Location, but not defensive genotype, determines ectomycorrhizal community composition in Scots pine (Pinus sylvestris L.) seedlings

Abstract For successful colonization of host roots, ectomycorrhizal (EM) fungi must overcome host defense systems, and defensive phenotypes have previously been shown to affect the community composition of EM fungi associated with hosts. Secondary metabolites, such as terpenes, form a core part of these defense systems, but it is not yet understood whether variation in these constitutive defenses can result in variation in the colonization of hosts by specific fungal species. We planted seedlings from twelve maternal families of Scots pine (Pinus sylvestris) of known terpene genotype reciprocally in the field in each of six sites. After 3 months, we characterized the mycorrhizal fungal community of each seedling using a combination of morphological categorization and molecular barcoding, and assessed the terpene chemodiversity for a subset of the seedlings. We examined whether parental genotype or terpene chemodiversity affected the diversity or composition of a seedling's mycorrhizal community. While we found that terpene chemodiversity was highly heritable, we found no evidence that parental defensive genotype or a seedling's terpene chemodiversity affected associations with EM fungi. Instead, we found that the location of seedlings, both within and among sites, was the only determinant of the diversity and makeup of EM communities. These results show that while EM community composition varies within Scotland at both large and small scales, variation in constitutive defensive compounds does not determine the EM communities of closely cohabiting pine seedlings. Patchy distributions of EM fungi at small scales may render any genetic variation in associations with different species unrealizable in field conditions. The case for selection on traits mediating associations with specific fungal species may thus be overstated, at least in seedlings.

[1]  J. Hadfield,et al.  Gradients in richness and turnover of a forest passerine's diet prior to breeding: A mixed model approach applied to faecal metabarcoding data , 2020, Molecular ecology.

[2]  J. Silvertown,et al.  Heritable genetic variation but no local adaptation in a pine-ectomycorrhizal interaction , 2020, Mycorrhiza.

[3]  A. Kulmatiski,et al.  Greenhouse- and Field-Measured Plant-Soil Feedbacks Are Not Correlated , 2019, Front. Environ. Sci..

[4]  L. Tedersoo,et al.  Evolutionary history of mycorrhizal symbioses and global host plant diversity. , 2018, The New phytologist.

[5]  R. Henrik Nilsson,et al.  The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications , 2018, Nucleic Acids Res..

[6]  R. Huddleston.  Structure , 2018, Jane Austen's Style.

[7]  Jason D. Hoeksema,et al.  Genetically determined fungal pathogen tolerance and soil variation influence ectomycorrhizal traits of loblolly pine , 2018, Ecology and evolution.

[8]  T. Whitham,et al.  Common garden experiments disentangle plant genetic and environmental contributions to ectomycorrhizal fungal community structure. , 2018, The New phytologist.

[9]  C. Orme,et al.  Environment and host as large-scale controls of ectomycorrhizal fungi , 2018, Nature.

[10]  Kelly A. Carscadden,et al.  Using niche breadth theory to explain generalization in mutualisms. , 2018, Ecology.

[11]  Jason D. Hoeksema,et al.  Accounting for local adaptation in ectomycorrhizas: a call to track geographical origin of plants, fungi, and soils in experiments , 2018, Mycorrhiza.

[12]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[13]  L. J. Lamit,et al.  Tree genotype influences ectomycorrhizal fungal community structure: Ecological and evolutionary implications , 2016 .

[14]  I. Anderson,et al.  Spatial ecology of ectomycorrhizal fungal communities , 2016 .

[15]  Jason D. Hoeksema,et al.  Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis , 2016, BMC Evolutionary Biology.

[16]  K. Garcia,et al.  Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. , 2015, The New phytologist.

[17]  L. Tedersoo,et al.  Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment , 2015, The ISME Journal.

[18]  W. Mohn,et al.  Local adaptation in migrated interior Douglas-fir seedlings is mediated by ectomycorrhizas and other soil factors. , 2015, The New phytologist.

[19]  Matthew S. Zinkgraf,et al.  Tree genotype mediates covariance among communities from microbes to lichens and arthropods , 2015 .

[20]  Andy F. S. Taylor,et al.  Strong altitudinal partitioning in the distributions of ectomycorrhizal fungi along a short (300 m) elevation gradient. , 2015, The New phytologist.

[21]  J. Bever.  Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. , 2015, The New phytologist.

[22]  J. Oldenburger,et al.  Environmental drivers of ectomycorrhizal communities in Europe's temperate oak forests , 2014, Molecular ecology.

[23]  T. Whitham,et al.  Plant genetics and interspecific competitive interactions determine ectomycorrhizal fungal community responses to climate change , 2014, Molecular ecology.

[24]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[25]  S. Jarvis,et al.  Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine , 2013, Global change biology.

[26]  R. Hüttl,et al.  Individual tree genotypes do not explain ectomycorrhizal biodiversity in soil cores of a pure stand of beech (Fagus sylvatica L.) , 2013, Trees.

[27]  R. Finkeldey,et al.  Spatial Patterns of Ectomycorrhizal Assemblages in a Monospecific Forest in Relation to Host Tree Genotype , 2013, Front. Plant Sci..

[28]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[29]  Jason D. Hoeksema,et al.  Geographic divergence in a species-rich symbiosis: interactions between monterey pines and ectomycorrhizal fungi. , 2012, Ecology.

[30]  I. Anderson,et al.  Spatial analysis of ectomycorrhizal fungi reveals that root tip communities are structured by competitive interactions , 2012, Molecular ecology.

[31]  M. Nilsson,et al.  Glasshouse vs field experiments: do they yield ecologically similar results for assessing N impacts on peat mosses? , 2012, The New phytologist.

[32]  S. Abdelgaleil,et al.  Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi , 2012 .

[33]  B. Moore,et al.  Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes? , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  Ronald W. Davis,et al.  A direct comparison of the KB™ Basecaller and phred for identifying the bases from DNA sequencing using chain termination chemistry , 2010, BMC Research Notes.

[35]  N. Barsoum,et al.  Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. , 2010, Ecology letters.

[36]  Pierre Taberlet,et al.  ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases , 2010, BMC Microbiology.

[37]  Jason D. Hoeksema,et al.  Ongoing coevolution in mycorrhizal interactions. , 2010, The New phytologist.

[38]  J. Lennon,et al.  Spatial and temporal ecology of Scots pine ectomycorrhizas. , 2010, The New phytologist.

[39]  T. May,et al.  Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages , 2010, Mycorrhiza.

[40]  Jason D. Hoeksema,et al.  A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. , 2010, Ecology letters.

[41]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[42]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[43]  T. Whitham,et al.  Genetically based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. , 2009, The New phytologist.

[44]  J. Whitaker,et al.  Distribution of monoterpenes between organic resources in upper soil horizons under monocultures of Picea abies, Picea sitchensis and Pinus sylvestris , 2009 .

[45]  L. Eckhardt,et al.  Effects of oleoresins and monoterpenes on in vitro growth of fungi associated with pine decline in the Southern United States , 2009 .

[46]  L. Marczak,et al.  The mutualism-parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. , 2008, Ecology.

[47]  J. Whitaker,et al.  Differential response of ectomycorrhizal and saprotrophic fungal mycelium from coniferous forest soils to selected monoterpenes , 2008 .

[48]  J. Hoeksema,et al.  Geographic structure in a widespread plant–mycorrhizal interaction: pines and false truffles , 2007, Journal of evolutionary biology.

[49]  V. Thoss,et al.  The role of genetic and chemical variation of Pinus sylvestris seedlings in influencing slug herbivory , 2007, Oecologia.

[50]  V. Thoss,et al.  Assessment and Implications of Intraspecific and Phenological Variability in Monoterpenes of Scots Pine (Pinus sylvestris) Foliage , 2007, Journal of Chemical Ecology.

[51]  T. Pennanen,et al.  Ectomycorrhizal community structure varies among Norway spruce (Picea abies) clones. , 2006, The New phytologist.

[52]  R. Mumm,et al.  Direct and indirect chemical defence of pine against folivorous insects. , 2006, Trends in plant science.

[53]  L. Jost.  Entropy and diversity , 2006 .

[54]  H. Blaschke,et al.  Vertical distribution of an ectomycorrhizal community in upper soil horizons of a young Norway spruce (Picea abies [L.] Karst.) stand of the Bavarian Limestone Alps , 2006, Mycorrhiza.

[55]  D. Elston,et al.  Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation , 2005 .

[56]  M. Villar,et al.  Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family , 2005, Mycorrhiza.

[57]  I. Anderson,et al.  Pine microsatellite markers allow roots and ectomycorrhizas to be linked to individual trees. , 2004, The New phytologist.

[58]  P. Grogan,et al.  Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities. , 2004, FEMS microbiology ecology.

[59]  T. Kuyper,et al.  Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. , 2003, The New phytologist.

[60]  J. Pérez‐Moreno,et al.  Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? , 2003, The New phytologist.

[61]  A. Werner,et al.  Concentrations of terpenes in mycorrhizal roots of Scots pine (Pinus sylvestris L.) seedlings grown in vitro , 2002, Acta Physiologiae Plantarum.

[62]  J. Cairney,et al.  Distribution and persistence of Australian Pisolithus species genets at native sclerophyll forest field sites , 2001 .

[63]  A. Dahlberg.  Community ecology of ectomycorrhizal fungi: an advancing interdisciplinary field , 2001 .

[64]  R. Agerer.  Exploration types of ectomycorrhizae , 2001, Mycorrhiza.

[65]  J. Debaud,et al.  Correspondence between genet diversity and spatial distribution of above‐ and below‐ground populations of the ectomycorrhizal fungus Hebeloma cylindrosporum , 2001, Molecular ecology.

[66]  E. Voigt,et al.  Mycorrhizal colonization and phenolic compounds accumulation on roots of Eucalyptus dunnii maiden inoculated with ectomycorrhizal fungi , 2000 .

[67]  J. Cairney,et al.  Molecular investigation of genet distribution and genetic variation of Cortinarius rotundisporus in eastern Australian sclerophyll forests , 1999 .

[68]  B. Dell,et al.  Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex Maiden. , 1994, The New phytologist.

[69]  R. Hiltunen,et al.  Variation and inheritance of terpenes in scots pine , 1989 .

[70]  B. Kinloch,et al.  CALEDONIAN SCOTS PINE: ORIGINS AND GENETIC STRUCTURE. , 1986, The New phytologist.

[71]  J. Trappe,et al.  Patterns of Ectomycorrhizal Host Specificity and Potential among Pacific Northwest Conifers and Fungi , 1982 .

[72]  J. Trappe,et al.  Ectomycorrhizal formation in Eucalyptus. I. Pure culture synthesis, host specificity and mycorrhizal compatibility with Pinus radiata , 1982 .

[73]  S. Krupa,et al.  Studies on Ectomycorrhizae of Pine II. Growth Inhibition of Mycorrhizal Fungi by Volatile Organic Constituents of Pinus silvestris (Scots Pine) Roots , 1971 .

[74]  J. W. Hanover.  Inheritance of 3-Carene Concentration in Pinus monticola , 1966 .

[75]  Ting Yang,et al.  Antifungal activity of monoterpenes against wood white-rot fungi , 2016 .

[76]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[77]  S. Hartley,et al.  The Ecology of Plant Secondary Metabolites: Frontmatter , 2012 .

[78]  B. Moore,et al.  Plant secondary metabolite polymorphisms and the extended chemical phenotype , 2012 .

[79]  Daniel M Durall,et al.  Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. , 2010, The New phytologist.

[80]  J. Whitaker,et al.  Potential for monoterpenes to affect ectomycorrhizal and saprotrophic fungal activity in coniferous forests is revealed by novel experimental system , 2009 .

[81]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[82]  P. Asprelli,et al.  THE GEOGRAPHIC MOSAIC OF COEVOLUTION , 2007 .

[83]  S. D. Cooper,et al.  Scale effects and extrapolation in ecological experiments , 2003 .

[84]  C. White.  The role of monoterpenes in soil nitrogen cycling processes in ponderosa pine , 1991 .

[85]  G. Forrest.  Genotypic Variation among Native Scots Pine Populations in Scotland based on Monoterpene Analysis , 1980 .

[86]  R. Hiltunen.  On variation, inheritance and chemical interrelationships of monoterpenes in scots pine (Pinus silvestris L.). , 1976, Suomalainen Tiedeakatemia toimituksia. Sar. A.4: Biologica.