Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi

Fungi play many essential roles in ecosystems. They facilitate plant access to nutrients and water, serve as decay agents that cycle carbon and nutrients through the soil, water and atmosphere, and are major regulators of macro‐organismal populations. Although technological advances are improving the detection and identification of fungi, there still exist key gaps in our ecological knowledge of this kingdom, especially related to function. Trait‐based approaches have been instrumental in strengthening our understanding of plant functional ecology and, as such, provide excellent models for deepening our understanding of fungal functional ecology in ways that complement insights gained from traditional and ‐omics‐based techniques. In this review, we synthesize current knowledge of fungal functional ecology, taxonomy and systematics and introduce a novel database of fungal functional traits (FunFun). FunFun is built to interface with other databases to explore and predict how fungal functional diversity varies by taxonomy, guild, and other evolutionary or ecological grouping variables. To highlight how a quantitative trait‐based approach can provide new insights, we describe multiple targeted examples and end by suggesting next steps in the rapidly growing field of fungal functional ecology.

[1]  R. Gazis,et al.  Endophytes from wild rubber trees as antagonists of the pathogen Corynespora cassiicola. , 2019, Phytopathology.

[2]  A. Zanne,et al.  Finding fungal ecological strategies: Is recycling an option? , 2019, Fungal Ecology.

[3]  N. Picard,et al.  Climatic controls of decomposition drive the global biogeography of forest-tree symbioses , 2019, Nature.

[4]  R. Kolka,et al.  Melanin mitigates the accelerated decay of mycorrhizal necromass with peatland warming. , 2019, Ecology letters.

[5]  Lynne Boddy,et al.  Handbook for the measurement of macrofungal functional traits: A start with basidiomycete wood fungi , 2018, Functional Ecology.

[6]  D. Hibbett,et al.  Contemporaneous radiations of fungi and plants linked to symbiosis , 2018, Nature Communications.

[7]  M. Rillig,et al.  Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. , 2018, The New phytologist.

[8]  M. Zobel Eltonian niche width determines range expansion success in ectomycorrhizal conifers. , 2018, The New phytologist.

[9]  B. Henrissat,et al.  High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. , 2018, The New phytologist.

[10]  Alejandro Ordonez,et al.  Below-ground biotic interactions moderated the postglacial range dynamics of trees. , 2018, The New phytologist.

[11]  W. Cornwell,et al.  Bridging reproductive and microbial ecology: a case study in arbuscular mycorrhizal fungi , 2018, The ISME Journal.

[12]  Silvio C. E. Tosatto,et al.  The Pfam protein families database in 2019 , 2018, Nucleic Acids Res..

[13]  L. Tedersoo,et al.  Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. , 2018, The New phytologist.

[14]  D. Hibbett,et al.  Evolutionary dynamics of host specialization in wood-decay fungi , 2018, BMC Evolutionary Biology.

[15]  Ebuka S. Arinze,et al.  Impact of Yeast Pigmentation on Heat Capture and Latitudinal Distribution , 2018, Current Biology.

[16]  D. Hibbett,et al.  Phylogenetic taxon definitions for Fungi, Dikarya, Ascomycota and Basidiomycota , 2018, IMA fungus.

[17]  Kessy Abarenkov,et al.  High-level classification of the Fungi and a tool for evolutionary ecological analyses , 2018, Fungal Diversity.

[18]  Hanhong Bae,et al.  Endophytic Trichoderma citrinoviride isolated from mountain-cultivated ginseng (Panax ginseng) has great potential as a biocontrol agent against ginseng pathogens , 2018, Journal of ginseng research.

[19]  Michelle E. Afkhami,et al.  Cooperation and coexpression: How coexpression networks shift in response to multiple mutualists , 2018, Molecular ecology.

[20]  J. Heilmann‐Clausen,et al.  Fungal spore diversity reflects substrate-specific deposition challenges , 2018, Scientific Reports.

[21]  K. Clemmensen,et al.  From mycorrhizal fungal traits to ecosystem properties – and back again , 2018 .

[22]  P. Kennedy,et al.  Melanization of mycorrhizal fungal necromass structures microbial decomposer communities , 2018 .

[23]  B. Sulman,et al.  Interactions among decaying leaf litter, root litter and soil organic matter vary with mycorrhizal type , 2018 .

[24]  K. Treseder,et al.  Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: A trait‐based predictive framework , 2018 .

[25]  T. Cajthaml,et al.  Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling , 2018, The ISME Journal.

[26]  P. Baldrian Microbial enzyme-catalyzed processes in soils and their analysis. A review , 2018 .

[27]  M. Tomšovský,et al.  Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots , 2018, The ISME Journal.

[28]  Andrew Nicholas Miller,et al.  The Mycology Collections Portal (MyCoPortal) , 2017 .

[29]  Josef C. Uyeda,et al.  Rethinking phylogenetic comparative methods , 2017, bioRxiv.

[30]  J. Powell,et al.  Relationships between mycorrhizal type and leaf flammability in the Australian flora , 2017 .

[31]  Jennifer M. Bhatnagar,et al.  Distributions of fungal melanin across species and soils , 2017 .

[32]  Brian J. McGill,et al.  The bien r package: A tool to access the Botanical Information and Ecology Network (BIEN) database , 2017 .

[33]  John J. Wiens,et al.  Inordinate Fondness Multiplied and Redistributed: the Number of Species on Earth and the New Pie of Life , 2017, The Quarterly Review of Biology.

[34]  J. Slot,et al.  Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases. , 2017, Microbiology spectrum.

[35]  Robert Lücking,et al.  Fungal Diversity Revisited: 2.2 to 3.8 Million Species , 2017, Microbiology spectrum.

[36]  T. Crowther,et al.  Applying allometric theory to fungi , 2017, The ISME Journal.

[37]  J. Elser,et al.  Carbon:Nitrogen:Phosphorus Stoichiometry in Fungi: A Meta-Analysis , 2017, Front. Microbiol..

[38]  Anna Norberg,et al.  Measuring and predicting the influence of traits on the assembly processes of wood‐inhabiting fungi , 2017 .

[39]  Daniel S Maynard,et al.  Diversity begets diversity in competition for space , 2017, Nature Ecology &Evolution.

[40]  Natalie Christian,et al.  Chapter 5 A Novel Framework for Decoding Fungal Endophyte Diversity , 2017 .

[41]  P. B. Matheny,et al.  How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. , 2017, The New phytologist.

[42]  J. Heilmann‐Clausen,et al.  Mean spore size and shape in ectomycorrhizal and saprotrophic assemblages show strong responses under resource constraints , 2017 .

[43]  M. Unterseher,et al.  What do we learn from cultures in the omics age? High-throughput sequencing and cultivation of leaf-inhabiting endophytes from beech (Fagus sylvatica L.) revealed complementary community composition but similar correlations with local habitat conditions , 2017 .

[44]  A. Mithöfer Plant carnivory: Pitching to the same target , 2017, Nature Plants.

[45]  P. Kennedy,et al.  Fungal endophytes as priority colonizers initiating wood decomposition , 2017 .

[46]  Mark A. Miller,et al.  T‐BAS: Tree‐Based Alignment Selector toolkit for phylogenetic‐based placement, alignment downloads and metadata visualization: an example with the Pezizomycotina tree of life , 2016, Bioinform..

[47]  D. Hibbett,et al.  Sequence-based classification and identification of Fungi , 2016, Mycologia.

[48]  Francis Martin,et al.  Unearthing the roots of ectomycorrhizal symbioses , 2016, Nature Reviews Microbiology.

[49]  A. Adholeya,et al.  Phylogenetic analyses reveal molecular signatures associated with functional divergence among Subtilisin like Serine Proteases are linked to lifestyle transitions in Hypocreales , 2016, BMC Evolutionary Biology.

[50]  G. May Here come the commensals. , 2016, American journal of botany.

[51]  P. Stevens,et al.  Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis , 2016, The American Naturalist.

[52]  Dehong Hu,et al.  Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta , 2016, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Conrad L. Schoch,et al.  Scaling up discovery of hidden diversity in fungi: impacts of barcoding approaches , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  J. Stajich,et al.  A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data , 2016, Mycologia.

[55]  Jianping Xu Fungal DNA barcoding. , 2016, Genome.

[56]  P. Kirk,et al.  Climate impacts on fungal community and trait dynamics , 2016 .

[57]  K. Peay,et al.  Competition-function tradeoffs in ectomycorrhizal fungi , 2016, PeerJ.

[58]  T. Crowther,et al.  Patterns of natural fungal community assembly during initial decay of coniferous and broadleaf tree logs , 2016 .

[59]  Natalie Christian,et al.  Plant Host and Geographic Location Drive Endophyte Community Composition in the Face of Perturbation , 2016, Microbial Ecology.

[60]  K. Peay,et al.  Dimensions of biodiversity in the Earth mycobiome , 2016, Nature Reviews Microbiology.

[61]  Michelle E. Afkhami,et al.  Native fungal endophytes suppress an exotic dominant and increase plant diversity over small and large spatial scales. , 2016, Ecology.

[62]  Scott T. Bates,et al.  FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild , 2016 .

[63]  D. Hibbett,et al.  Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities. , 2016, Molecular biology and evolution.

[64]  J. Dighton Fungi in Ecosystem Processes, Second Edition , 2016 .

[65]  R. Henrik Nilsson,et al.  Top 50 most wanted fungi , 2016 .

[66]  J. Dighton Fungi in Ecosystem Processes , 2016 .

[67]  Benjamin L Turner,et al.  Shifts in symbiotic associations in plants capable of forming multiple root symbioses across a long‐term soil chronosequence , 2016, Ecology and evolution.

[68]  P. Kennedy,et al.  Revisiting the 'Gadgil effect': do interguild fungal interactions control carbon cycling in forest soils? , 2016, The New phytologist.

[69]  K. Peay,et al.  Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. , 2016, The New phytologist.

[70]  Marcus L. Roper,et al.  Mushrooms use convectively created airflows to disperse their spores , 2016, Proceedings of the National Academy of Sciences.

[71]  Natalia N. Ivanova,et al.  The standard operating procedure of the DOE-JGI Metagenome Annotation Pipeline (MAP v.4) , 2016, Standards in Genomic Sciences.

[72]  S. Lumyong,et al.  Relationships between terrestrial and freshwater lignicolous fungi , 2016 .

[73]  K. Hyde,et al.  Lignicolous freshwater fungi along a north-south latitudinal gradient in the Asian/Australian region; can we predict the impact of global warming on biodiversity and function? , 2016 .

[74]  F. Bärlocher Aquatic hyphomycetes in a changing environment , 2016 .

[75]  G. Newcombe,et al.  Fungal endophytes: modifiers of plant disease , 2015, Plant Molecular Biology.

[76]  M. Bidochka,et al.  Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi , 2015, Plant Molecular Biology.

[77]  R. Tavares,et al.  Soil DNA pyrosequencing and fruitbody surveys reveal contrasting diversity for various fungal ecological guilds in chestnut orchards. , 2015, Environmental microbiology reports.

[78]  J. Schilling,et al.  Comparing lignocellulose physiochemistry after decomposition by brown rot fungi with distinct evolutionary origins. , 2015, Environmental microbiology.

[79]  Jay T. Lennon,et al.  Microbiomes in light of traits: A phylogenetic perspective , 2015, Science.

[80]  D. Hibbett,et al.  Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors , 2015, The New phytologist.

[81]  M. V. D. van der Heijden,et al.  Regulation of resource exchange in the arbuscular mycorrhizal symbiosis , 2015, Nature Plants.

[82]  R. Brandl,et al.  Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles , 2015 .

[83]  Natalie Christian,et al.  Microbiomes: unifying animal and plant systems through the lens of community ecology theory , 2015, Front. Microbiol..

[84]  C. Kuske,et al.  Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland , 2015, Front. Microbiol..

[85]  B. Henrissat,et al.  Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry , 2015 .

[86]  G. Berg,et al.  The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes , 2015, Microbiology and Molecular Reviews.

[87]  Petr Baldrian,et al.  Biotic interactions mediate soil microbial feedbacks to climate change , 2015, Proceedings of the National Academy of Sciences.

[88]  K. Treseder,et al.  Fungal Traits That Drive Ecosystem Dynamics on Land , 2015, Microbiology and Molecular Reviews.

[89]  Michael J. Aspinwall,et al.  BAAD: a Biomass And Allometry Database for woody plants , 2015 .

[90]  Zewei Song,et al.  Signature Wood Modifications Reveal Decomposer Community History , 2015, PloS one.

[91]  R. B. Jackson,et al.  Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. , 2015, The New phytologist.

[92]  E. Kiers,et al.  Order of arrival structures arbuscular mycorrhizal colonization of plants. , 2015, The New phytologist.

[93]  R. Miller,et al.  Mycorrhizal phenotypes and the Law of the Minimum. , 2015, The New phytologist.

[94]  A. Salamov,et al.  Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists , 2015, Nature Genetics.

[95]  P. Baldrian,et al.  Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi , 2015 .

[96]  R. Gazis,et al.  Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea , 2015, Mycologia.

[97]  In-Jung Lee,et al.  Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus , 2015 .

[98]  A. Casadevall,et al.  Microbiology: Ditch the term pathogen , 2014, Nature.

[99]  J. G. Burleigh,et al.  Synthesis of phylogeny and taxonomy into a comprehensive tree of life , 2014, Proceedings of the National Academy of Sciences.

[100]  J. Heilmann‐Clausen,et al.  Communities of wood‐inhabiting bryophytes and fungi on dead beech logs in Europe – reflecting substrate quality or shaped by climate and forest conditions? , 2014 .

[101]  R. Henrik Nilsson,et al.  Global diversity and geography of soil fungi , 2014, Science.

[102]  Juancarlos Chan,et al.  Gene Ontology Consortium: going forward , 2014, Nucleic Acids Res..

[103]  T. Crowther,et al.  Untangling the fungal niche: the trait-based approach , 2014, Front. Microbiol..

[104]  Michelle E. Afkhami,et al.  Mutualist-mediated effects on species' range limits across large geographic scales. , 2014, Ecology letters.

[105]  Ignazio Carbone,et al.  Tissue storage and primer selection influence pyrosequencing‐based inferences of diversity and community composition of endolichenic and endophytic fungi , 2014, Molecular ecology resources.

[106]  M. Rillig,et al.  Ecological understanding of root-infecting fungi using trait-based approaches. , 2014, Trends in plant science.

[107]  Jianchu Xu,et al.  One stop shop: backbones trees for important phytopathogenic genera: I (2014) , 2014, Fungal Diversity.

[108]  J. R. King,et al.  Climate fails to predict wood decomposition at regional scales , 2014 .

[109]  R. Henrik Nilsson,et al.  Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi , 2014, Database J. Biol. Databases Curation.

[110]  A. Salamov,et al.  Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi , 2014, Proceedings of the National Academy of Sciences.

[111]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[112]  M. Heil,et al.  Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. , 2014, FEMS microbiology letters.

[113]  Hsiao-Che Kuo,et al.  Secret lifestyles of Neurospora crassa , 2014, Scientific Reports.

[114]  R. Henrik Nilsson,et al.  Improving ITS sequence data for identification of plant pathogenic fungi , 2014, Fungal Diversity.

[115]  P. Reich The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto , 2014 .

[116]  Matthew W. Pennell,et al.  Functional distinctiveness of major plant lineages , 2014 .

[117]  Jack W. McFarland,et al.  A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning , 2014 .

[118]  R. Koide,et al.  The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress , 2013 .

[119]  Inna Dubchak,et al.  MycoCosm portal: gearing up for 1000 fungal genomes , 2013, Nucleic Acids Res..

[120]  J. Klironomos,et al.  A trait-based framework to understand life history of mycorrhizal fungi. , 2013, Trends in plant science.

[121]  Richard P Phillips,et al.  The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. , 2013, The New phytologist.

[122]  T. Kuyper,et al.  A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. , 2013, FEMS microbiology reviews.

[123]  P. Reich,et al.  New handbook for standardised measurement of plant functional traits worldwide , 2013 .

[124]  Otso Ovaskainen,et al.  Specialist species of wood‐inhabiting fungi struggle while generalists thrive in fragmented boreal forests , 2013 .

[125]  Conrad L. Schoch,et al.  Filling Gaps in Biodiversity Knowledge for Macrofungi: Contributions and Assessment of an Herbarium Collection DNA Barcode Sequencing Project , 2013, PloS one.

[126]  Jin-Rong Xu,et al.  Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi , 2013, BMC Genomics.

[127]  O. Ovaskainen,et al.  Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest , 2013, Science.

[128]  Kessy Abarenkov,et al.  Fungal community analysis by high-throughput sequencing of amplified markers – a user's guide , 2013, The New phytologist.

[129]  Michelle E. Afkhami,et al.  Fungal Symbionts as Manipulators of Plant Reproductive Biology , 2013, The American Naturalist.

[130]  I. Schmitt,et al.  Comparison of ITS1 and ITS2 rDNA in 454 sequencing of hyperdiverse fungal communities , 2013 .

[131]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[132]  A. Salamov,et al.  Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi , 2012, PLoS pathogens.

[133]  P. Baldrian,et al.  Fungal community on decomposing leaf litter undergoes rapid successional changes , 2012, The ISME Journal.

[134]  Matthew G. Bakker,et al.  Harnessing the rhizosphere microbiome through plant breeding and agricultural management , 2012, Plant and Soil.

[135]  M. Wallenstein,et al.  A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning , 2012, Biogeochemistry.

[136]  Albee Y. Ling,et al.  The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes , 2012, Science.

[137]  A. Salamov,et al.  Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. , 2012, The New phytologist.

[138]  N. Gerardo,et al.  Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae , 2012, Biology Letters.

[139]  J. Brownstein,et al.  Emerging fungal threats to animal, plant and ecosystem health , 2012, Nature.

[140]  Antonio Di Pietro,et al.  The Top 10 fungal pathogens in molecular plant pathology. , 2012, Molecular plant pathology.

[141]  Guy Leonard,et al.  Marine fungi: their ecology and molecular diversity. , 2012, Annual review of marine science.

[142]  John Wieczorek,et al.  Darwin Core: An Evolving Community-Developed Biodiversity Data Standard , 2012, PloS one.

[143]  S. Stark,et al.  Microbially Mediated Plant Functional Traits , 2011 .

[144]  Fiona J. Thomson,et al.  Seed dispersal distance is more strongly correlated with plant height than with seed mass , 2011 .

[145]  B. Kendrick Fungi: Ecological Importance and Impact on Humans , 2011 .

[146]  L. Boddy,et al.  Saprotrophic basidiomycete mycelia and their interspecific interactions affect the spatial distribution of extracellular enzymes in soil. , 2011, FEMS microbiology ecology.

[147]  K. Treseder,et al.  Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. , 2011, Ecology letters.

[148]  D. Hibbett,et al.  Fueling the future with fungal genomics , 2011 .

[149]  S. Higgins,et al.  TRY – a global database of plant traits , 2011, Global Change Biology.

[150]  S. West,et al.  Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis , 2011, Science.

[151]  A. Salamov,et al.  The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi , 2011, Science.

[152]  C. Mora,et al.  How Many Species Are There on Earth and in the Ocean? , 2011, PLoS biology.

[153]  Kerstin Voigt,et al.  Where is the unseen fungal diversity hidden? A study of Mortierella reveals a large contribution of reference collections to the identification of fungal environmental sequences. , 2011, The New phytologist.

[154]  Bernard Henrissat,et al.  Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea , 2011, PLoS genetics.

[155]  J. Kopecký,et al.  Active and total microbial communities in forest soil are largely different and highly stratified during decomposition , 2011, The ISME Journal.

[156]  Kristin H. Kane Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region , 2011 .

[157]  M. Raizada,et al.  Conservation and Diversity of Seed Associated Endophytes in Zea across Boundaries of Evolution, Ethnography and Ecology , 2011, PloS one.

[158]  K. Peay,et al.  Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? , 2011 .

[159]  P. Bakker,et al.  Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria , 2011, Science.

[160]  K. Newsham A meta-analysis of plant responses to dark septate root endophytes. , 2011, The New phytologist.

[161]  N. Stenseth,et al.  Mushroom's spore size and time of fruiting are strongly related: is moisture important? , 2011, Biology Letters.

[162]  M. Blackwell The fungi: 1, 2, 3 ... 5.1 million species? , 2011, American journal of botany.

[163]  Guo-Ping Zhao,et al.  Genome Sequencing and Comparative Transcriptomics of the Model Entomopathogenic Fungi Metarhizium anisopliae and M. acridum , 2011, PLoS genetics.

[164]  Pari Skamnioti,et al.  Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism , 2010, Science.

[165]  L. Tedersoo,et al.  454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. , 2010, The New phytologist.

[166]  M. Hijri,et al.  Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. , 2010, FEMS microbiology letters.

[167]  T. Fukami,et al.  Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. , 2010, Ecology letters.

[168]  M. Wingfield,et al.  Comparison of procedures to evaluate the pathogenicity of Ceratocystisfimbriata sensu lato isolates from Eucalyptus in South Africa , 2010 .

[169]  A. Endo A historical perspective on the discovery of statins , 2010, Proceedings of the Japan Academy. Series B, Physical and biological sciences.

[170]  N. Moran,et al.  Lateral Transfer of Genes from Fungi Underlies Carotenoid Production in Aphids , 2010, Science.

[171]  Andy F. S. Taylor,et al.  The UNITE database for molecular identification of fungi--recent updates and future perspectives. , 2010, The New phytologist.

[172]  M. Rillig,et al.  Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi , 2009, Proceedings of the Royal Society B: Biological Sciences.

[173]  Jason E. Stajich,et al.  The Fungi , 2009, Current Biology.

[174]  K. Peay,et al.  Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? , 2009, Ecology.

[175]  Jolanta Miadlikowska,et al.  A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? , 2009, Systematic biology.

[176]  T. Bechtold,et al.  Handbook of Natural Colorants , 2009 .

[177]  A. Arnold,et al.  Fungal endophytes: diversity and functional roles. , 2009, The New phytologist.

[178]  David Hewitt,et al.  The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. , 2009, Systematic biology.

[179]  Jane E. Smith Mycorrhizal Symbiosis (Third Edition) , 2009 .

[180]  A. Salamov,et al.  Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion , 2009, Proceedings of the National Academy of Sciences.

[181]  S. Allison,et al.  Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change , 2008 .

[182]  Thomas D. Bruns,et al.  Fungal Community Ecology: A Hybrid Beast with a Molecular Master , 2008 .

[183]  A. Varma,et al.  The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. , 2008, Molecular plant-microbe interactions : MPMI.

[184]  J. Avalos,et al.  The White Collar protein WcoA of Fusarium fujikuroi is not essential for photocarotenogenesis, but is involved in the regulation of secondary metabolism and conidiation. , 2008, Fungal genetics and biology : FG & B.

[185]  J. Piotrowski,et al.  Dynamics of mycorrhizae during development of riparian forests along an unregulated river , 2008 .

[186]  J. Klironomos,et al.  Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning , 2007, Science.

[187]  T. Osono Ecology of ligninolytic fungi associated with leaf litter decomposition , 2007, Ecological Research.

[188]  P. Crous,et al.  Pathogenicity testing of lesser-known vascular fungi of grapevines , 2007, Australasian Plant Pathology.

[189]  Laura E. Green,et al.  The role of ecological theory in microbial ecology , 2007, Nature Reviews Microbiology.

[190]  T. Taylor,et al.  Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. , 2007, The New phytologist.

[191]  S. Lumyong,et al.  A Phylogenetic Evaluation of Whether Endophytes Become Saprotrophs at Host Senescence , 2007, Microbial Ecology.

[192]  J. Spatafora,et al.  Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes , 2007, Molecular ecology.

[193]  Rytas Vilgalys,et al.  Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR , 2007, Mycologia.

[194]  David K. Johnson,et al.  Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production , 2007, Science.

[195]  S. Trumbore,et al.  Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. , 2007, The New phytologist.

[196]  R. Redman,et al.  A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance , 2007, Science.

[197]  R. Henrik Nilsson,et al.  Taxonomic Reliability of DNA Sequences in Public Sequence Databases: A Fungal Perspective , 2006, PloS one.

[198]  K. Thorpe Diseases of Trees and Shrubs , 2006 .

[199]  R. Kjøller Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. , 2006, FEMS microbiology ecology.

[200]  C. Machado,et al.  Effects of ergot alkaloids on food preference and satiety in rabbits, as assessed with gene-knockout endophytes in perennial ryegrass (Lolium perenne). , 2006, Journal of agricultural and food chemistry.

[201]  M. Westoby,et al.  Seed size and plant strategy across the whole life cycle , 2006 .

[202]  Jennifer A. Rudgers,et al.  Plant-fungus mutualism affects spider composition in successional fields. , 2006, Ecology letters.

[203]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2006, Cell.

[204]  Roderick S. Bain,et al.  Explaining Dioscorides' “Double Difference”: Why Are Some Mushrooms Poisonous, and Do They Signal Their Unprofitability? , 2005, The American Naturalist.

[205]  Lynne Boddy,et al.  Living in a fungal world: impact of fungi on soil bacterial niche development. , 2005, FEMS microbiology reviews.

[206]  Rytas Vilgalys,et al.  Fungal Community Analysis by Large-Scale Sequencing of Environmental Samples , 2005, Applied and Environmental Microbiology.

[207]  P. R. Scott,et al.  Plant disease: a threat to global food security. , 2005, Annual review of phytopathology.

[208]  Jennifer A. Rudgers,et al.  Connecting plant–microbial interactions above and belowground: a fungal endophyte affects decomposition , 2005, Oecologia.

[209]  M. Rillig Arbuscular mycorrhizae, glomalin, and soil aggregation , 2004 .

[210]  L. Poorter,et al.  Leaf traits and herbivory rates of tropical tree species differing in successional status. , 2004, Plant biology.

[211]  J. Whipps Prospects and limitations for mycorrhizas in biocontrol of root pathogens , 2004 .

[212]  Richard P. Shefferson,et al.  Evolutionary studies of ectomycorrhizal fungi: recent advances and future directions , 2004 .

[213]  P. Reich,et al.  Global patterns of plant leaf N and P in relation to temperature and latitude. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[214]  C. Lovelock,et al.  Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rain forest soil , 2004 .

[215]  Sean Martin,et al.  Globally distributed object identification for biological knowledgebases , 2004, Briefings Bioinform..

[216]  A. Rincón,et al.  Biocontrol mechanisms of Trichoderma strains. , 2004, International microbiology : the official journal of the Spanish Society for Microbiology.

[217]  B. Thomma Alternaria spp.: from general saprophyte to specific parasite. , 2003, Molecular plant pathology.

[218]  P. Reich,et al.  The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies , 2003, International Journal of Plant Sciences.

[219]  J. Nosanchuk,et al.  Melanin and fungi , 2003, Current opinion in infectious diseases.

[220]  Catherine G. Parks,et al.  Coarse-scale population structure of pathogenic Armillaria species in a mixed-conifer forest in the Blue Mountains of northeast Oregon , 2003 .

[221]  J. Henson,et al.  Thermotolerance Generated by Plant/Fungal Symbiosis , 2002, Science.

[222]  K. Mendgen,et al.  Plant infection and the establishment of fungal biotrophy. , 2002, Trends in plant science.

[223]  R. Sinsabaugh,et al.  Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss , 2002 .

[224]  R. Stevenson,et al.  AGTR2 Mutations in X-Linked Mental Retardation , 2002, Science.

[225]  M. Allen,et al.  Endo- and ectomycorrhizas in Quercusagrifolia Nee. (Fagaceae): patterns of root colonization and effects on seedling growth , 2001, Mycorrhiza.

[226]  M. Berbee,et al.  The phylogeny of plant and animal pathogens in the Ascomycota , 2001 .

[227]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.

[228]  P. Reich,et al.  Strategy shifts in leaf physiology, structure and nutrient content between species of high‐ and low‐rainfall and high‐ and low‐nutrient habitats , 2001 .

[229]  R. Augé Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis , 2001, Mycorrhiza.

[230]  L. Guzmán-Dávalos,et al.  Some aphyllophorales tested for organic dyes , 2001 .

[231]  A. Bessette,et al.  The Rainbow Beneath My Feet: A Mushroom Dyer's Field Guide , 2001 .

[232]  D. Malinowski,et al.  Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue , 2000, Plant and Soil.

[233]  D. McLaughlin,et al.  Systematics and Evolution , 2000, The Mycota.

[234]  R. Sinsabaugh,et al.  MICROBIAL ENZYME SHIFTS EXPLAIN LITTER DECAY RESPONSES TO SIMULATED NITROGEN DEPOSITION , 2000 .

[235]  J. Usall,et al.  Biological control of blue mould on apple by a strain of Candida sake under several controlled atmosphere conditions. , 2000, International journal of food microbiology.

[236]  D. Godbold,et al.  Metal toxicity and ectomycorrhizas , 2000 .

[237]  James F. White,et al.  An Overview of Endophytic Microbes: Endophytism Defined , 2000 .

[238]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[239]  Ian R. Sanders,et al.  Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity , 1998, Nature.

[240]  K. Saikkonen,et al.  FUNGAL ENDOPHYTES: A Continuum of Interactions with Host Plants , 1998 .

[241]  A. Varma,et al.  PIRIFORMOSPORA INDICA, GEN. ET SP. NOV., A NEW ROOT-COLONIZING FUNGUS , 1998 .

[242]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[243]  J. Bever,et al.  Genetic variation of morphological characters within a single isolate of the endomycorrhizal fungus Glomus clarum (Glomaceae). , 1997, American journal of botany.

[244]  R. Zabel,et al.  Comparison of wood decay among diverse lignicolous fungi , 1997 .

[245]  E. Jacobson,et al.  Antioxidant function of melanin in black fungi , 1995, Infection and immunity.

[246]  Dennis C. Wilson Endophyte: The Evolution of a Term, and Clarification of Its Use and Definition , 1995 .

[247]  P. Klinkhamer Plant allometry: The scaling of form and process , 1995 .

[248]  A. Jarosz,et al.  Effects of disease in wild plant populations and the evolution of pathogen aggressiveness , 1995 .

[249]  A. Wennström Endophyte: The Misuse of an Old Term , 1994 .

[250]  G. Gadd Interactions of fungip with toxic metals , 1993 .

[251]  D. Hibbett,et al.  Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. , 1992, Molecular phylogenetics and evolution.

[252]  K. Clay Fungal Endophytes of Grasses: A Defensive Mutualism between Plants and Fungi , 1988 .

[253]  C. Brownlee,et al.  The structure and function of mycelial systems of ectomycorrhizal roots with special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport , 1983, Plant and Soil.

[254]  John F. Muratore,et al.  Nitrogen and Lignin Control of Hardwood Leaf Litter Decomposition Dynamics , 1982 .

[255]  W. Gams Introduction to the history of mycology , 1977, Netherlands journal of plant pathology.

[256]  J. P. Grime Vegetation classification by reference to strategies , 1974, Nature.

[257]  P. Gadgil,et al.  Mycorrhiza and Litter Decomposition , 1971, Nature.

[258]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[259]  Ph. Gitta L. Coaker,et al.  Plant Pathology , 1957, Nature.

[260]  G. W. Martin Systematic Position of the Slime Molds and Its Bearing on the Classification of the Fungi , 1932, Botanical Gazette.

[261]  V. Blackman THE SIGNIFICANCE OF THE EFFICIENCY INDEX OF PLANT GROWTH. , 1920 .

[262]  21. B. Frank: Ueber die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze , 1885, Berichte der Deutschen Botanischen Gesellschaft.

[263]  Lauren C. Cline,et al.  Ecological and functional effects of fungal endophytes on wood decomposition , 2018 .

[264]  Bernard Henrissat,et al.  The genome of Xylona heveae provides a window into fungal endophytism. , 2016, Fungal biology.

[265]  A. Bennett,et al.  Unpredictable assembly of arbuscular mycorrhizal fungal communities , 2016 .

[266]  D. McLaughlin Systematics and Evolution : Part B , 2015 .

[267]  R. Koide,et al.  Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. , 2014, The New phytologist.

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

[269]  T. Mengiste Plant immunity to necrotrophs. , 2012, Annual review of phytopathology.

[270]  M. Sadowsky,et al.  Competition between two wood-degrading fungi with distinct influences on residues. , 2012, FEMS microbiology ecology.

[271]  P. Gadgil,et al.  SUPPRESSION OF LITTER DECOMPOSITION BY MYCORRHIZAL ROOTS OF PINUS RADIATA , 2012 .

[272]  J. Maron,et al.  Soil fungal pathogens and the relationship between plant diversity and productivity. , 2011, Ecology letters.

[273]  F. Martin,et al.  Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. , 2011, Trends in genetics : TIG.

[274]  P. Baldrian,et al.  Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil , 2010, Plant and Soil.

[275]  Schmaile Mycotoxins in Crops: A Threat to Human and Domestic Animal Health , 2009 .

[276]  B. Lindahl,et al.  Chapter 10 Distribution and function of litter basidiomycetes in coniferous forests , 2008 .

[277]  Jonathan P. Lynch,et al.  ROOT STRATEGIES FOR PHOSPHORUS ACQUISITION , 2008 .

[278]  Jennifer A. Rudgers,et al.  Forest succession suppressed by an introduced plant-fungal symbiosis. , 2007, Ecology.

[279]  U. Nehls,et al.  Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. , 2007, Phytochemistry.

[280]  Christian P. Kubicek,et al.  Fungal decomposers of plant litter in aquatic ecosystems (chapter 17) , 2007 .

[281]  G. Gadd Fungi in biogeochemical cycles , 2006 .

[282]  Gary E. Harman,et al.  Trichoderma species — opportunistic, avirulent plant symbionts , 2004, Nature Reviews Microbiology.

[283]  Jennifer A. Rudgers,et al.  Endophytic fungi alter relationships between diversity and ecosystem properties , 2004 .

[284]  M. Westoby,et al.  ECOLOGICAL STRATEGIES : Some Leading Dimensions of Variation Between Species , 2002 .

[285]  A. Johansen,et al.  Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi. , 2000 .

[286]  A. Varma,et al.  Mycorrhiza , 1995, Springer Berlin Heidelberg.

[287]  O. Petrini Fungal Endophytes of Tree Leaves , 1991 .

[288]  Thomas D. Bruns,et al.  Fungal Molecular Systematics , 1991 .

[289]  Lynne Boddy,et al.  Fungal decomposition of wood , 1988 .

[290]  H. Mooney,et al.  Resource Limitation in Plants-An Economic Analogy , 1985 .

[291]  R. Gilbertson Wood-Rotting Fungi of North America , 1980 .

[292]  L. Valadon Carotenoids as additional taxonomic characters in fungi: A review , 1976 .

[293]  Agostino Bassi,et al.  Del mal del segno , 1958 .

[294]  Theophrastus.,et al.  Enquiry into plants , 1916 .

[295]  D. Hibbett,et al.  Non-commercial Research and Educational Use including without Limitation Use in Instruction at Your Institution, Sending It to Specific Colleagues That You Know, and Providing a Copy to Your Institution's Administrator. All Other Uses, Reproduction and Distribution, including without Limitation Comm , 2022 .