence, as did the original source of the endophyte (whether or not the isolate used originated from the same host species). Experimental conditions also influenced the plant–endophyte relationship, with the most important being the availability and sources of carbon and organic nitrogen, particularly peat moss. Although our analysis demonstrates that overall plant biomass and nitrogen concentration responses to ascomycetous root endophyte inoculation is neutral to negative, these results are somewhat confounded by among-study differences in experimental conditions, which undoubtedly contribute to the high levels of variability in plant response seen in the literature.

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References

  • Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13

    Article  Google Scholar 

  • Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868

    Article  PubMed  CAS  Google Scholar 

  • Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470

    Article  CAS  Google Scholar 

  • Arnqvist G, Wooster D (1995a) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10:236–240

    Article  PubMed  CAS  Google Scholar 

  • Arnqvist G, Wooster D (1995b) Reply from G. Arnqvist and D. Wooster. Trends Ecol Evol 10:460–461

    Article  Google Scholar 

  • Bajwa R, Abuarghub S, Read DJ (1985) The biology of mycorrhiza in the Ericaceae X: the utilization of proteins and the production of proteolytic enzymes by the mycorrhizal endophyte and by mycorrhizal plants. New Phytol 101:469–486

    Article  CAS  Google Scholar 

  • Brenn N, Menkis A, Grünig CR, Sieber TN, Holdenrieder O (2008) Community structure of Phialocephala fortinii s. lat. in European tree nurseries, and assessment of the potential of the seedlings as dissemination vehicles. Mycol Res 112:650–662

    Article  PubMed  CAS  Google Scholar 

  • Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 179–190

    Chapter  Google Scholar 

  • Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 92:230–232

    Article  Google Scholar 

  • Cameron SL (1998) Colonization of Populus tremuloides seedlings by the fungus Phialocephala fortinii in the presence of the ectomycorrhizal fungus Thelephora terrestris. M.Sc. Thesis, The University of Guelph, Guelph, Ont

  • Davet P, Rouxel F (2000) Detection and isolation of soil fungi. Science, Enfield

    Google Scholar 

  • Grünig CR, McDonald BA, Sieber TN, Rogers SO, Holdenrieder O (2004) Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fungal Genet Biol 41:676–687

    Article  PubMed  Google Scholar 

  • Grünig CR, Duò A, Sieber TN, Holdenrieder O (2008a) Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.–Acephala applanata species complex. Mycologia 100:47–67

    Article  PubMed  Google Scholar 

  • Grünig CR, Queloz V, Sieber TN, Holdenrieder O (2008b) Dark septate endophytes (DSE) of the Phialocephala fortinii s.l.–Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany 86:1355–1369

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149

    Article  Google Scholar 

  • Hashimoto Y, Hyakumachi M (2001) Effects of isolates of ectomycorrhizal fungi and endophytic Mycelium radicis atrovirens that were dominant in soil from disturbed sites on growth of Betula platyphylla var. japonica seedlings. Ecol Res 16:117–125

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310

    Article  Google Scholar 

  • Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265

    Article  CAS  Google Scholar 

  • Karst J, Marczak L, Jones MD, Turkington R (2008) The mutualism–parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. Ecology 4:1032–1042

    Article  Google Scholar 

  • Kernaghan G, Patriquin G (2011) Host associations between fungal root endophytes and boreal trees. Microb Ecol 62:460–473

    Article  PubMed  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Lajeunesse MJ, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecol Lett 6:448–454

    Article  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol:173–189

  • Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102(4):813–821

    Article  PubMed  Google Scholar 

  • Marx DH, Zak B (1965) Effect of pH on mycorrhizal formation of slash pine in aseptic culture. For Sci 11:66–75

    Google Scholar 

  • Mayerhofer MS (2011) Fungal root endophytes and host plant growth. M. Sc. Thesis, Saint-Mary's University, Halifax, N.S

  • Melin E (1922) On the mycorrhizas of Pinus silvestris L. and Picea abies Karst: a preliminary note. J Ecol 9:254–257

    Article  Google Scholar 

  • Mucciarelli M, Scannerini S, Bertea CM, Maffei M (2002) An ascomycetous endophyte isolated from Mentha piperita L.: biological features and molecular studies. Mycologia 94:28–39

    Article  PubMed  Google Scholar 

  • Newsham KK (1999) Phialophora graminicola, a dark septate fungus, is a beneficial associate of the grass Vulpia ciliata spp. ambigua. New Phytol 144:517–524

    Article  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 10:783–793

    Article  Google Scholar 

  • Perez-Naranjo JC (2009) Dark septate and arbuscular mycorrhizal fungal endophytes in roots prairie grass. Ph.D. Thesis, University of Saskatoon, Saskatoon

  • Queloz V, Grünig CR, Sieber TN, Holdenrieder O (2005) Monitoring the spatial and temporal dynamics of a community of the tree-root endophyte Phialocephala fortinii s.l. New Phytol 168:651–660

    Article  PubMed  Google Scholar 

  • 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. Environ Microbiol 14:1064–1076

    Article  PubMed  Google Scholar 

  • Richard C, Fortin A (1974) Distribution géographique, écologie, physiologie, pathogenicité et sporulation du Mycelium radicis atrovirens. Phytoprotection 55:67–88

    Google Scholar 

  • Richard C, Fortin J-A, Fortin A (1971) Protective effect of an ectomycorrhizal fungus against the root pathogen Mycelium radicis atrovirens. Can J For Res 1:246–251

    Article  Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis, version 2. Sinauer Associates, Sunderland

    Google Scholar 

  • Ruotsalainen AL, Kytöviita M-M (2004) Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. Oecologia 140:226–233

    Article  PubMed  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Schulz B (2006) Mutualistic interactions with fungal root endophytes. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 261–279

    Chapter  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004

    Article  CAS  Google Scholar 

  • Sieber TN, Grünig CR (2006) Biodiversity of fungal root-endophyte communities and populations, in particular of the dark septate endophyte Phialocephala fortinii s.l. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 107–132

    Chapter  Google Scholar 

  • Stoyke G, Currah RS (1993) Resynthesis in pure culture of a common sub-alpine fungus–root association using Phialocephala fortinii and Menziesia ferruginea (Ericaceae). Arct Alp Res 25:189–193

    Article  Google Scholar 

  • Summerbell RC (2005) Root endophyte and mycorrhizosphere fungi of black spruce, Picea mariana, in a boreal forest habitat: influence of site factors on fungal distributions. Stud Mycol 53:121–145

    Article  Google Scholar 

  • Tellenbach C, Grunig CR, Sieber TN (2011) Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environ Microbiol 13:2508–2517

    Article  PubMed  Google Scholar 

  • Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11

    Article  PubMed  Google Scholar 

  • Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184

    Article  PubMed  CAS  Google Scholar 

  • Usuki F, Narisawa K, Yonezawa M, Kakishima M, Hashiba T (2002) An efficient inoculation method for colonization of Chinese cabbage seedlings by the root endophytic fungus Heteroconium chaetospira. J Gen Plant Pathol 68:326–332

    Article  Google Scholar 

  • Varma A, Verma S, Sudha Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    PubMed  CAS  Google Scholar 

  • Wilcox HE, Wang CJK (1987) Mycorrhizal and pathological associations of dematiaceous fungi in roots of 7-month-old tree seedlings. Can J For Res 17:884–899

    Article  Google Scholar 

  • Wu L-Q, Guo S-X (2008) Interaction between an isolate of dark-septate fungi and its host plant Saussurea involucrata. Mycorrhiza 18:79–85

    Article  PubMed  CAS  Google Scholar 

  • Wu LQ, Lv YL, Meng ZX, Chen J, Guo SX (2010) The promoting role of an isolate of dark-septate fungus on its host plant Saussurea involucrata Kar. et Kir. Mycorrhiza 20:127–135

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Tang M, Chen H, Wang Y (2012) Effects of a dark-septate endophytic isolate LBF-2 on the medicinal plant Lycium barbarum L. J Microbiol 50:91–96

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank the National Sciences and Engineering Research Council of Canada and Saint Mary’s University, Halifax, NS, who provided financial support for this project. We also appreciate helpful comments from anonymous reviewers.

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Correspondence to Gavin Kernaghan.

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Online Resource 1

List of factors and categories used for the categorical analyses (PDF 18 kb)

Online Resource 2

Detailed list of data collected for all the studies used to conduct the meta-analysis, including publication from which the studies were extracted, values for the 21 factors used in the analyses as well as values for sample sizes and response ratios (XLSX 87 kb)

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Mayerhofer, M.S., Kernaghan, G. & Harper, K.A. The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23, 119–128 (2013). https://doi.org/10.1007/s00572-012-0456-9

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