Unearthing the roots of ectomycorrhizal symbioses

During the diversification of Fungi and the rise of conifer-dominated and angiosperm- dominated forests, mutualistic symbioses developed between certain trees and ectomycorrhizal fungi that enabled these trees to colonize boreal and temperate regions. The evolutionary success of these symbioses is evident from phylogenomic analyses that suggest that ectomycorrhizal fungi have arisen in approximately 60 independent saprotrophic lineages, which has led to the wide range of ectomycorrhizal associations that exist today. In this Review, we discuss recent genomic studies that have revealed the adaptations that seem to be fundamental to the convergent evolution of ectomycorrhizal fungi, including the loss of some metabolic functions and the acquisition of effectors that facilitate mutualistic interactions with host plants. Finally, we consider how these insights can be integrated into a model of the development of ectomycorrhizal symbioses.

[1]  S. Reissmann,et al.  Fungal effectors and plant susceptibility. , 2015, Annual review of plant biology.

[2]  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.

[3]  F. Martin,et al.  Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis. , 2011, Current opinion in plant biology.

[4]  S. Duplessis,et al.  Living in harmony in the wood underground: ectomycorrhizal genomics. , 2007, Current opinion in plant biology.

[5]  R. Finlay Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. , 2007, Journal of experimental botany.

[6]  Shiv D. Kale,et al.  A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development , 2011, Current Biology.

[7]  U. Güldener,et al.  Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica , 2011, PLoS pathogens.

[8]  E. Kothe,et al.  Identification of a Hydrophobin Gene That is Developmentally Regulated in the Ectomycorrhizal Fungus Tricholoma terreum , 2002, Applied and Environmental Microbiology.

[9]  K. Garcia,et al.  Take a Trip Through the Plant and Fungal Transportome of Mycorrhiza. , 2016, Trends in plant science.

[10]  E. Danchin,et al.  Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. , 2014, Fungal genetics and biology : FG & B.

[11]  R. Peterson,et al.  Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces , 2004 .

[12]  B. Lindahl,et al.  Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. , 2015, The New phytologist.

[13]  K. Ljung,et al.  Development of the Poplar-Laccaria bicolor Ectomycorrhiza Modifies Root Auxin Metabolism, Signaling, and Response1 , 2015, Plant Physiology.

[14]  E. Morin,et al.  Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins , 2015, Front. Microbiol..

[15]  E. Kothe,et al.  Biosynthesis and Secretion of Indole-3-Acetic Acid and Its Morphological Effects on Tricholoma vaccinum-Spruce Ectomycorrhiza , 2015, Applied and Environmental Microbiology.

[16]  G. Bécard,et al.  Evolution of the plant-microbe symbiotic 'toolkit'. , 2013, Trends in plant science.

[17]  F. Martin,et al.  Reconsidering mutualistic plant-fungal interactions through the lens of effector biology. , 2015, Current opinion in plant biology.

[18]  D. Read,et al.  The dawn of symbiosis between plants and fungi , 2011, Biology Letters.

[19]  David Read,et al.  Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes , 2004 .

[20]  R. Solano,et al.  The Bacterial Effector HopX1 Targets JAZ Transcriptional Repressors to Activate Jasmonate Signaling and Promote Infection in Arabidopsis , 2014, PLoS biology.

[21]  M. V. D. van der Heijden,et al.  Mycorrhizal ecology and evolution : the past , the present , and the future , 2015 .

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

[23]  J. Manners,et al.  JAZ repressors and the orchestration of phytohormone crosstalk. , 2012, Trends in plant science.

[24]  Daniel M. Durall,et al.  Net transfer of carbon between ectomycorrhizal tree species in the field , 1997, Nature.

[25]  N. Requena,et al.  A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy , 2011, Current Biology.

[26]  C. Troein,et al.  Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus , 2013, The ISME Journal.

[27]  D. Haltrich,et al.  Extracellular electron transfer systems fuel cellulose oxidative degradation , 2016, Science.

[28]  F. Martin,et al.  The Laccaria genome: a symbiont blueprint decoded. , 2008, The New phytologist.

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

[30]  I. Grigoriev,et al.  Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor. , 2012, Fungal genetics and biology : FG & B.

[31]  P. Bonfante,et al.  Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. , 2010, Nature communications.

[32]  Li Yang,et al.  Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. , 2014, Cell host & microbe.

[33]  M. Kemppainen,et al.  Overexpression of Laccaria bicolor aquaporin JQ585595 alters root water transport properties in ectomycorrhizal white spruce (Picea glauca) seedlings. , 2015, The New phytologist.

[34]  S. He,et al.  Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. , 2013, Annual review of phytopathology.

[35]  R. D. de Vries,et al.  Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes , 2014, Microbiology and Molecular Reviews.

[36]  B. Sundberg,et al.  Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. , 2014, The New phytologist.

[37]  Mark C. Brundrett,et al.  Coevolution of roots and mycorrhizas of land plants. , 2002, The New phytologist.

[38]  Alga Zuccaro,et al.  Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. , 2016, Current opinion in microbiology.

[39]  I. Feussner,et al.  Upgrading Root Physiology for Stress Tolerance by Ectomycorrhizas: Insights from Metabolite and Transcriptional Profiling into Reprogramming for Stress Anticipation1[C][W][OA] , 2009, Plant Physiology.

[40]  H. Ohta,et al.  Basic Helix-Loop-Helix Transcription Factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 Are Negative Regulators of Jasmonate Responses in Arabidopsis1[W][OPEN] , 2013, Plant Physiology.

[41]  Peter E. Larsen,et al.  Multi-Omics Approach Identifies Molecular Mechanisms of Plant-Fungus Mycorrhizal Interaction , 2016, Front. Plant Sci..

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

[43]  F. Martin,et al.  Poplar root exudates contain compounds that induce the expression of MiSSP7 in Laccaria bicolor , 2012, Plant signaling & behavior.

[44]  D. J. Lodge,et al.  Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae , 2009 .

[45]  M. Selosse,et al.  The land flora: a phototroph-fungus partnership? , 1998, Trends in ecology & evolution.

[46]  I. Kottke,et al.  The cellular structure of the Hartig net: coenocytic and transfer cell‐like organization , 1987 .

[47]  D. Soltis,et al.  Rosid radiation and the rapid rise of angiosperm-dominated forests , 2009, Proceedings of the National Academy of Sciences.

[48]  S E Baker,et al.  Sequencing the fungal tree of life. , 2011, The New phytologist.

[49]  K. Garcia,et al.  The role of mycorrhizal associations in plant potassium nutrition , 2014, Front. Plant Sci..

[50]  K. Treseder,et al.  An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi , 2006 .

[51]  B. LePage,et al.  Fossil ectomycorrhizae from the Middle Eocene. , 1997, American journal of botany.

[52]  D. Strullu,et al.  Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. , 2014, The New phytologist.

[53]  M. Ali,et al.  From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association , 2014, Front. Plant Sci..

[54]  J. Bousquet,et al.  Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants , 1993, Nature.

[55]  S. Hacquard,et al.  Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments. , 2013, Environmental microbiology.

[56]  B. Wolfe,et al.  The Irreversible Loss of a Decomposition Pathway Marks the Single Origin of an Ectomycorrhizal Symbiosis , 2012, PloS one.

[57]  R. Currah,et al.  Oidiodendron maius: Saprobe in Sphagnum Peat, Mutualist in Ericaceous Roots? , 2006 .

[58]  A. Kohler,et al.  The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N. , 2008, The New phytologist.

[59]  K. Palme,et al.  Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture , 2015, Nature Communications.

[60]  D. Hibbett,et al.  Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay , 2013, Mycologia.

[61]  Bernard Henrissat,et al.  Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis , 2010, Nature.

[62]  Christian Körner,et al.  Belowground carbon trade among tall trees in a temperate forest , 2016, Science.

[63]  M. Weiß,et al.  The sugar porter gene family of Laccaria bicolor: function in ectomycorrhizal symbiosis and soil-growing hyphae. , 2008, The New phytologist.

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

[65]  F. Martin,et al.  Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. , 2014, The New phytologist.

[66]  J. Metraux,et al.  Plant cell wall in pathogenesis, parasitism and symbiosis , 2014, Front. Plant Sci..

[67]  F. Richard,et al.  Mycorrhizal networks: des liaisons dangereuses? , 2006, Trends in ecology & evolution.

[68]  P. Spanu The genomics of obligate (and nonobligate) biotrophs. , 2012, Annual review of phytopathology.

[69]  D. Hibbett,et al.  The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses , 2009, BMC Biology.

[70]  D. Scheel,et al.  Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. , 2015, The New phytologist.

[71]  Andy F. S. Taylor,et al.  ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi , 2009, The ISME Journal.

[72]  Nadejda A. Soudzilovskaia,et al.  Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry , 2015 .

[73]  D. Hibbett,et al.  Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes , 2013, Mycologia.

[74]  Martin Parniske,et al.  Arbuscular mycorrhiza: the mother of plant root endosymbioses , 2008, Nature Reviews Microbiology.

[75]  D. Malloch,et al.  The origin of land plants: a matter of mycotrophism. , 1975, Bio Systems.

[76]  P. Högberg,et al.  Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. , 2002, The New phytologist.

[77]  B. Henrissat,et al.  Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum , 2016, Nature Communications.

[78]  A. Goossens,et al.  Jasmonates: signal transduction components and their roles in environmental stress responses , 2016, Plant Molecular Biology.

[79]  S. He,et al.  Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors , 2013, PLoS pathogens.

[80]  C. Walker,et al.  Arbuscular mycorrhizal-like fungi in Carboniferous arborescent lycopsids. , 2011, The New phytologist.

[81]  Francis Martin,et al.  Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. , 2004, The New phytologist.

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

[83]  M. Binder,et al.  Evolutionary history of Serpulaceae (Basidiomycota): molecular phylogeny, historical biogeography and evidence for a single transition of nutritional mode , 2011, BMC Evolutionary Biology.

[84]  R. Bhalerao,et al.  The Ectomycorrhizal Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling1[W] , 2009, Plant Physiology.

[85]  J. W. Taylor,et al.  Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with Piloderma-Pinus symbiosis: improved methodologies for assessing gene expression in situ. , 2014, Environmental microbiology.

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

[87]  J. Morrell-Falvey,et al.  Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes , 2014, Proceedings of the National Academy of Sciences.

[88]  T. Tschaplinski,et al.  Populus trichocarpa and Populus deltoides exhibit different metabolomic responses to colonization by the symbiotic fungus Laccaria bicolor. , 2014, Molecular plant-microbe interactions : MPMI.

[89]  R. Marmeisse,et al.  A fungal conserved gene from the basidiomycete Hebeloma cylindrosporum is essential for efficient ectomycorrhiza formation. , 2014, Molecular plant-microbe interactions : MPMI.

[90]  G. Tuskan,et al.  Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. , 2013, Plant, cell & environment.

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

[92]  F. Martin,et al.  Immunolocalization of hydrophobin HYDPt-1 from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots. , 2001, The New phytologist.

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

[94]  S. Duplessis,et al.  Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. , 2001, The New phytologist.

[95]  Y. Van de Peer,et al.  The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis , 2008, Nature.

[96]  P. Punjabi,et al.  The Past, The Present and The Future , 2010 .

[97]  Bernard Henrissat,et al.  Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists , 2015, Nature Genetics.

[98]  P. Lammers,et al.  Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis , 2013, Proceedings of the National Academy of Sciences.

[99]  I. Grigoriev,et al.  The Mutualist Laccaria bicolor Expresses a Core Gene Regulon During the Colonization of Diverse Host Plants and a Variable Regulon to Counteract Host-Specific Defenses. , 2015, Molecular plant-microbe interactions : MPMI.

[100]  B. Henrissat,et al.  Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete Hebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis. , 2015, The New phytologist.

[101]  T. Lundell,et al.  Genomics, Lifestyles and Future Prospects of Wood-Decay and Litter-Decomposing Basidiomycota , 2014 .