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Annual Review of Phytopathology

Volume 56, 2018

Biology of Fungi and Their Bacterial Endosymbionts

Abstract

Heritable symbioses, in which endosymbiotic bacteria (EB) are transmitted vertically between host generations, are an important source of evolutionary novelties. A primary example of such symbioses is the eukaryotic cell with its EB-derived organelles. Recent discoveries suggest that endosymbiosis-related innovations can be also found in associations formed by early divergent fungi in the phylum Mucoromycota with heritable EB from two classes, Betaproteobacteria and Mollicutes. These symbioses exemplify novel types of host-symbiont interactions. Studies of these partnerships fuel theoretical models describing mechanisms that stabilize heritable symbioses, control the rate of molecular evolution, and enable the establishment of mutualisms. Lastly, by altering host phenotypes and metabolism, these associations represent an important instrument for probing the basic biology of the Mucoromycota hosts, which remain one of the least explored filamentous fungi.

Keyword(s): arbuscular mycorrhizal fungi, Mycoavidus cysteinexigens, Rhizopus microsporus, ‘Candidatus Glomeribacter gigasporarum,’ ‘Candidatus Moeniiplasma glomeromycotorum,’ Mortierella elongata
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2018-08-25
2024-04-18
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Literature Cited

  1. 1.  Aanen DK, Hoekstra RF 2007. The evolution of obligate mutualism: If you can't beat 'em, join 'em. Trends Ecol. Evol. 22:506–9
     [Google Scholar]
  2. 2.  Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402–7
     [Google Scholar]
  3. 3.  Anca IA, Lumini E, Ghignone S, Salvioli A, Bianciotto V, Bonfante P 2009. The ftsZ gene of the endocellular bacterium ‘Candidatus Glomeribacter gigasporarum’ is preferentially expressed during the symbiotic phases of its host mycorrhizal fungus. Mol. Plant-Microbe Interact. 22:302–10
     [Google Scholar]
  4. 4.  Axelrod R, Hamilton WD 1981. The evolution of cooperation. Science 211:1390–96
     [Google Scholar]
  5. 5.  Benjamin RK, Mehrotra BS 1963. Obligate azygospore formation in two species of Mucor (Mucorales). Aliso J. Syst. Evol. Bot. 5:235–45
     [Google Scholar]
  6. 6.  Bennett GM, Moran NA 2013. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol. Evol. 5:1675–88
     [Google Scholar]
  7. 7.  Bennett GM, Moran NA 2015. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. PNAS 112:10169–76
     [Google Scholar]
  8. 8.  Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A et al. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLOS Biol 4:e226
     [Google Scholar]
  9. 9.  Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P 1996. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl. Environ. Microbiol. 62:3005–10
     [Google Scholar]
  10. 10.  Bianciotto V, Genre A, Jargeat P, Lumini E, Becard G, Bonfante P 2004. Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl. Environ. Microbiol. 70:3600–8
     [Google Scholar]
  11. 11.  Bianciotto V, Lumini E, Bonfante P, Vandamme P 2003. ‘Candidatus Glomeribacter gigasporarum’ gen. nov., sp nov., an endosymbiont of arbuscular mycorrhizal fungi. Int. J. Syst. Evol. Microbiol. 53:121–24
     [Google Scholar]
  12. 12.  Bianciotto V, Lumini E, Lanfranco L, Minerdi D, Bonfante P, Perotto S 2000. Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl. Environ. Microbiol. 66:4503–9
     [Google Scholar]
  13. 13.  Birky CW Jr. 1995. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. PNAS 92:11331–38
     [Google Scholar]
  14. 14.  Blow MJ, Clark TA, Daum CG, Deutschbauer AM, Fomenkov A et al. 2016. The epigenomic landscape of prokaryotes. PLOS Genet 12:e1005854
     [Google Scholar]
  15. 15.  Bonfante P, Desirò A 2017. Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. ISME J 11:1727–35
     [Google Scholar]
  16. 16.  Bonito G, Hameed K, Ventura R, Krishnan J, Schadt CW, Vilgalys R 2016. Isolating a functionally relevant guild of fungi from the root microbiome of Populus. . Fungal Ecol 22:35–42
     [Google Scholar]
  17. 17.  Bravo A, Brands M, Wewer V, Dormann P, Harrison MJ 2017. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol 214:1631–45
     [Google Scholar]
  18. 18.  Bull JJ, Rice WR 1991. Distinguishing mechanisms for the evolution of cooperation. J. Theor. Biol. 149:63–74
     [Google Scholar]
  19. 19.  Canbäck B, Tamas I, Andersson SGE 2004. A phylogenomic study of endosymbiotic bacteria. Mol. Biol. Evol. 21:1110–22
     [Google Scholar]
  20. 20.  Castillo DM, Pawlowska TE 2010. Molecular evolution in bacterial endosymbionts of fungi. Mol. Biol. Evol. 27:622–36
     [Google Scholar]
  21. 21.  Connor RC 1986. Pseudo-reciprocity: investing in mutualism. Anim. Behav. 34:1562–84
     [Google Scholar]
  22. 22.  Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A et al. 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13:343–59
     [Google Scholar]
  23. 23.  Croll D, Sanders IR 2009. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evol. Biol. 9:13
     [Google Scholar]
  24. 24.  den Bakker HC, Vankuren NW, Morton JB, Pawlowska TE 2010. Clonality and recombination in the life history of an asexual arbuscular mycorrhizal fungus. Mol. Biol. Evol. 27:2474–86
     [Google Scholar]
  25. 25.  Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P 2015. Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol 205:1464–72
     [Google Scholar]
  26. 26.  Desirò A, Hao Z, Liber JA, Benucci GMN, Lowry D et al. 2018. Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle. ISME J https://doi.org/10.1038/s41396-018-0053-9
    [Crossref]
  27. 27.  Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S et al. 2014. Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME J 8:257–70
     [Google Scholar]
  28. 28.  Doebeli M, Knowlton N 1998. The evolution of interspecific mutualisms. PNAS 95:8676–80
     [Google Scholar]
  29. 29.  Fine PEM 1975. Vectors and vertical transmission: an epidemiologic perspective. Ann. N. Y. Acad. Sci. 266:173–94
     [Google Scholar]
  30. 30.  Frank SA 1996. Host control of symbiont transmission: the separation of symbionts into germ and soma. Am. Nat. 148:1113–24
     [Google Scholar]
  31. 31.  Frank SA 1996. Host-symbiont conflict over the mixing of symbiotic lineages. Proc. R. Soc. Lond. Ser. B 263:339–44
     [Google Scholar]
  32. 32.  Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A 2011. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 75:583–609
     [Google Scholar]
  33. 33.  Fu Y, Luo GZ, Chen K, Deng X, Yu M et al. 2015. N6-methyldeoxyadenosine marks active transcription start sites in Chlamydomonas. . Cell 161:879–92
     [Google Scholar]
  34. 34.  Fujimura R, Nishimura A, Ohshima S, Sato Y, Nishizawa T et al. 2014. Draft genome sequence of the betaproteobacterial endosymbiont associated with the fungus Mortierella elongata FMR23–6. Genome Announc 2:e01272–14
     [Google Scholar]
  35. 35.  Funk DJ, Wernegreen JJ, Moran NA 2001. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157:477–89
     [Google Scholar]
  36. 36.  Gams W, Chien C-Y, Domsch KH 1972. Zygospore formation by the heterothallic Mortierella elongata and a related homothallic species, M. epigama sp.nov. Trans. Br. Mycol. Soc. 58:5–13
     [Google Scholar]
  37. 37.  Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G et al. 2012. The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6:136–45
     [Google Scholar]
  38. 38.  Ginman A, Young TWK 1989. Azygospore morphology in Mucor azygospora and M. bainieri. Mycol. . Res 93:314–20
     [Google Scholar]
  39. 39.  Gourlay CW, Ayscough KR 2006. Actin-induced hyperactivation of the Ras signaling pathway leads to apoptosis in Saccharomyces cerevisiae. Mol. Cell. . Biol 26:6487–501
     [Google Scholar]
  40. 40.  Greer EL, Blanco MA, Gu L, Sendinc E, Liu J et al. 2015. DNA methylation on N6-adenine in C. elegans. . Cell 161:868–78
     [Google Scholar]
  41. 41.  Gyllenberg M, Preoteasa D, Saikkonen K 2002. Vertically transmitted symbionts in structured host metapopulations. Bull. Math. Biol. 64:959–78
     [Google Scholar]
  42. 42.  Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N 2011. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–23
     [Google Scholar]
  43. 43.  Herre EA, Knowlton N, Mueller UG, Rehner SA 1999. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14:49–53
     [Google Scholar]
  44. 44.  Jany JL, Pawlowska TE 2010. Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota. Am. Nat. 175:424–35
     [Google Scholar]
  45. 45.  Jiang Y, Wang W, Xie Q, Liu N, Liu L et al. 2017. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–75
     [Google Scholar]
  46. 46.  Kalleda N, Naorem A, Manchikatla RV 2013. Targeting fungal genes by diced siRNAs: a rapid tool to decipher gene function in Aspergillus nidulans. . PLOS ONE 8:e75443
     [Google Scholar]
  47. 47.  Kana-uchi A, Yamashiro CT, Tanabe S, Murayama T 1997. A ras homologue of Neurospora crassa regulates morphology. Mol. Gen. Genet. 254:427–32
     [Google Scholar]
  48. 48.  Keller NP, Turner G, Bennett JW 2005. Fungal secondary metabolism: from biochemistry to genomics. Nat. Rev. Microbiol. 3:937–47
     [Google Scholar]
  49. 49.  Keymer A, Pimprikar P, Wewer V, Huber C, Brands M et al. 2017. Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife 6:e29107
     [Google Scholar]
  50. 50.  Koziol MJ, Bradshaw CR, Allen GE, Costa ASH, Frezza C, Gurdon JB 2016. Identification of methylated deoxyadenosines in vertebrates reveals diversity in DNA modifications. Nat. Struct. Mol. Biol. 23:24–30
     [Google Scholar]
  51. 51.  Kumar S, Stecher G, Tamura K 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870–74
     [Google Scholar]
  52. 52.  Lackner G, Moebius N, Hertweck C 2011. Endofungal bacterium controls its host by an hrp type III secretion system. ISME J 5:252–61
     [Google Scholar]
  53. 53.  Lackner G, Moebius N, Partida-Martinez L, Hertweck C 2011. Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J. . Bacteriol 193:783–84
     [Google Scholar]
  54. 54.  Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C 2011. Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genom 12:210
     [Google Scholar]
  55. 55.  Lanfranco L, Fiorilli V, Venice F, Bonfante P 2017. Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J. Exp. Bot. 69:2175–88
     [Google Scholar]
  56. 56.  Lastovetsky OA, Gaspar ML, Mondo SJ, LaButti KM, Sandor L et al. 2016. Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria. PNAS 113:15102–7Host lipid metabolism plays a role in the establishment of the Rm-Burkholderia mutualism. Some lipid metabolic genes active in this process are only found in early divergent fungi.
     [Google Scholar]
  57. 57.  Law R 1985. Evolution in a mutualistic environment. The Biology of Mutualism. Ecology and Evolution DH Boucher 145–70 New York: Oxford Univ. Press
     [Google Scholar]
  58. 58.  Law R, Lewis DH 1983. Biotic environments and the maintenance of sex: some evidence from mutualistic symbioses. Biol. J. Linn. Soc. 20:249–76
     [Google Scholar]
  59. 59.  Lee N, Kronstad JW 2002. ras2 controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. . Eukaryot. Cell 1:954–66
     [Google Scholar]
  60. 60.  Li Z, Yao Q, Dearth SP, Entler MR, Castro Gonzalez HF et al. 2017. Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system. Environ. Microbiol. 19:1041–53
     [Google Scholar]
  61. 61.  Lipsitch M, Nowak MA, Ebert D, May RM 1995. The population dynamics of vertically and horizontally transmitted parasites. Proc. R. Soc. Lond. Ser. B 260:321–27
     [Google Scholar]
  62. 62.  Lipsitch M, Siller S, Nowak MA 1996. The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50:1729–41
     [Google Scholar]
  63. 63.  Lively CM, Clay K, Wade MJ, Fuqua C 2005. Competitive co-existence of vertically and horizontally transmitted parasites. Evol. Ecol. Res. 7:1183–90
     [Google Scholar]
  64. 64.  Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV et al. 2017. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356:1175–78
     [Google Scholar]
  65. 65.  Lumini E, Bianciotto V, Jargeat P, Novero M, Salvioli A et al. 2007. Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria. Cell. Microbiol. 9:1716–29
     [Google Scholar]
  66. 66.  Luo G-Z, Blanco MA, Greer EL, He C, Shi Y 2015. DNA N6-methyladenine: a new epigenetic mark in eukaryotes?. Nat. Rev. Mol. Cell Biol. 16:705–10
     [Google Scholar]
  67. 67.  Luo G-Z, Wang F, Weng X, Chen K, Hao Z et al. 2016. Characterization of eukaryotic DNA N6-methyladenine by a highly sensitive restriction enzyme-assisted sequencing. Nat. Commun. 7:11301
     [Google Scholar]
  68. 68.  McCutcheon JP, Moran NA 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13–26
     [Google Scholar]
  69. 69.  Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C 2014. Active invasion of bacteria into living fungal cells. eLife 3:e03007
     [Google Scholar]
  70. 70.  Mondo SJ, Dannebaum RO, Kuo RC, Louie KB, Bewick AJ et al. 2017. Widespread adenine N6-methylation of active genes in fungi. Nat. Genet. 49:964–68The 6mA DNA modification, which is common in bacteria, is also found in early divergent fungi and plays a role in gene activation.
     [Google Scholar]
  71. 71.  Mondo SJ, Lastovetsky OA, Gaspar ML, Schwardt NH, Barber CC et al. 2017. Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi. Nat. Commun. 8:1843Burkholderia EB interact with sexual reproduction in Rm. This interaction revealed candidate receptors of trisporic acids, mating pheromones unique to Mucoromycotina.
     [Google Scholar]
  72. 72.  Mondo SJ, Salvioli A, Bonfante P, Morton JB, Pawlowska TE 2016. Nondegenerative evolution in ancient heritable bacterial endosymbionts of fungi. Mol. Biol. Evol. 33:2216–31In contrast to degenerately evolving heritable essential EB of insects, genome evolution in CaGg is nondegenerative.
     [Google Scholar]
  73. 73.  Mondo SJ, Toomer KH, Morton JB, Lekberg Y, Pawlowska TE 2012. Evolutionary stability in a 400-million-year-old heritable facultative mutualism. Evolution 66:2564–76
     [Google Scholar]
  74. 74.  Moran NA 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. PNAS 93:2873–78
     [Google Scholar]
  75. 75.  Moran NA, Bennett GM 2014. The tiniest tiny genomes. Annu. Rev. Microbiol. 68:195–215
     [Google Scholar]
  76. 76.  Moran NA, McCutcheon JP, Nakabachi A 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165–90
     [Google Scholar]
  77. 77.  Moran NA, McLaughlin HJ, Sorek R 2009. The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379–82
     [Google Scholar]
  78. 78.  Moran NA, Mira A 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. . Genome Biol. 2:Research0054
     [Google Scholar]
  79. 79.  Muller HJ 1964. The relation of recombination to mutational advance. Mutation Res 1:2–9
     [Google Scholar]
  80. 80.  Naito M, Desirò A, Gonzalez JB, Tao G, Bonfante P et al. 2017. ‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi. Int. J. Syst. Evol. Microbiol. 67:1177–84
     [Google Scholar]
  81. 81.  Naito M, Morton JB, Pawlowska TE 2015. Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota. PNAS 112:7791–96
     [Google Scholar]
  82. 82.  Naito M, Pawlowska TE 2016. Defying Muller's ratchet: heritable endobacteria escape extinction through recombination and genome plasticity. mBio 7:e02057–15Genome plasticity counters genomic degeneration in CaMg.
     [Google Scholar]
  83. 83.  Naito M, Pawlowska TE 2016. The role of mobile genetic elements in evolutionary longevity of heritable endobacteria. Mob. Genet. Elem. 6:e1136375
     [Google Scholar]
  84. 84.  Naumann M, Schüßler A, Bonfante P 2010. The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4:862–71
     [Google Scholar]
  85. 85.  Nilsson AI, Koskiniemi S, Eriksson S, Kugelberg E, Hinton JCD, Andersson DI 2005. Bacterial genome size reduction by experimental evolution. PNAS 102:12112–16
     [Google Scholar]
  86. 86.  O'Fallon B 2008. Population structure, levels of selection, and the evolution of intracellular symbionts. Evolution 62:361–73
     [Google Scholar]
  87. 87.  Ohshima S, Sato Y, Fujimura R, Takashima Y, Hamada M et al. 2016. Mycoavidus cysteinexigens gen. nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata. . Int. J. Syst. Evol. Microbiol. 66:2052–57
     [Google Scholar]
  88. 88.  Ohta T 1972. Population size and rate of evolution. J. Mol. Evol. 1:305–14
     [Google Scholar]
  89. 89.  Ohta T 1973. Slightly deleterious mutant substitutions in evolution. Nature 246:96–98
     [Google Scholar]
  90. 90.  Olsson S, Bonfante P, Pawlowska TE 2017. Ecology and evolution of fungal-bacterial interactions. The Fungal Community: Its Organization and Role in the Ecosystem J Dighton, JF White 563–83 Boca Raton, FL: Taylor & Francis
     [Google Scholar]
  91. 91.  Orive ME 1993. Effective population size in organisms with complex life-histories. Theor. Popul. Biol. 44:316–40
     [Google Scholar]
  92. 92.  Otto SP, Orive ME 1995. Evolutionary consequences of mutation and selection within an individual. Genetics 141:1173–87
     [Google Scholar]
  93. 93.  Pannebakker BA, Loppin B, Elemans CP, Humblot L, Vavre F 2007. Parasitic inhibition of cell death facilitates symbiosis. PNAS 104:213–15
     [Google Scholar]
  94. 94.  Partida-Martinez LP, Bandemer S, Ruchel R, Dannaoui E, Hertweck C 2008. Lack of evidence of endosymbiotic toxin-producing bacteria in clinical Rhizopus isolates. Mycoses 51:266–69
     [Google Scholar]
  95. 95.  Partida-Martinez LP, Groth I, Schmitt I, Richter W, Roth M, Hertweck C 2007. Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus. . Int. J. Syst. Evol. Microbiol. 57:2583–90
     [Google Scholar]
  96. 96.  Partida-Martinez LP, Hertweck C 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–88
     [Google Scholar]
  97. 97.  Partida-Martinez LP, Monajembashi S, Greulich KO, Hertweck C 2007. Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr. Biol. 17:773–77
     [Google Scholar]
  98. 98.  Remy W, Taylor TN, Hass H, Kerp H 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. PNAS 91:11841–43
     [Google Scholar]
  99. 99.  Ropars J, Toro KS, Noel J, Pelin A, Charron P et al. 2016. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat. Microbiol. 1:16033
     [Google Scholar]
  100. 100.  Roth JR, Lawrence JG, Bobik TA 1996. Cobalamin (coenzyme B12): synthesis and biological significance. Annu. Rev. Microbiol. 50:137–81
     [Google Scholar]
  101. 101.  Roze D, Michod RE 2001. Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity. Am. Nat. 158:638–54
     [Google Scholar]
  102. 102.  Russell JA, Moran NA 2005. Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl. Environ. Microbiol. 71:7987–94
     [Google Scholar]
  103. 103.  Russell JA, Moran NA 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. B 273:603–10
     [Google Scholar]
  104. 104.  Sachs JL, Essenberg CJ, Turcotte MM 2011. New paradigms for the evolution of beneficial infections. Trends Ecol. Evol. 26:202–9
     [Google Scholar]
  105. 105.  Sachs JL, Mueller UG, Wilcox TP, Bull JJ 2004. The evolution of cooperation. Q. Rev. Biol. 79:135–60
     [Google Scholar]
  106. 106.  Saikkonen K, Ion D, Gyllenberg M 2002. The persistence of vertically transmitted fungi in grass metapopulations. Proc. R. Soc. Lond. Ser. B 269:1397–403
     [Google Scholar]
  107. 107.  Salvioli A, Chiapello M, Fontaine J, Hadj-Sahraoui AL, Grandmougin-Ferjani A et al. 2010. Endobacteria affect the metabolic profile of their host Gigaspora margarita, an arbuscular mycorrhizal fungus. Environ. Microbiol. 12:2083–95
     [Google Scholar]
  108. 108.  Salvioli A, Ghignone S, Novero M, Navazio L, Venice F et al. 2016. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10:130–44
     [Google Scholar]
  109. 109.  Scherlach K, Busch B, Lackner G, Paszkowski U, Hertweck C 2012. Symbiotic cooperation in the biosynthesis of a phytotoxin. Angew. Chem. 51:9615–18
     [Google Scholar]
  110. 110.  Schipper MAA 1976. Induced azygospore formation in Mucor (Rhizomucor) pusillus by Absidia corymbifera. . Antonie Van Leeuwenhoek 42:141–44
     [Google Scholar]
  111. 111.  Schipper MAA, Gauger W, Van Den Ende H 1985. Hybridization of Rhizopus species. Microbiology 131:2359–65
     [Google Scholar]
  112. 112.  Schmitt I, Partida-Martinez LP, Winkler R, Voigt K, Einax E et al. 2008. Evolution of host resistance in a toxin-producing bacterial-fungal alliance. ISME J 2:632–41
     [Google Scholar]
  113. 113.  Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86
     [Google Scholar]
  114. 114.  Silipo A, Leone MR, Lanzetta R, Parrilli M, Lackner G et al. 2012. Structural characterization of two lipopolysaccharide O-antigens produced by the endofungal bacterium Burkholderia sp. HKI-402 (B4). Carbohydr. Res. 347:95–98
     [Google Scholar]
  115. 115.  Smith SE, Read DJ 2008. Mycorrhizal Symbiosis New York: Academic
  116. 116.  Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME et al. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–46This paper placed AMF in the phylum Mucoromycota and inspired our speculations about the impact of EB on the reproductive biology of AMF.
     [Google Scholar]
  117. 117.  Tajima F 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607
     [Google Scholar]
  118. 118.  Tamas I, Klasson L, Canbäck B, Naslund AK, Eriksson AS et al. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376–79
     [Google Scholar]
  119. 119.  Tang N, San Clemente H, Roy S, Bécard G, Zhao B, Roux C 2016. A survey of the gene repertoire of Gigaspora rosea unravels conserved features among Glomeromycota for obligate biotrophy. Front. Microbiol. 7:233
     [Google Scholar]
  120. 120.  Thevenieau F, Nicaud J-M 2013. Microorganisms as sources of oils. OCL 20:D603
     [Google Scholar]
  121. 121.  Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A et al. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. PNAS 110:20117–22
     [Google Scholar]
  122. 122.  Toomer KH, Chen X, Naito M, Mondo SJ, den Bakker HC et al. 2015. Molecular evolution patterns reveal life history features of mycoplasma-related endobacteria associated with arbuscular mycorrhizal fungi. Mol. Ecol. 24:3485–500
     [Google Scholar]
  123. 123.  Torres-Cortés G, Ghignone S, Bonfante P, Schüßler A 2015. Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma-fungus association. PNAS 112:7785–90
     [Google Scholar]
  124. 124.  Trépanier M, Becard G, Moutoglis P, Willemot C, Gagné S et al. 2005. Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl. Environ. Microbiol. 71:5341–47
     [Google Scholar]
  125. 125.  Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal PK et al. 2017. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ. . Microbiol 19:2964–83
     [Google Scholar]
  126. 126.  Uzum Z, Silipo A, Lackner G, De Felice A, Molinaro A, Hertweck C 2015. Structure, genetics and function of an exopolysaccharide produced by a bacterium living within fungal hyphae. ChemBioChem 16:387–92
     [Google Scholar]
  127. 127.  Vannini C, Carpentieri A, Salvioli A, Novero M, Marsoni M et al. 2016. An interdomain network: The endobacterium of a mycorrhizal fungus promotes antioxidative responses in both fungal and plant hosts. New Phytol 211:265–75
     [Google Scholar]
  128. 128.  Weber OB 2014. Biofertilizers with arbuscular mycorrhizal fungi in agriculture. Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration ZM Solaiman, LK Abbott, A Varma 45–66 Berlin: Springer
     [Google Scholar]
  129. 129.  Wernegreen JJ, Moran NA 1999. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol. Biol. Evol. 16:83–97
     [Google Scholar]
  130. 130.  Wewer V, Brands M, Dörmann P 2014. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. . Plant J 79:398–412
     [Google Scholar]
  131. 131.  Weyl EG, Frederickson ME, Yu DW, Pierce NE 2010. Economic contract theory tests models of mutualism. PNAS 107:15712–16
     [Google Scholar]
  132. 132.  Winsor GL, Khaira B, Van Rossum T, Lo R, Whiteside MD, Brinkman FS 2008. The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24:2803–4
     [Google Scholar]
  133. 133.  Wöstemeyer J, Schimek C 2007. Trisporic acid and mating in Zygomycetes. Sex in Fungi: Molecular Determination and Evolutionary Implications J Heitman, JW Kronstad, JW Taylor, LA Casselton 431–43 Washington, DC: ASM Press
     [Google Scholar]
  134. 134.  Wu TP, Wang T, Seetin MG, Lai Y, Zhu S et al. 2016. DNA methylation on N6-adenine in mammalian embryonic stem cells. Nature 532:329–33
     [Google Scholar]
  135. 135.  Yamamura N 1993. Vertical transmission and evolution of mutualism from parasitism. Theor. Popul. Biol. 44:95–109
     [Google Scholar]
  136. 136.  Zhang G, Huang H, Liu D, Cheng Y, Liu X et al. 2015. N6-methyladenine DNA modification in Drosophila. . Cell 161:893–906
     [Google Scholar]
/content/journals/10.1146/annurev-phyto-080417-045914
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Biology of Fungi and Their Bacterial Endosymbionts
Annual Review of Phytopathology 56, 289 (2018); https://doi.org/10.1146/annurev-phyto-080417-045914
/content/journals/10.1146/annurev-phyto-080417-045914
/content/journals/10.1146/annurev-phyto-080417-045914
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