1887

Chapter 2 : Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap02-1.gif /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap02-2.gif

Abstract:

The fungal lineage is one of the three large eukaryotic lineages that dominate terrestrial ecosystems. They share a common ancestor with animals in the eukaryotic supergroup Opisthokonta and have a deeper common ancestry with plants, yet several phenotypes such as morphological, physiological, or nutritional traits make them unique among all living organisms. This article provides an overview of some of the most important fungal traits, how they evolve, and what major genes and gene families contribute to their development. The traits highlighted here represent just a sample of the characteristics that have evolved in fungi, including polarized multicellular growth, fruiting body development, dimorphism, secondary metabolism, wood decay, and mycorrhizae. However, a great deal of other important traits also underlie the evolution of the taxonomically and phenotypically hyperdiverse fungal kingdom, which could fill up a volume on its own. After reviewing the evolution of these six well-studied traits in fungi, we discuss how the recurrent evolution of phenotypic similarity, that is, convergent evolution in the broad sense, has shaped their phylogenetic distribution in extant species.

Citation: Nagy L, Tóth R, Kiss E, Slot J, Gácser A, Kovács G. 2017. Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases, p 35-56. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0036-2016
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Overview of the phylogenetic distribution of the traits presented in this article. Phylogeny of the major fungal groups and the phylogenetic distribution of the traits discussed in this article. Tree modified and redrawn from MycoCosm (http://genome.jgi.doe.gov/programs/fungi/index.jsf). Thick branches denote well-known relationships, while thin branches mark uncertainties in our understanding of fungal relationships. Presence or absence of a given trait is highlighted by black or white shading, respectively. Gray shading denotes rare or not fully developed states of the given trait, while blue denotes the secondary partial loss of multicellular growth in yeasts. The evolution of hyphae from unicellular ancestors (left, ; photo courtesy of Don Barr, http://www.bsu.edu/classes/ruch/msa/barr/4-15.jpg). Hyphae evolved in several groups, including the Monoblepharidomycetes (middle, sp.; [from reference ]) and the crown fungi (top right, mycelium growing on sawdust). Also shown are hyphal and yeast-like colonies of the dimorphic fungus (bottom right). Detailed view of the major orders, their wood-rotting characteristics, and the distribution of agaricoid fruiting body morphologies of the Agaricomycetes. Brown and beige represent brown and white rot lineages, respectively, whereas empty rectangles denote groups that do not degrade wood (Wallemiomycetes, Tremellomycetes) or cause an uncharacterized type of wood decay or mycorrhiza (Sebacinales and Cantharellales). Examples of typical white (, top) and brown (, bottom) rot Basidiomycota. Examples of the diversity of fruiting body morphologies in the Agaricomycetes, including from left to right, resupinate (); auricularioid, jelly fungi (); club and coral fungi (); puffballs (); and agaricoid morphologies ( sp). Photos: L. Nagy unless stated otherwise.

Citation: Nagy L, Tóth R, Kiss E, Slot J, Gácser A, Kovács G. 2017. Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases, p 35-56. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0036-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Secondary metabolites produced by fungi. HC toxin is a nonribosomal peptide virulence factor produced by plant pathogens such as the Northern corn leaf spot fungus, . Gibberellic acid is a diterpene-derived plant growth hormone produced by some spp. (e.g., ), which leads to growth defects in grass seedlings. Usnic acid is a common polyketide secondary metabolite thought to protect against biotic and abiotic stress in many lichens. Aflatoxin B1 is a highly carcinogenic polyketide produced by molds that spoils grain and peanut harvests. Psilocybin is a hallucinogenic indole alkaloid produced by a variety of mushrooms. Alpha amanitin is a deadly peptide alkaloid that inhibits RNA polymerase II, produced by diverse mushroom-forming fungi.

Citation: Nagy L, Tóth R, Kiss E, Slot J, Gácser A, Kovács G. 2017. Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases, p 35-56. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0036-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819583.chap2
1. Harris SD,, Momany M . 2004. Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet Biol 41 : 391400.[CrossRef] [PubMed]
2. Harris SD . 2011. Hyphal morphogenesis: an evolutionary perspective. Fungal Biol 115 : 475484.[CrossRef] [PubMed]
3. Dee JM,, Mollicone M,, Longcore JE,, Roberson RW,, Berbee ML . 2015. Cytology and molecular phylogenetics of Monoblepharidomycetes provide evidence for multiple independent origins of the hyphal habit in the Fungi. Mycologia 107 : 710728.[CrossRef] [PubMed]
4. Moore D . 2013. Fungal Biology in the Origin and Emergence of Life. Cambridge University Press, Cambridge, United Kingdom.[CrossRef] [PubMed]
5. Jedd G . 2011. Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol 21 : 1219.[CrossRef]
6. Healy RA,, Kumar TK,, Hewitt DA,, McLaughlin DJ . 2013. Functional and phylogenetic implications of septal pore ultrastructure in the ascoma of Neolecta vitellina . Mycologia 105 : 802813.[CrossRef] [PubMed]
7. Lew RR . 2011. How does a hypha grow? The biophysics of pressurized growth in fungi. Nat Rev Microbiol 9 : 509518.[CrossRef] [PubMed]
8. Harris SD . 2008. Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems. Mycologia 100 : 823832.[CrossRef] [PubMed]
9. Wendland J . 2001. Comparison of morphogenetic networks of filamentous fungi and yeast. Fungal Genet Biol 34 : 6382.[CrossRef] [PubMed]
10. Bartnicki-Garcia S,, Hergert F,, Gierz G . 1989. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal(tip) growth. Protoplasma 153 : 4657.[CrossRef]
11. Bartnicki-Garcia S . 2002. Hyphal Tip Growth: Outstanding Questions. Marcel Dekker, New York, NY.[PubMed]
12. Berepiki A,, Lichius A,, Read ND . 2011. Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9 : 876887.[CrossRef] [PubMed]
13. Virag A,, Harris SD . 2006. The Spitzenkörper: a molecular perspective. Mycol Res 110 : 413.[CrossRef] [PubMed]
14. Harris SD . 2001. Septum formation in Aspergillus nidulans . Curr Opin Microbiol 4 : 736739.[CrossRef] [PubMed]
15. Ruiz-Herrera J . 2012. Dimorphic Fungi: Their Importance as Models for Differentiation and Fungal Pathogenesis. Bentham Science Publishers, Dubai, United Arab Emirates.
16. Dickinson JR . 2005. Are yeasts free-living unicellular eukaryotes? Lett Appl Microbiol 41 : 445447.[CrossRef] [PubMed]
17. Nagy LG,, Ohm RA,, Kovács GM,, Floudas D,, Riley R,, Gácser A,, Sipiczki M,, Davis JM,, Doty SL,, de Hoog GS,, Lang BF,, Spatafora JW,, Martin FM,, Grigoriev IV,, Hibbett DS . 2014. Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts. Nat Commun 5 : 4471.[CrossRef] [PubMed]
18. Nemecek JC,, Wüthrich M,, Klein BS . 2006. Global control of dimorphism and virulence in fungi. Science 312 : 583588.[CrossRef] [PubMed]
19. Lewis ER,, Bowers JR,, Barker BM . 2015. Dust devil: the life and times of the fungus that causes valley fever. PLoS Pathog 11 : e1004762.[CrossRef] [PubMed]
20. Wang L,, Lin X . 2012. Morphogenesis in fungal pathogenicity: shape, size, and surface. PLoS Pathog 8 : e1003027.[CrossRef] [PubMed]
21. Gauthier GM . 2015. Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog 11 : e1004608.[CrossRef] [PubMed]
22. Gauthier G,, Klein BS . 2008. Insights into fungal morphogenesis and immune evasion: fungal conidia, when situated in mammalian lungs, may switch from mold to pathogenic yeasts or spore-forming spherules. Microbe Wash DC 3 : 416423.[CrossRef] [PubMed]
23. Restrepo A,, Salazar ME,, Cano LE,, Stover EP,, Feldman D,, Stevens DA . 1984. Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis. Infect Immun 46 : 346353.[PubMed]
24. Youngchim S,, Nosanchuk JD,, Pornsuwan S,, Kajiwara S,, Vanittanakom N . 2013. The role of l-DOPA on melanization and mycelial production in Malassezia furfur . PLoS One 8 : e63764.[CrossRef] [PubMed]
25. Brown GD,, Gordon S . 2005. Immune recognition of fungal beta-glucans. Cell Microbiol 7 : 471479.[CrossRef] [PubMed]
26. Hogan LH,, Klein BS . 1994. Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62 : 35433546.[PubMed]
27. Rappleye CA,, Eissenberg LG,, Goldman WE . 2007. Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci USA 104 : 13661370.[CrossRef] [PubMed]
28. Holbrook ED,, Smolnycki KA,, Youseff BH,, Rappleye CA . 2013. Redundant catalases detoxify phagocyte reactive oxygen and facilitate Histoplasma capsulatum pathogenesis. Infect Immun 81 : 23342346.[CrossRef] [PubMed]
29. Chao LY,, Rine J,, Marletta MA . 2008. Spectroscopic and kinetic studies of Nor1, a cytochrome P450 nitric oxide reductase from the fungal pathogen Histoplasma capsulatum . Arch Biochem Biophys 480 : 132137.[CrossRef] [PubMed]
30. Campos EG,, Jesuino RS,, Dantas AS,, Brígido MM,, Felipe MS . 2005. Oxidative stress response in Paracoccidioides brasiliensis . Genet Mol Res 4 : 409429.[PubMed]
31. Sims CR,, Ostrosky-Zeichner L,, Rex JH . 2005. Invasive candidiasis in immunocompromised hospitalized patients. Arch Med Res 36 : 660671.[CrossRef] [PubMed]
32. Trofa D,, Gácser A,, Nosanchuk JD . 2008. Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21 : 606625.[CrossRef] [PubMed]
33. Goldani LZ,, Santos RP . 2010. Candida tropicalis as an emerging pathogen in Candida meningitis: case report and review. Braz J Infect Dis 14 : 631633.[PubMed]
34. Sullivan D,, Coleman D . 1997. Candida dubliniensis: an emerging opportunistic pathogen. Curr Top Med Mycol 8 : 1525.[PubMed]
35. Thompson DS,, Carlisle PL,, Kadosh D . 2011. Coevolution of morphology and virulence in Candida species. Eukaryot Cell 10 : 11731182.[CrossRef] [PubMed]
36. Li CH,, Cervantes M,, Springer DJ,, Boekhout T,, Ruiz-Vazquez RM,, Torres-Martinez SR,, Heitman J,, Lee SC . 2011. Sporangiospore size dimorphism is linked to virulence of Mucor circinelloides . PLoS Pathog 7 : e1002086.[CrossRef] [PubMed]
37. Lillis JV,, Dawson ES,, Chang R,, White CR Jr . 2010. Disseminated dermal Trichophyton rubrum infection: an expression of dermatophyte dimorphism? J Cutan Pathol 37 : 11681169.[CrossRef] [PubMed]
38. Nadal M,, García-Pedrajas MD,, Gold SE . 2008. Dimorphism in fungal plant pathogens. FEMS Microbiol Lett 284 : 127134.[CrossRef] [PubMed]
39. Cissé OH,, Almeida JM,, Fonseca A,, Kumar AA,, Salojärvi J,, Overmyer K,, Hauser PM,, Pagni M . 2013. Genome sequencing of the plant pathogen Taphrina deformans, the causal agent of peach leaf curl. MBio 4 : e00055-13.[CrossRef] [PubMed]
40. Vollmeister E,, Schipper K,, Baumann S,, Haag C,, Pohlmann T,, Stock J,, Feldbrügge M . 2012. Fungal development of the plant pathogen Ustilago maydis . FEMS Microbiol Rev 36 : 5977.[CrossRef] [PubMed]
41. Naruzawa ES,, Bernier L . 2014. Control of yeast-mycelium dimorphism in vitro in Dutch elm disease fungi by manipulation of specific external stimuli. Fungal Biol 118 : 872884.[CrossRef] [PubMed]
42. Smith ME,, Gryganskyi A,, Bonito G,, Nouhra E,, Moreno-Arroyo B,, Benny G . 2013. Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales. Fungal Genet Biol 61 : 6168.[CrossRef] [PubMed]
43. Liu YJ,, Hall BD . 2004. Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci USA 101 : 45074512.[CrossRef] [PubMed]
44. Pukkila PJ . 2011. Coprinopsis cinerea . Curr Biol 21 : R616R617.[CrossRef] [PubMed]
45. Binder M,, Hibbett DS,, Larsson K-H,, Larsson E,, Langer E . 2005. The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes). Syst Biodivers 3 : 113157.[CrossRef]
46. Hibbett D . 2004. Trends in morphological evolution in homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches. Syst Biol 53 : 889903.[CrossRef] [PubMed]
47. Hibbett DS,, Binder M . 2002. Evolution of complex fruiting-body morphologies in homobasidiomycetes. Proc Biol Sci 269 : 19631969.[PubMed]
48. Pöggeler S,, Nowrousian MKU, . 2006. Fruiting-body development in Ascomycetes, p 325355. In Esser K (ed), The Mycota: Growth, Differentiation and Sexuality. Springer-Verlag, Berlin, Germany.[CrossRef]
49. Hibbett DS . 2007. After the gold rush, or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century. Mycol Res 111 : 10011018.[CrossRef] [PubMed]
50. Miller OK, . 1971. The relationship of cultural characters to the taxonomy of the agarics, p 197215. In Petersen RH (ed), Evolution in the Higher Basidiomycetes. University of Tennessee Press, Knoxville, TN.[PubMed]
51. Peintner U,, Bougher NL,, Castellano MA,, Moncalvo JM,, Moser MM,, Trappe JM,, Vilgalys R . 2001. Multiple origins of sequestrate fungi related to Cortinarius (Cortinariaceae). Am J Bot 88 : 21682179.[CrossRef] [PubMed]
52. Bodensteiner P,, Binder M,, Moncalvo JM,, Agerer R,, Hibbett DS . 2004. Phylogenetic relationships of cyphelloid homobasidiomycetes. Mol Phylogenet Evol 33 : 501515.[CrossRef] [PubMed]
53. Schmitt I, . 2011. Fruiting body evolution in the Ascomycota: a molecular perspective integrating lichenized and non-lichenized groups, p 187204. In Pöggeler S,, Wöstemeyer J (ed), The Mycota: Evolution of Fungi and Fungal-Like Organisms. Springer-Verlag, Berlin, Germany.
54. Kovacs GM,, Trappe JM, . 2014. Nomenclatural history and genealogies of desert truffles, p 2137. In Kagan-Zur V,, Roth-Bejerano N,, Sitrit Y,, Morte A (ed), Desert Truffles: Phylogeny, Physiology, Distribution and Domestication. Springer, Berlin Germany.[PubMed]
55. Kües U,, Liu Y . 2000. Fruiting body production in Basidiomycetes. Appl Microbiol Biotechnol 54 : 141152.[CrossRef] [PubMed]
56. Kües U . 2000. Life history and developmental processes in the basidiomycete Coprinus cinereus . Microbiol Mol Biol Rev 64 : 316353.[CrossRef] [PubMed]
57. Nagy LG,, Házi J,, Szappanos B,, Kocsubé S,, Bálint B,, Rákhely G,, Vágvölgyi C,, Papp T . 2012. The evolution of defense mechanisms correlate with the explosive diversification of autodigesting Coprinellus mushrooms (Agaricales, Fungi). Syst Biol 61 : 595607.[CrossRef] [PubMed]
58. Clémencon H,, Emmett V,, Emmett EE (ed). 2004. Cytology and Plectology of Hymenomycetes. J Cramer, Berlin, Germany.
59. Singer R . 1986. The Agaricales in Modern Taxonomy, 4th ed. Koeltz Scientific Books, Koenigstein, Germany.
60. Thiers HD . 1984. The secotioid syndrome. Mycologia 76 : 18.[CrossRef]
61. Bahn YS,, Xue C,, Idnurm A,, Rutherford JC,, Heitman J,, Cardenas ME . 2007. Sensing the environment: lessons from fungi. Nat Rev Microbiol 5 : 5769.[CrossRef] [PubMed]
62. Kamada T,, Sano H,, Nakazawa T,, Nakahori K . 2010. Regulation of fruiting body photomorphogenesis in Coprinopsis cinerea . Fungal Genet Biol 47 : 917921.[CrossRef] [PubMed]
63. Bayram O,, Krappmann S,, Ni M,, Bok JW,, Helmstaedt K,, Valerius O,, Braus-Stromeyer S,, Kwon NJ,, Keller NP,, Yu JH,, Braus GH . 2008. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320 : 15041506.[CrossRef] [PubMed]
64. Bayram O,, Braus GH . 2012. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36 : 124.[CrossRef] [PubMed]
65. Kück U,, Beier AM,, Teichert I . 2016. The composition and function of the striatin-interacting phosphatases and kinases (STRIPAK) complex in fungi. Fungal Genet Biol 90 : 3138.[CrossRef] [PubMed]
66. Frey S . 2015. The STRIPAK Complex and Its Role in Fruiting-Body Development of the Filamentous Fungus Sordaria macrospora . Georg-August University School of Science, Göttingen, Germany.
67. Ohm RA,, de Jong JF,, de Bekker C,, Wösten HA,, Lugones LG . 2011. Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation. Mol Microbiol 81 : 14331445.[CrossRef] [PubMed]
68. Ohm RA,, de Jong JF,, Lugones LG,, Aerts A,, Kothe E,, Stajich JE,, de Vries RP,, Record E,, Levasseur A,, Baker SE,, Bartholomew KA,, Coutinho PM,, Erdmann S,, Fowler TJ,, Gathman AC,, Lombard V,, Henrissat B,, Knabe N,, Kües U,, Lilly WW,, Lindquist E,, Lucas S,, Magnuson JK,, Piumi F,, Raudaskoski M,, Salamov A,, Schmutz J,, Schwarze FW,, vanKuyk PA,, Horton JS,, Grigoriev IV,, Wösten HA . 2010. Genome sequence of the model mushroom Schizophyllum commune . Nat Biotechnol 28 : 957963.[CrossRef] [PubMed]
69. Masloff S,, Pöggeler S,, Kück U . 1999. The pro1(+) gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152 : 191199.[PubMed]
70. Traeger S,, Altegoer F,, Freitag M,, Gabaldon T,, Kempken F,, Kumar A,, Marcet-Houben M,, Pöggeler S,, Stajich JE,, Nowrousian M . 2013. The genome and development-dependent transcriptomes of Pyronema confluens: a window into fungal evolution. PLoS Genet 9 : e1003820.[CrossRef] [PubMed]
71. Boulianne RP,, Liu Y,, Aebi M,, Lu BC,, Kües U . 2000. Fruiting body development in Coprinus cinereus: regulated expression of two galectins secreted by a non-classical pathway. Microbiology 146 : 18411853.[CrossRef] [PubMed]
72. Iijima N,, Yoshino H,, Ten LC,, Ando A,, Watanabe K,, Nagata Y . 2002. Two genes encoding fruit body lectins of Pleurotus cornucopiae: sequence similarity with the lectin of a nematode-trapping fungus. Biosci Biotechnol Biochem 66 : 20832089.[CrossRef] [PubMed]
73. Wösten HAB . 2001. Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55 : 625646.[CrossRef] [PubMed]
74. Floudas D , , et al . 2012. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336 : 17151719.[CrossRef] [PubMed]
75. Nagy LG,, Riley R,, Tritt A,, Adam C,, Daum C,, Floudas D,, Sun H,, Yadav JS,, Pangilinan J,, Larsson KH,, Matsuura K,, Barry K,, Labutti K,, Kuo R,, Ohm RA,, Bhattacharya SS,, Shirouzu T,, Yoshinaga Y,, Martin FM,, Grigoriev IV,, Hibbett DS . 2016. Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Mol Biol Evol 33 : 959970.[CrossRef] [PubMed]
76. Riley R,, Salamov AA,, Brown DW,, Nagy LG,, Floudas D,, Held BW,, Levasseur A,, Lombard V,, Morin E,, Otillar R,, Lindquist EA,, Sun H,, LaButti KM,, Schmutz J,, Jabbour D,, Luo H,, Baker SE,, Pisabarro AG,, Walton JD,, Blanchette RA,, Henrissat B,, Martin F,, Cullen D,, Hibbett DS,, Grigoriev IV . 2014. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci USA 111 : 99239928.[CrossRef] [PubMed]
77. Floudas D,, Held BW,, Riley R,, Nagy LG,, Koehler G,, Ransdell AS,, Younus H,, Chow J,, Chiniquy J,, Lipzen A,, Tritt A,, Sun H,, Haridas S,, LaButti K,, Ohm RA,, Kües U,, Blanchette RA,, Grigoriev IV,, Minto RE,, Hibbett DS . 2015. Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii . Fungal Genet Biol 76 : 7892.[CrossRef] [PubMed]
78. Martinez D , , et al . 2009. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106 : 19541959.[CrossRef] [PubMed]
79. Martinez D,, Larrondo LF,, Putnam N,, Gelpke MD,, Huang K,, Chapman J,, Helfenbein KG,, Ramaiya P,, Detter JC,, Larimer F,, Coutinho PM,, Henrissat B,, Berka R,, Cullen D,, Rokhsar D . 2004. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22 : 695700.[CrossRef] [PubMed]
80. Berbee ML,, Taylor JW . 2010. Dating the molecular clock in fungi: how close are we? Fungal Biol Rev 24 : 116.[CrossRef]
81. Beimforde C,, Feldberg K,, Nylinder S,, Rikkinen J,, Tuovila H,, Dörfelt H,, Gube M,, Jackson DJ,, Reitner J,, Seyfullah LJ,, Schmidt AR . 2014. Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol Phylogenet Evol 78 : 386398.[CrossRef] [PubMed]
82. Chang Y,, Wang S,, Sekimoto S,, Aerts AL,, Choi C,, Clum A,, LaButti KM,, Lindquist EA,, Yee Ngan C,, Ohm RA,, Salamov AA,, Grigoriev IV,, Spatafora JW,, Berbee ML . 2015. Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7 : 15901601.[CrossRef] [PubMed]
83. Robinson JM . 1990. Lignin, land plants, and fungi: biological evolution affecting Phanerozoic oxygen balance. Geology 18 : 607610.[CrossRef]
84. Eastwood DC, . 2014. Evolution of fungal wood decay, p 93112. In Schultz TP,, Goodell B,, Nicholas DD (ed). Deterioration and Protection of Sustainable Biomaterials. ACS Symposium Series. American Chemical Society, Washington, DC.
85. Cragg SM,, Beckham GT,, Bruce NC,, Bugg TD,, Distel DL,, Dupree P,, Etxabe AG,, Goodell BS,, Jellison J,, McGeehan JE,, McQueen-Mason SJ,, Schnorr K,, Walton PH,, Watts JE,, Zimmer M . 2015. Lignocellulose degradation mechanisms across the tree of life. Curr Opin Chem Biol 29 : 108119.[CrossRef] [PubMed]
86. Hibbett DS,, Donoghue MJ . 2001. Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50 : 215242.[CrossRef] [PubMed]
87. Rytioja J,, Hildén K,, Yuzon J,, Hatakka A,, de Vries RP,, Mäkelä MR . 2014. Plant-polysaccharide-degrading enzymes from Basidiomycetes. Microbiol Mol Biol Rev 78 : 614649.[CrossRef] [PubMed]
88. Ruiz-Dueñas FJ,, Lundell T,, Floudas D,, Nagy LG,, Barrasa JM,, Hibbett DS,, Martínez AT . 2013. Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia 105 : 14281444.[CrossRef] [PubMed]
89. Ruiz-Dueñas FJ,, Martínez AT . 2009. Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2 : 164177.[CrossRef] [PubMed]
90. Vaaje-Kolstad G,, Westereng B,, Horn SJ,, Liu Z,, Zhai H,, Sørlie M,, Eijsink VG . 2010. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330 : 219222.[CrossRef] [PubMed]
91. Morgenstern I,, Powlowski J,, Tsang A . 2014. Fungal cellulose degradation by oxidative enzymes: from dysfunctional GH61 family to powerful lytic polysaccharide monooxygenase family. Brief Funct Genomics 13 : 471481.[PubMed]
92. van den Brink J,, de Vries RP . 2011. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol 91 : 14771492.[CrossRef] [PubMed]
93. Ruiz-Dueñas FJ,, Fernández E,, Martínez MJ,, Martínez AT . 2011. Pleurotus ostreatus heme peroxidases: an in silico analysis from the genome sequence to the enzyme molecular structure. C R Biol 334 : 795805.[CrossRef] [PubMed]
94. Martinez AT,, Speranza M,, Ruiz-Duenas FJ,, Ferreira P,, Camarero S,, Guillen F , , et al . 2005. Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8 : 195204.[PubMed]
95. Firn RD,, Jones CG . 2003. Natural products: a simple model to explain chemical diversity. Nat Prod Rep 20 : 382391.[CrossRef] [PubMed]
96. Li YF,, Tsai KJ,, Harvey CJ,, Li JJ,, Ary BE,, Berlew EE,, Boehman BL,, Findley DM,, Friant AG,, Gardner CA,, Gould MP,, Ha JH,, Lilley BK,, McKinstry EL,, Nawal S,, Parry RC,, Rothchild KW,, Silbert SD,, Tentilucci MD,, Thurston AM,, Wai RB,, Yoon Y,, Aiyar RS,, Medema MH,, Hillenmeyer ME,, Charkoudian LK . 2016. Comprehensive curation and analysis of fungal biosynthetic gene clusters of published natural products. Fungal Genet Biol 89 : 1828.[CrossRef] [PubMed]
97. Lewis K . 2013. Platforms for antibiotic discovery. Nat Rev Drug Discov 12 : 371387.[CrossRef] [PubMed]
98. Inglis DO,, Binkley J,, Skrzypek MS,, Arnaud MB,, Cerqueira GC,, Shah P,, Wymore F,, Wortman JR,, Sherlock G . 2013. Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae . BMC Microbiol 13 : 91.[CrossRef] [PubMed]
99. Brakhage AA . 2013. Regulation of fungal secondary metabolism. Nat Rev Microbiol 11 : 2132.[CrossRef] [PubMed]
100. Wolpert TJ,, Dunkle LD,, Ciuffetti LM . 2002. Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40 : 251285.[CrossRef] [PubMed]
101. Brosch G,, Ransom R,, Lechner T,, Walton JD,, Loidl P . 1995. Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum . Plant Cell 7 : 19411950.[CrossRef] [PubMed]
102. Sharon A,, Elad Y,, Barakat R,, Tudzynski P, . 2007. Phytohormones in Botrytis-plant interactions, p 163179. In Elad Y,, Williamson B,, Tudzynski P,, Delen N (ed), Botrytis: Biology, Pathology and Control. Springer, Dordrecht, The Netherlands.[CrossRef]
103. Kosentka P,, Sprague SL,, Ryberg M,, Gartz J,, May AL,, Campagna SR,, Matheny PB . 2013. Evolution of the toxins muscarine and psilocybin in a family of mushroom-forming fungi. PLoS One 8 : e64646.[CrossRef] [PubMed]
104. Rohlfs M,, Albert M,, Keller NP,, Kempken F . 2007. Secondary chemicals protect mould from fungivory. Biol Lett 3 : 523525.[CrossRef] [PubMed]
105. Rudgers JA,, Clay K . 2007. Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21 : 107124.[CrossRef]
106. Soliman SS,, Greenwood JS,, Bombarely A,, Mueller LA,, Tsao R,, Mosser DD,, Raizada MN . 2015. An endophyte constructs fungicide-containing extracellular barriers for its host plant. Curr Biol 25 : 25702576.[CrossRef] [PubMed]
107. Arnold AE,, Mejía LC,, Kyllo D,, Rojas EI,, Maynard Z,, Robbins N,, Herre EA . 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100 : 1564915654.[CrossRef] [PubMed]
108. Hider RC,, Kong X . 2010. Chemistry and biology of siderophores. Nat Prod Rep 27 : 637657.[CrossRef] [PubMed]
109. Hwang LH,, Mayfield JA,, Rine J,, Sil A . 2008. Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization. PLoS Pathog 4 : e1000044.[CrossRef] [PubMed]
110. Mascuch SJ,, Moree WJ,, Hsu CC,, Turner GG,, Cheng TL,, Blehert DS,, Kilpatrick AM,, Frick WF,, Meehan MJ,, Dorrestein PC,, Gerwick L . 2015. Direct detection of fungal siderophores on bats with white-nose syndrome via fluorescence microscopy-guided ambient ionization mass spectrometry. PLoS One 10 : e0119668.[CrossRef] [PubMed]
111. Eisenman HC,, Casadevall A . 2012. Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol 93 : 931940.[CrossRef] [PubMed]
112. Smith ML,, Bruhn JN,, Anderson JB . 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356 : 428431.[CrossRef]
113. Nosanchuk JD,, Casadevall A . 2003. The contribution of melanin to microbial pathogenesis. Cell Microbiol 5 : 203223.[CrossRef] [PubMed]
114. Molnár K,, Farkas E . 2010. Current results on biological activities of lichen secondary metabolites: a review. Z Naturforsch C 65 : 157173.[CrossRef] [PubMed]
115. Hoffmeister D,, Keller NP . 2007. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24 : 393416.[CrossRef] [PubMed]
116. Walton JD,, Hallen-Adams HE,, Luo H . 2010. Ribosomal biosynthesis of the cyclic peptide toxins of Amanita mushrooms. Biopolymers 94 : 659664.[CrossRef] [PubMed]
117. Mitchell NJ,, Bowers E,, Hurburgh C,, Wu F . 2016. Potential economic losses to the US corn industry from aflatoxin contamination. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 33 : 540550.[CrossRef] [PubMed]
118. Endo A . 2010. A historical perspective on the discovery of statins. Proc Jpn Acad Ser B Phys Biol Sci 86 : 484493.[CrossRef] [PubMed]
119. Woloshuk CP,, Shim WB . 2013. Aflatoxins, fumonisins, and trichothecenes: a convergence of knowledge. FEMS Microbiol Rev 37 : 94109.[CrossRef] [PubMed]
120. Gallois A,, Gross B,, Langlois D,, Spinnler H-E,, Brunerie P . 1990. Influence of culture conditions on production of flavour compounds by 29 ligninolytic Basidiomycetes. Mycol Res 94 : 494504.[CrossRef]
121. Panaccione DG,, Beaulieu WT,, Cook D . 2014. Bioactive alkaloids in vertically transmitted fungal endophytes. Funct Ecol 28 : 299314.[CrossRef]
122. Araújo AM,, Carvalho F,, Bastos ML,, Guedes de Pinho P,, Carvalho M . 2015. The hallucinogenic world of tryptamines: an updated review. Arch Toxicol 89 : 11511173.[CrossRef] [PubMed]
123. Bidartondo MI,, Read DJ,, Trappe JM,, Merckx V,, Ligrone R,, Duckett JG . 2011. The dawn of symbiosis between plants and fungi. Biol Lett 7 : 574577.[CrossRef] [PubMed]
124. Keller NP,, Hohn TM . 1997. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21 : 1729.[CrossRef]
125. Gluck-Thaler E,, Slot JC . 2015. Dimensions of horizontal gene transfer in eukaryotic microbial pathogens. PLoS Pathog 11 : e1005156.[CrossRef] [PubMed]
126. Campbell MA,, Rokas A,, Slot JC . 2012. Horizontal transfer and death of a fungal secondary metabolic gene cluster. Genome Biol Evol 4 : 289293.[CrossRef] [PubMed]
127. Marcet-Houben M,, Gabaldón T . 2016. Horizontal acquisition of toxic alkaloid synthesis in a clade of plant associated fungi. Fungal Genet Biol 86 : 7180.[CrossRef] [PubMed]
128. Slot JC,, Rokas A . 2011. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21 : 134139.[CrossRef] [PubMed]
129. Bradshaw RE,, Slot JC,, Moore GG,, Chettri P,, de Wit PJ,, Ehrlich KC,, Ganley AR,, Olson MA,, Rokas A,, Carbone I,, Cox MP . 2013. Fragmentation of an aflatoxin-like gene cluster in a forest pathogen. New Phytol 198 : 525535.[CrossRef] [PubMed]
130. Heckman DS,, Geiser DM,, Eidell BR,, Stauffer RL,, Kardos NL,, Hedges SB . 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293 : 11291133.[CrossRef] [PubMed]
131. Frank B . 1885. Über die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Ber Dtsch Bot Ges 3 : 128145.
132. Trappe JMAB . 2005. A.B. Frank and mycorrhizae: the challenge to evolutionary and ecologic theory. Mycorrhiza 15 : 277281.[CrossRef] [PubMed]
133. Smith SE,, Read DJ . 2008. Mycorrhizal Symbiosis. Academic Press: San Diego, CA.
134. Brundrett MC . 2002. Coevolution of roots and mycorrhizas of land plants. New Phytol 154 : 275304.[CrossRef]
135. Brundrett MC . 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320 : 3777.[CrossRef]
136. Wang B,, Qiu YL . 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16 : 299363.[CrossRef] [PubMed]
137. Tedersoo L,, May TW,, Smith ME . 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20 : 217263.[CrossRef] [PubMed]
138. van der Heijden MG,, Martin FM,, Selosse MA,, Sanders IR . 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205 : 14061423.[CrossRef] [PubMed]
139. Read DJ,, Perez-Moreno J . 2003. Mycorrhizas and nutrient cycling in ecosystems: a journey towards relevance? New Phytol 157 : 475492.[CrossRef]
140. Vohník M,, Sadowsky JJ,, Kohout P,, Lhotáková Z,, Nestby R,, Kolařík M . 2012. Novel root-fungus symbiosis in Ericaceae: sheathed ericoid mycorrhiza formed by a hitherto undescribed basidiomycete with affinities to Trechisporales. PLoS One 7 : e39524.[CrossRef] [PubMed]
141. Peterson RL,, Massicotte HB,, Melville LH . 2004. Mycorrhizas: Anatomy and Cell Biology. National Research Council of Canada, Ottawa, Canada.
142. Cameron DD,, Leake JR,, Read DJ . 2006. Mutualistic mycorrhiza in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens . New Phytol 171 : 405416.[CrossRef] [PubMed]
143. Kottke I , , et al . 2010. Atractiellomycetes belonging to the ‘rust’ lineage (Pucciniomycotina) form mycorrhizae with terrestrial and epiphytic neotropical orchids. Proc Biol Sci 277 : 12891298.[PubMed]
144. Fitter AH,, Moyersoen B . 1996. Evolutionary trends in root-microbe symbioses. Philos Trans R Soc Lond, B 351 : 13671375.[CrossRef]
145. Brachmann A,, Parniske M . 2006. The most widespread symbiosis on Earth. PLoS Biol 4 : e239.[CrossRef] [PubMed]
146. Pagano MC,, Oehl F,, Silva GA,, Maia LC,, Silva DK,, Cabello MN, . 2016. Advances in arbuscular mycorrhizal taxonomy, p 1521. In Pagano M (ed), Recent Advances on Mycorrhizal Fungi. Springer, Cham, Switzerland.[CrossRef]
147. Tisserant E,, Malbreil M,, Kuo A,, Kohler A,, Symeonidi A,, Balestrini R,, Charron P,, Duensing N,, Frei dit Frey N,, Gianinazzi-Pearson V,, Gilbert LB,, Handa Y,, Herr JR,, Hijri M,, Koul R,, Kawaguchi M,, Krajinski F,, Lammers PJ,, Masclaux FG,, Murat C,, Morin E,, Ndikumana S,, Pagni M,, Petitpierre D,, Requena N,, Rosikiewicz P,, Riley R,, Saito K,, San Clemente H,, Shapiro H,, van Tuinen D,, Bécard G,, Bonfante P,, Paszkowski U,, Shachar-Hill YY,, Tuskan GA,, Young JP,, Sanders IR,, Henrissat B,, Rensing SA,, Grigoriev IV,, Corradi N,, Roux C,, Martin F . 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110 : 2011720122.[CrossRef] [PubMed]
148. Ropars J,, Toro KS,, Noel J,, Pelin A,, Charron P,, Farinelli L,, Marton T,, Krüger M,, Fuchs J,, Brachmann A,, Corradi N . 2016. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol 1 : 16033.[CrossRef] [PubMed]
149. Bonfante P,, Genre A . 2015. Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20 : 150154.[CrossRef] [PubMed]
150. Parniske M . 2000. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3 : 320328.[CrossRef]
151. Huisman R,, Bouwmeester K,, Brattinga M,, Govers F,, Bisseling T,, Limpens E . 2015. Haustorium formation in Medicago truncatula roots infected by Phytophthora palmivora does not involve the common endosymbiotic program shared by arbuscular mycorrhizal fungi and rhizobia. Mol Plant Microbe Interact 28 : 12711280.[CrossRef] [PubMed]
152. Stubblefield SP,, Taylor TN,, Trappe JM . 1987. Fossil mycorrhizae: a case for symbiosis. Science 237 : 5960.[CrossRef] [PubMed]
153. Remy W,, Taylor TN,, Hass H,, Kerp H . 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91 : 1184111843.[CrossRef] [PubMed]
154. Redecker D,, Kodner R,, Graham LE . 2000. Glomalean fungi from the Ordovician. Science 289 : 19201921.[CrossRef] [PubMed]
155. Duckett JG,, Carafa A,, Ligrone R . 2006. A highly differentiated glomeromycotean association with the mucilage-secreting, primitive antipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. Am J Bot 93 : 797813.[CrossRef] [PubMed]
156. Russell J,, Bulman S . 2005. The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165 : 567579.[CrossRef] [PubMed]
157. Krings M,, Taylor TN,, Hass H,, Kerp H,, Dotzler N,, Hermsen EJ . 2007. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174 : 648657.[CrossRef] [PubMed]
158. Ligrone R,, Carafa A,, Lumini E,, Bianciotto V,, Bonfante P,, Duckett JG . 2007. Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94 : 17561777.[CrossRef] [PubMed]
159. Pirozynski KA,, Malloch DW . 1975. The origin of land plants: a matter of mycotrophism. Biosystems 6 : 153164.[CrossRef]
160. Spatafora JW,, Chang Y,, Benny GL,, Lazarus K,, Smith ME,, Berbee ML,, Bonito G,, Corradi N,, Grigoriev I,, Gryganskyi A,, James TY,, O’Donnell K,, Roberson RW,, Taylor TN,, Uehling J,, Vilgalys R,, White MM,, Stajich JE . 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108 : 10281046.[CrossRef] [PubMed]
161. Redecker D,, Raab P . 2006. Phylogeny of the glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98 : 885895.[CrossRef] [PubMed]
162. Lee J,, Young JP . 2009. The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytol 183 : 200211.[CrossRef] [PubMed]
163. Lin K,, Limpens E,, Zhang Z,, Ivanov S,, Saunders DG,, Mu D,, Pang E,, Cao H,, Cha H,, Lin T,, Zhou Q,, Shang Y,, Li Y,, Sharma T,, van Velzen R,, de Ruijter N,, Aanen DK,, Win J,, Kamoun S,, Bisseling T,, Geurts R,, Huang S . 2014. Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10 : e1004078.[CrossRef] [PubMed]
164. Desiro A,, Duckett JG,, Pressel S,, Villarreal JC,, Bidartondo MI . 2013. Fungal symbioses in hornworts: a chequered history. Proc Biol Sci 280 : 20130207.[PubMed]
165. Field KJ,, Rimington WR,, Bidartondo MI,, Allinson KE,, Beerling DJ,, Cameron DD,, Duckett JG,, Leake JR,, Pressel S . 2015. First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytol 205 : 743756.[CrossRef] [PubMed]
166. Field KJ,, Rimington WR,, Bidartondo MI,, Allinson KE,, Beerling DJ,, Cameron DD,, Duckett JG,, Leake JR,, Pressel S . 2016. Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. ISME J 10 : 15141526.[CrossRef] [PubMed]
167. Strullu-Derrien C,, Kenrick P,, Pressel S,, Duckett JG,, Rioult JP,, Strullu DG . 2014. 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. New Phytol 203 : 964979.[CrossRef] [PubMed]
168. Bravo A,, York T,, Pumplin N,, Mueller LA,, Harrison MJ . 2016. Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2 : 15208.[CrossRef] [PubMed]
169. Martin F,, Kohler A,, Murat C,, Veneault-Fourrey C,, Hibbett DS . 2016. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 14 : 760773.[CrossRef] [PubMed]
170. Kottke I,, Kovács GM, . 2013. Mycorrhizae-rhizosphere determinants of plant communities: what can we learn from the tropics? p 40-140-13. In Eshel A,, Beeckman T (ed), Plant Roots: The Hidden Half, 4th ed. CRC Press, Boca Raton, FL.
171. Kottke I,, Oberwinkler F . 1987. The cellular structure of the Hartig net: coenocytic and transfer cell-like organization. Nord J Bot 7 : 8595.[CrossRef]
172. Agerer R . 2001. Exploration types of ectomycorrhizae. Mycorrhiza 11 : 107114.[CrossRef]
173. Kohler A , , et al, Mycorrhizal Genomics Initiative Consortium . 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47 : 410415.[CrossRef] [PubMed]
174. Martin F , , et al . 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464 : 10331038.[CrossRef] [PubMed]
175. Plett JM,, Martin F . 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends Genet 27 : 1422.[CrossRef] [PubMed]
176. Kuo A,, Kohler A,, Martin FM,, Grigoriev IV . 2014. Expanding genomics of mycorrhizal symbiosis. Front Microbiol 5 : 582.[CrossRef] [PubMed]
177. Plett JM,, Daguerre Y,, Wittulsky S,, Vayssières A,, Deveau A,, Melton SJ,, Kohler A,, Morrell-Falvey JL,, Brun A,, Veneault-Fourrey C,, Martin F . 2014. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci USA 111 : 82998304.[CrossRef] [PubMed]
178. Plett JM,, Martin F . 2015. Reconsidering mutualistic plant-fungal interactions through the lens of effector biology. Curr Opin Plant Biol 26 : 4550.[CrossRef] [PubMed]
179. Trappe JM . 1996. What is a mycorrhiza?, p 36. In Mycorrhizas in Integrated Systems from Genes to Plant Development. Proceedings of the 4th European Symposium on Mycorrhizas. European Commission, Directorate-General XII, Science, Research and Development, Brussels, Belgium.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error