1932

Abstract

Gene transfer has been identified as a prevalent and pervasive phenomenon and an important source of genomic innovation in bacteria. The role of gene transfer in microbial eukaryotes seems to be of a reduced magnitude but in some cases can drive important evolutionary innovations, such as new functions that underpin the colonization of different niches. The aim of this review is to summarize published cases that support the hypothesis that horizontal gene transfer (HGT) has played a role in the evolution of phytopathogenic traits in fungi and oomycetes. Our survey of the literature identifies 46 proposed cases of transfer of genes that have a putative or experimentally demonstrable phytopathogenic function. When considering the life-cycle steps through which a pathogen must progress, the majority of the HGTs identified are associated with invading, degrading, and manipulating the host. Taken together, these data suggest HGT has played a role in shaping how fungi and oomycetes colonize plant hosts.

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2014-08-04
2024-06-21
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Literature Cited

  1. Adl SM, Simpson AG, Lane CE, Lukes J, Bass D. 1.  et al. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:429–93 [Google Scholar]
  2. Akagi Y, Akamatsu H, Otani H, Kodama M. 2.  2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot. Cell 8:1732–38Experimental demonstration of transfer of pathogenicity chromosomes between strains generating hybrids with expanded host range and pathogenic phenotypes. [Google Scholar]
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 3.  1990. Basic local alignment search tool. J. Mol. Biol. 215:403–10 [Google Scholar]
  4. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP. 4.  et al. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7:e1002230 [Google Scholar]
  5. Amsellem Z, Cohen BA, Gressel J. 5.  2002. Engineering hypervirulence in a mycoherbicidal fungus for efficient weed control. Nat. Biotechnol. 20:1035–39 [Google Scholar]
  6. Armijos Jaramillo VD, Alberto VW, Sukno SA, Thon MR. 6.  2013. Horizontal transfer of a subtilisin gene from plants into an ancestor of the plant pathogenic fungal genus Colletotrichum. PLoS ONE 8:e59078 [Google Scholar]
  7. Bachhawat AK, Thakur A, Kaur J, Zulkifli M. 7.  2013. Glutathione transporters. Biochim. Biophys. Acta 1830:3154–64 [Google Scholar]
  8. Bailey BA. 8.  1995. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology 85:1250–55 [Google Scholar]
  9. Bapteste E, O'Malley MA, Beiko RG, Ereshefsky M, Gogarten JP. 9.  et al. 2009. Prokaryotic evolution and the tree of life are two different things. Biol. Direct 4:34 [Google Scholar]
  10. Barclay M, Tett VA, Knowles CJ. 10.  1998. Metabolism and enzymology of cyanide/metallocyanide biodegradation by Fusarium solani under neutral and acidic conditions. Enzyme Microb. Technol. 23:321–30 [Google Scholar]
  11. Beiko RG, Harlow TJ, Ragan MA. 11.  2005. Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. USA 102:14332–37 [Google Scholar]
  12. Belbahri L, Calmin G, Mauch F, Andersson JO. 12.  2008. Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408:1–8 [Google Scholar]
  13. Bever JD, Wang M. 13.  2005. Arbuscular mycorrhizal fungi: hyphal fusion and multigenomic structure. Nature 433:E3–4 [Google Scholar]
  14. Blumenthal T. 14.  2004. Operons in eukaryotes. Brief Funct. Genomics Proteomics 3:199–211 [Google Scholar]
  15. Bohin JP. 15.  2000. Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol. Lett. 186:11–19 [Google Scholar]
  16. Brown CJ, Todd KM, Rosenzweig RF. 16.  1998. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15:931–42 [Google Scholar]
  17. Brown NA, Antoniw J, Hammond-Kosack KE. 17.  2012. The predicted secretome of the plant pathogenic fungus Fusarium graminearum: a refined comparative analysis. PLoS ONE 7:e33731 [Google Scholar]
  18. Cabral A, Oome S, Sander N, Kufner I, Nurnberger T, Van den Ackerveken G. 18.  2012. Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis: repression of necrosis-inducing activity by a surface-exposed region. Mol. Plant-Microbe Interact. 25:697–708 [Google Scholar]
  19. Cary JW, Ehrlich KC. 19.  2006. Aflatoxigenicity in Aspergillus: molecular genetics, phylogenetic relationships and evolutionary implications. Mycopathologia 162:167–77 [Google Scholar]
  20. Cavalier-Smith T. 20.  1987. The origin of fungi and pseudofungi. Evolutionary Biology of the Fungi ADM Rayer 339–53 Br. Mycol. Soc. Symp. Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  21. Cavalier-Smith T, Chao EE. 21.  2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J. Mol. Evol. 62:388–420 [Google Scholar]
  22. Coelho MA, Gonçalves C, Sampaio JP, Gonçalves P. 22.  2013. Extensive intra-kingdom horizontal gene transfer converging on a fungal fructose transporter gene. PLoS Genet. 9:e1003587 [Google Scholar]
  23. Cohan FM. 23.  2002. What are bacterial species?. Annu. Rev. Microbiol. 56:457–87 [Google Scholar]
  24. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC. 24.  et al. 2009. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5:e1000618 [Google Scholar]
  25. Cools HJ, Hammond-Kosack KE. 25.  2013. Exploitation of genomics in fungicide research: current status and future perspectives. Mol. Plant Pathol. 14:197–210 [Google Scholar]
  26. Cramer RA, Lawrence CB. 26.  2004. Identification of Alternaria brassicicola genes expressed in planta during pathogenesis of Arabidopsis thaliana. Fungal Genet. Biol. 41:115–28 [Google Scholar]
  27. Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M. 27.  et al. 2008. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 4:924–37Provided evidence of anastomosis between genetically distinct arbuscular mycorrhizal fungi leading to transfer of genetic material and production of stable progeny with altered phenotypes. [Google Scholar]
  28. Dagan T, Artzy-Randrup Y, Martin W. 28.  2008. Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc. Natl. Acad. Sci. USA 105:10039–44 [Google Scholar]
  29. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK. 29.  et al. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–86 [Google Scholar]
  30. de Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG. 30.  1998. Agrobacterium tumefaciens–mediated transformation of filamentous fungi. Nat. Biotechnol. 16:839–42 [Google Scholar]
  31. Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P. 31.  et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA 109:5110–15Found that Ave1 markedly contributes to fungal virulence and is only found in plant-associated fungi and bacteria. Phylogeny suggests the gene is derived from plants by HGT, providing an example of a host-derived HGT gene encoding a pathogenic phenotype. [Google Scholar]
  32. Del Bem LE, Vincentz MG. 32.  2010. Evolution of xyloglucan-related genes in green plants. BMC Evol. Biol. 10:341 [Google Scholar]
  33. Devescovi G, Bigirimana J, Degrassi G, Cabrio L, LiPuma JJ. 33.  et al. 2007. Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl. Environ. Microbiol. 73:4950–58 [Google Scholar]
  34. Dijksterhuis J, de Vries RP. 34.  2006. Compatible solutes and fungal development. Biochem. J. 399:e3–5 [Google Scholar]
  35. Doke N, Miura Y, Sanchez LM, Park HJ, Noritake T. 35.  et al. 1996. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence—a review. Gene 179:45–51 [Google Scholar]
  36. Dong S, Kong G, Qutob D, Yu X, Tang J. 36.  et al. 2012. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol. Plant-Microbe Interact. 25:896–909 [Google Scholar]
  37. Doolittle WF. 37.  1999. Lateral genomics. Trends Cell Biol. 9:M5–8 [Google Scholar]
  38. Doolittle WF. 38.  2008. Microbial evolution: stalking the wild bacterial species. Curr. Biol. 18:R565–67 [Google Scholar]
  39. Dujon B. 39.  2006. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22:375–87 [Google Scholar]
  40. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S. 40.  et al. 2004. Genome evolution in yeasts. Nature 430:35–44 [Google Scholar]
  41. Dulermo T, Rascle C, Billon-Grand G, Gout E, Bligny R, Cotton P. 41.  2010. Novel insights into mannitol metabolism in the fungal plant pathogen Botrytis cinerea. Biochem. J. 427:323–32 [Google Scholar]
  42. Dulermo T, Rascle C, Chinnici G, Gout E, Bligny R, Cotton P. 42.  2009. Dynamic carbon transfer during pathogenesis of sunflower by the necrotrophic fungus Botrytis cinerea: from plant hexoses to mannitol. New Phytol. 183:1149–62 [Google Scholar]
  43. Eddy SR. 43.  2009. A new generation of homology search tools based on probabilistic inference. Genome Inform. 23:205–11 [Google Scholar]
  44. Elliott CE, Gardiner DM, Thomas G, Cozijnsen A, Van De Wouw A, Howlett BJ. 44.  2007. Production of the toxin sirodesmin PL by Leptosphaeria maculans during infection of Brassica napus. Mol. Plant Pathol. 8:791–802 [Google Scholar]
  45. Ezzi MI, Lynch JM. 45.  2005. Biodegradation of cyanide by Trichoderma spp. and Fusarium spp. Enzyme Microbial Technol. 36:849–54 [Google Scholar]
  46. Feng BZ, Li PQ. 46.  2013. Molecular characterization and functional analysis of the Nep1-like protein-encoding gene from Phytophthora capsici. Genet. Mol. Res. 12:1468–78 [Google Scholar]
  47. Feng BZ, Li PQ, Fu L, Sun BB, Zhang XG. 47.  2011. Identification of 18 genes encoding necrosis-inducing proteins from the plant pathogen Phytophthora capsici (Pythiaceae: Oomycetes). Genet. Mol. Res. 10:910–22 [Google Scholar]
  48. Feng J, Wang F, Liu G, Greenshields D, Shen W. 48.  et al. 2009. Analysis of a Blumeria graminis–secreted lipase reveals the importance of host epicuticular wax components for fungal adhesion and development. Mol. Plant-Microbe Interact. 22:1601–10 [Google Scholar]
  49. Fitzpatrick DA. 49.  2012. Horizontal gene transfer in fungi. FEMS Microbiol. Lett. 329:1–8 [Google Scholar]
  50. Fitzpatrick DA, Logue ME, Butler G. 50.  2008. Evidence of recent interkingdom horizontal gene transfer between bacteria and Candida parapsilosis. BMC Evol. Biol. 8:181 [Google Scholar]
  51. Fitzpatrick DA, Logue ME, Stajich JE, Butler G. 51.  2006. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6:99 [Google Scholar]
  52. Fox EM, Howlett BJ. 52.  2008. Secondary metabolism: regulation and role in fungal biology. Curr. Opin. Microbiol. 11:481–87 [Google Scholar]
  53. Friesen TL, Faris JD, Solomon PS, Oliver RP. 53.  2008. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol. 10:1421–28 [Google Scholar]
  54. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H. 54.  et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953–56Used comparative genomics to identify transfer of a virulence factor between fungi and then showed that this transfer is linked with the emergence of a new class of pathogenic fungi. [Google Scholar]
  55. Gabriela Roca M, Read ND, Wheals AE. 55.  2005. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol. Lett. 249:191–98 [Google Scholar]
  56. Galeote V, Novo M, Salema-Oom M, Brion C, Valerio E. 56.  et al. 2011. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology 156:3754–61 [Google Scholar]
  57. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G. 57.  et al. 2011. Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet. 7:e1001264 [Google Scholar]
  58. Gardiner DM, Jarvis RS, Howlett BJ. 58.  2005. The ABC transporter gene in the sirodesmin biosynthetic gene cluster of Leptosphaeria maculans is not essential for sirodesmin production but facilitates self-protection. Fungal Genet. Biol. 42:257–63 [Google Scholar]
  59. Gardiner DM, Kazan K, Manners JM. 59.  2013. Cross-kingdom gene transfer facilitates the evolution of virulence in fungal pathogens. Plant Sci. 210:151–58 [Google Scholar]
  60. Gardiner DM, McDonald MC, Covarelli L, Solomon PS, Rusu AG. 60.  et al. 2012. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathog. 8:e1002952Used comparative genomics to identify HGTs associated with the pathogenic lifestyle of fungi that infect cereal hosts and then used these data as a foundation for functional analysis. Gene disruption analysis confirms that one HGT derived from a bacterial source has a pathogenic phenotype. [Google Scholar]
  61. Gardiner DM, Waring P, Howlett BJ. 61.  2005. The epipolythiodioxopiperazine (ETP) class of fungal toxins: distribution, mode of action, functions and biosynthesis. Microbiology 151:1021–32 [Google Scholar]
  62. Gijzen M, Nurnberger T. 62.  2006. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67:1800–7 [Google Scholar]
  63. Girard V, Dieryckx C, Job C, Job D. 63.  2013. Secretomes: the fungal strike force. Proteomics 13:597–608 [Google Scholar]
  64. Glass NL, Jacobson DJ, Shiu PK. 64.  2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu. Rev. Genet. 34:165–86 [Google Scholar]
  65. Gojkovic Z, Knecht W, Zameitat E, Warneboldt J, Coutelis JB. 65.  et al. 2004. Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol. Genet. Genomics 271:387–93 [Google Scholar]
  66. Goodwin SB, Ben M'Barek S, Dhillon B, Wittenberg AH, Crane CF. 66.  et al. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7:e1002070 [Google Scholar]
  67. Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C. 67.  et al. 2008. Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc. Natl. Acad. Sci. USA 105:18631–36 [Google Scholar]
  68. Hall C, Brachat S, Dietrich FS. 68.  2005. Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot. Cell 4:1102–15Key study quantifying and exploring the extent and nature of HGT into a fungal (Saccharomyces cerevisiae) genome. [Google Scholar]
  69. Hall C, Dietrich FS. 69.  2007. The reacquisition of biotin prototrophy in Saccharomyces cerevisiae involved horizontal gene transfer, gene duplication and gene clustering. Genetics 177:2293–307 [Google Scholar]
  70. Hamilton JP, Neeno-Eckwall EC, Adhikari BN, Perna NT, Tisserat N. 70.  et al. 2011. The comprehensive phytopathogen genomics resource: a web-based resource for data-mining plant pathogen genomes. Database (Oxford) 2011:bar053 [Google Scholar]
  71. Han Y, Liu X, Benny U, Kistler HC, VanEtten HD. 71.  2001. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J. 25:305–14 [Google Scholar]
  72. Harris PJ, Stone BA. 72.  2009. Chemistry and molecular organization of plant cell walls. Biomass Recalcitrance M Himmel 61–93 Hoboken, NJ: Blackwell Publ. Ltd. [Google Scholar]
  73. Hayman GT, Bolen PL. 73.  1993. Movement of shuttle plasmids from Escherichia coli into yeasts other than Saccharomyces cerevisiae using trans-kingdom conjugation. Plasmid 30:251–57 [Google Scholar]
  74. He C, Rusu AG, Poplawski AM, Irwin JA, Manners JM. 74.  1998. Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150:1459–66 [Google Scholar]
  75. Heinemann JA, Sprague GF Jr. 75.  1989. Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340:205–9 [Google Scholar]
  76. Heller J, Tudzynski P. 76.  2011. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu. Rev. Phytopathol. 49:369–90 [Google Scholar]
  77. Hellman J, Loiselle PM, Tehan MM, Allaire JE, Boyle LA. 77.  et al. 2000. Outer membrane protein A, peptidoglycan-associated lipoprotein, and murein lipoprotein are released by Escherichia coli bacteria into serum. Infect. Immun. 68:2566–72 [Google Scholar]
  78. Hématy K, Cherk C, Somerville S. 78.  2009. Host-pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 12:406–13 [Google Scholar]
  79. Hult K, Veide A, Gatenbeck S. 79.  1980. The distribution of the NADPH regenerating mannitol cycle among fungal species. Arch. Microbiol. 128:253–55 [Google Scholar]
  80. Inomata K, Nishikawa M, Yoshida K. 80.  1994. The yeast Saccharomyces kluyveri as a recipient eukaryote in transkingdom conjugation: behavior of transmitted plasmids in transconjugants. J. Bacteriol. 176:4770–73 [Google Scholar]
  81. Ishikawa FH, Souza EA, Read ND, Roca MG. 81.  2010. Live-cell imaging of conidial fusion in the bean pathogen, Colletotrichum lindemuthianum. Fungal Biol. 114:2–9 [Google Scholar]
  82. Ishikawa FH, Souza EA, Shoji JY, Connolly L, Freitag M. 82.  et al. 2012. Heterokaryon incompatibility is suppressed following conidial anastomosis tube fusion in a fungal plant pathogen. PLoS ONE 7:e31175 [Google Scholar]
  83. Jain R, Rivera MC, Moore JE, Lake JA. 83.  2003. Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20:1598–602 [Google Scholar]
  84. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V. 84.  et al. 2006. Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–22 [Google Scholar]
  85. Johnson CH, Klotz MG, York JL, Kruft V, McEwen JE. 85.  2002. Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148:1129–42 [Google Scholar]
  86. Kamper J, Kahmann R, Bölker M, Ma LJ, Brefort T. 86.  et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101 [Google Scholar]
  87. Keeling PJ, Inagaki Y. 87.  2004. A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1α. Proc. Natl. Acad. Sci. USA 101:15380–85 [Google Scholar]
  88. Keeling PJ, Palmer JD. 88.  2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605–18 [Google Scholar]
  89. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE. 89.  et al. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog. 7:e1002137 [Google Scholar]
  90. Klotz MG, Loewen PC. 90.  2003. The molecular evolution of catalatic hydroperoxidases: evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota. Mol. Biol. Evol. 20:1098–112 [Google Scholar]
  91. Knight CJ, Bailey AM, Foster GD. 91.  2010. Investigating Agrobacterium-mediated transformation of Verticillium albo-atrum on plant surfaces. PLoS ONE 5:e13684 [Google Scholar]
  92. Konstantinidis KT, Tiedje JM. 92.  2005. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. USA 102:2567–72 [Google Scholar]
  93. Koski LB, Golding GB. 93.  2001. The closest BLAST hit is often not the nearest neighbor. J. Mol. Evol. 52:540–42 [Google Scholar]
  94. Koski LB, Morton RA, Golding GB. 94.  2001. Codon bias and base composition are poor indicators of horizontally transferred genes. Mol. Biol. Evol. 18:404–12 [Google Scholar]
  95. Kufner I, Ottmann C, Oecking C, Nurnberger T. 95.  2009. Cytolytic toxins as triggers of plant immune response. Plant Sig. Behav. 4:977–79 [Google Scholar]
  96. Kuhn G, Hijri M, Sanders IR. 96.  2001. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–48 [Google Scholar]
  97. Kulkarni AR, Pena MJ, Avci U, Mazumder K, Urbanowicz BR. 97.  et al. 2012. The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes. Glycobiology 22:439–51 [Google Scholar]
  98. Lang AS, Beatty JT. 98.  2007. Importance of widespread gene transfer agent genes in α-proteobacteria. Trends Microbiol. 15:54–62 [Google Scholar]
  99. Lawrence J. 99.  1999. Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr. Opin. Genet. Dev. 9:642–48 [Google Scholar]
  100. Lawrence JG, Ochman H. 100.  1997. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44:383–97 [Google Scholar]
  101. Lawrence JG, Ochman H. 101.  2002. Reconciling the many faces of lateral gene transfer. Trends Microbiol. 10:1–4 [Google Scholar]
  102. Lawrence JG, Roth JR. 102.  1996. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843–60 [Google Scholar]
  103. Lin CC, Aronson JM. 103.  1970. Chitin and cellulose in the cell walls of the oomycete, Apodachlya sp. Arch. Mikrobiol. 72:111–14 [Google Scholar]
  104. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J. 104.  et al. 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433:865–68 [Google Scholar]
  105. Lowe RG, Howlett BJ. 105.  2012. Indifferent, affectionate, or deceitful: lifestyles and secretomes of fungi. PLoS Pathog. 8:e1002515 [Google Scholar]
  106. Lu H, Higgins VJ. 106.  1999. The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiol. Mol. Plant Pathol. 54:131–43 [Google Scholar]
  107. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O'Donnell K. 107.  et al. 2013. Fusarium pathogenomics. Annu. Rev. Microbiol. 67:399–416 [Google Scholar]
  108. Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G. 108.  et al. 2009. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet. 5:e1000549 [Google Scholar]
  109. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ. 109.  et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–73 [Google Scholar]
  110. Mallet LV, Becq J, Deschavanne P. 110.  2010. Whole genome evaluation of horizontal transfers in the pathogenic fungus Aspergillus fumigatus. BMC Genomics 11:171 [Google Scholar]
  111. Maloney A, VanEtten H. 111.  1994. A gene from the fungal plant pathogen Nectria haematococca that encodes the phytoalexin-detoxifying enzyme pisatin demethylase defines a new cytochrome P450 family. Mol. Gen. Genet. MGG 243:506–14 [Google Scholar]
  112. Maor R, Shirasu K. 112.  2005. The arms race continues: battle strategies between plants and fungal pathogens. Curr. Opin. Microbiol. 8:399–404 [Google Scholar]
  113. Marcet-Houben M, Gabaldon T. 113.  2010. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26:5–8 [Google Scholar]
  114. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S. 114.  et al. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99:12246–51 [Google Scholar]
  115. Masel AM, He C, Poplawski AM, Irwin JAG, Manners JM. 115.  1996. Molecular evidence for chromosome transfer between biotypes of Colletotrichum gloeosporioides. Mol. Plant-Microbe Interact. 5:339–48 [Google Scholar]
  116. Mattinen L, Tshuikina M, Mae A, Pirhonen M. 116.  2004. Identification and characterization of Nip, necrosis-inducing virulence protein of Erwinia carotovora subsp. carotovora. Mol. Plant-Microbe Interact. 17:1366–75 [Google Scholar]
  117. McGary KL, Slot JC, Rokas A. 117.  Physical linkage of metabolic genes in fungi is an adaptation against the accumulation of toxic intermediate compounds. Proc. Natl. Acad. Sci. USA 110:11481–86 [Google Scholar]
  118. Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M'barek S. 118.  et al. 2011. Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol. Rev. 35:542–54 [Google Scholar]
  119. Mélida H, Sandoval-Sierra JV, Diéguez-Uribeondo J, Bulone V. 119.  2013. Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryot. Cell 12:194–203 [Google Scholar]
  120. Mellersh DG, Foulds IV, Higgins VJ, Heath MC. 120.  2002. H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29:257–68 [Google Scholar]
  121. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I. 121.  et al. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–35 [Google Scholar]
  122. Milani NA, Lawrence DP, Arnold AE, VanEtten HD. 122.  2012. Origin of pisatin demethylase (PDA) in the genus Fusarium. Fungal Genet. Biol. 49:933–42 [Google Scholar]
  123. Mirocha CJ, Gilchrist DG, Shier WT, Abbas HK, Wen Y, Vesonder RF. 123.  1992. AAL toxins, fumonisins (biology and chemistry) and host-specificity concepts. Mycopathologia 117:47–56 [Google Scholar]
  124. Molina L, Kahmann R. 124.  2007. An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19:2293–309 [Google Scholar]
  125. Motteram J, Kufner I, Deller S, Brunner F, Hammond-Kosack KE. 125.  et al. 2009. Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol. Plant-Microbe Interact. 22:790–99 [Google Scholar]
  126. Nathues E, Joshi S, Tenberge KB, von den Driesch M, Oeser B. 126.  et al. 2004. CPTF1, a CREB-like transcription factor, is involved in the oxidative stress response in the phytopathogen Claviceps purpurea and modulates ROS level in its host Secale cereale. Mol. Plant-Microbe Interact. 17:383–93 [Google Scholar]
  127. Nevoigt E, Fassbender A, Stahl U. 127.  2000. Cells of the yeast Saccharomyces cerevisiae are transformable by DNA under non-artificial conditions. Yeast 16:1107–10Showed that in starvation conditions, yeast takes up extracellular DNA (plasmids), providing evidence that a subset of mechanisms required for HGT are present in fungi. [Google Scholar]
  128. O'Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R. 128.  2005. Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71:5544–50 [Google Scholar]
  129. Oliver R. 129.  2012. Genomic tillage and the harvest of fungal phytopathogens. New Phytol. 196:1015–23Emphasized the importance of genomic variation in the evolution of plant-pathogenic groups. [Google Scholar]
  130. Oliver RP, Lord M, Rybak K, Faris JD, Solomon PS. 130.  2008. Emergence of tan spot disease caused by toxigenic Pyrenophora tritici-repentis in Australia is not associated with increased deployment of toxin-sensitive cultivars. Phytopathology 98:488–91 [Google Scholar]
  131. Ottmann C, Luberacki B, Kufner I, Koch W, Brunner F. 131.  et al. 2009. A common toxin fold mediates microbial attack and plant defense. Proc. Natl. Acad. Sci. USA 106:10359–64 [Google Scholar]
  132. Pal C, Hurst LD. 132.  2004. Evidence against the selfish operon theory. Trends Genet. 20:232–34 [Google Scholar]
  133. Patron NJ, Waller RF, Cozijnsen AJ, Straney DC, Gardiner DM. 133.  et al. 2007. Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 7:174 [Google Scholar]
  134. Petersen TN, Brunak S, von Heijne G, Nielsen H. 134.  2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785–86 [Google Scholar]
  135. Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R. 135.  et al. 2003. Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J. Biol. Chem. 278:47905–14 [Google Scholar]
  136. Poptsova MS, Gogarten JP. 136.  2007. The power of phylogenetic approaches to detect horizontally transferred genes. BMC Evol. Biol. 7:45 [Google Scholar]
  137. Price MN, Huang KH, Arkin AP, Alm EJ. 137.  2005. Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res. 15:809–19 [Google Scholar]
  138. Qutob D, Kamoun S, Gijzen M. 138.  2002. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 32:361–73 [Google Scholar]
  139. Ragan MA. 139.  2001. Detection of lateral gene transfer among microbial genomes. Curr. Opin. Genet. Dev. 11:620–26 [Google Scholar]
  140. Ragan MA. 140.  2001. On surrogate methods for detecting lateral gene transfer. FEMS Microbiol. Lett. 201:187–91 [Google Scholar]
  141. Ragan MA, Harlow TJ, Beiko RG. 141.  2006. Do different surrogate methods detect lateral genetic transfer events of different relative ages?. Trends Microbiol. 14:4–8 [Google Scholar]
  142. Rao VG, Desai MK, Kulkarni NB. 142.  1965. Cultural and physiological studies of Phytophthora palmvora Butl. causing fruit rot of Achras sapota. Mycopathologia 28:241–48 [Google Scholar]
  143. Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW. 143.  2008. Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol. Plant Pathol. 9:339–55 [Google Scholar]
  144. Richards TA. 144.  2011. Genome evolution: horizontal movements in the fungi. Curr. Biol. 21:R166–68 [Google Scholar]
  145. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ. 145.  2006. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16:1857–64 [Google Scholar]
  146. Richards TA, Hirt RP, Williams BA, Embley TM. 146.  2003. Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154:17–32 [Google Scholar]
  147. Richards TA, Leonard G, Soanes DM, Talbot NJ. 147.  2011. Gene transfer into the fungi. Fungal Biol. Rev. 25:98–110 [Google Scholar]
  148. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ. 148.  2009. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21:1897–911 [Google Scholar]
  149. Richards TA, Soanes DM, Jones MD, Vasieva O, Leonard G. 149.  et al. 2011. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl. Acad. Sci. USA 108:15258–63HGT has played a role in the evolution of phytopathogenic traits in some plant-pathogenic oomycetes. [Google Scholar]
  150. Richards TA, Talbot NJ. 150.  2013. Horizontal gene transfer in osmotrophs: playing with public goods. Nat. Rev. Micro. 11:720–27 [Google Scholar]
  151. Roca MG, Davide LC, Davide LM, Mendes-Costa MC, Schwan RF, Wheals AE. 151.  2004. Conidial anastomosis fusion between Colletotrichum species. Mycol. Res. 108:1320–26 [Google Scholar]
  152. Rolland T, Neuveglise C, Sacerdot C, Dujon B. 152.  2009. Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. PLoS ONE 4:e6515 [Google Scholar]
  153. Rosewich UL, Kistler HC. 153.  2000. Role of horizontal gene transfer in the evolution of fungi. Annu. Rev. Phytopathol. 38:325–63 [Google Scholar]
  154. Sawasaki Y, Inomata K, Yoshida K. 154.  1996. Trans-kingdom conjugation between Agrobacterium tumefaciens and Saccharomyces cerevisiae, a bacterium and a yeast. Plant Cell Physiol. 37:103–6 [Google Scholar]
  155. Selosse MA, Le Tacon F. 155.  1998. The land flora: a phototroph-fungus partnership?. Trends Ecol. Evol. 13:15–20 [Google Scholar]
  156. Sepúlveda-Jiménez G, Rueda-Benitez P, Porta H, Rocha-Sosa M. 156.  2005. A red beet (Beta vulgaris) UDP-glucosyltransferase gene induced by wounding, bacterial infiltration and oxidative stress. J. Exp. Bot. 56:605–11 [Google Scholar]
  157. Sexton AC, Howlett BJ. 157.  2000. Characterisation of a cyanide hydratase gene in the phytopathogenic fungus Leptosphaeria maculans. Mol. Gen. Genet. 263:463–70 [Google Scholar]
  158. Slot JC, Rokas A. 158.  2010. Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc. Natl. Acad. Sci. USA 107:10136–41 [Google Scholar]
  159. Slot JC, Rokas A. 159.  2011. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr. Biol. 21:134–39 [Google Scholar]
  160. Smith MW, Feng DF, Doolittle RF. 160.  1992. Evolution by acquisition: the case for horizontal gene transfers. Trends Biochem. Sci. 17:489–93 [Google Scholar]
  161. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C. 161.  et al. 2008. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE 3:e2300 [Google Scholar]
  162. Soanes DM, Richards TA, Talbot NJ. 162.  2007. Insights from sequencing fungal and oomycete genomes: What can we learn about plant disease and the evolution of pathogenicity?. Plant Cell 19:3318–26 [Google Scholar]
  163. Solomon PS, Waters OD, Jörgens CI, Lowe RGT, Rechberger J. 163.  et al. 2006. Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch). Biochem. J. 399:231–39 [Google Scholar]
  164. Solomon PS, Waters OD, Oliver RP. 164.  2007. Decoding the mannitol enigma in filamentous fungi. Trends Microbiol. 15:257–62 [Google Scholar]
  165. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM. 165.  et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–46 [Google Scholar]
  166. Stukenbrock EH, McDonald BA. 166.  2007. Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol. Plant Pathol. 8:321–32 [Google Scholar]
  167. Sun B-F, Xiao J-H, He S, Liu L, Murphy RW, Huang D-W. 167.  2013. Multiple interkingdom horizontal gene transfers in Pyrenophora and closely related species and their contributions to phytopathogenic lifestyles. PLoS ONE 8:e60029 [Google Scholar]
  168. Syvanen M. 168.  1985. Cross-species gene transfer; implications for a new theory of evolution. J. Theor. Biol. 112:333–43 [Google Scholar]
  169. Temporini ED, VanEtten HD. 169.  2004. An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Neocosmospora boniensis. Curr. Genet. 46:29–36 [Google Scholar]
  170. Thomas CM, Nielsen KM. 170.  2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3:711–21 [Google Scholar]
  171. Tian S, Qin G, Li B. 171.  2013. Reactive oxygen species involved in regulating fruit senescence and fungal pathogenicity. Plant Mol. Biol. 82:593–602 [Google Scholar]
  172. Tiburcio RA, Costa GGL, Carazzolle MF, Mondego JMC, Schuster SC. 172.  et al. 2010. Genes acquired by horizontal transfer are potentially involved in the evolution of phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, two of the major pathogens of Cacao. J. Mol. Evol. 70:85–97 [Google Scholar]
  173. Tomas A, Feng GH, Reeck GR, Bockus WW, Leach JE. 173.  1990. Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol. Plant-Microbe Interact. 3:221–24 [Google Scholar]
  174. Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y. 174.  et al. 2012. Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet. Biol. 49:48–57 [Google Scholar]
  175. van den Brink J, de Vries RP. 175.  2011. Fungal enzyme sets for plant polysaccharide degradation. Appl. Microbiol. Biotechnol. 91:1477–92 [Google Scholar]
  176. van der Does HC, Rep M. 176.  2007. Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol. Plant-Microbe Interact. 20:1175–82 [Google Scholar]
  177. Vélëz H, Glassbrook NJ, Daub ME. 177.  2008. Mannitol biosynthesis is required for plant pathogenicity by Alternaria alternata. FEMS Microbiol. Lett. 285:122–29 [Google Scholar]
  178. Voegele RT, Hahn M, Lohaus G, Link T, Heiser I, Mendgen K. 178.  2005. Possible roles for mannitol and mannitol dehydrogenase in the biotrophic plant pathogen Uromyces fabae. Plant Physiol. 137:190–98 [Google Scholar]
  179. Voigt CA, Schafer W, Salomon S. 179.  2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42:364–75 [Google Scholar]
  180. Walton JD. 180.  2000. Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet. Biol. 30:167–71 [Google Scholar]
  181. Wang P, Sandrock RW, VanEtten HD. 181.  1999. Disruption of the cyanide hydratase gene in Gloeocercospora sorghi increases its sensitivity to the phytoanticipin cyanide but does not affect its pathogenicity on the cyanogenic plant sorghum. Fungal Genet. Biol. 28:126–34 [Google Scholar]
  182. Wapinski I, Pfeffer A, Friedman N, Regev A. 182.  2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61 [Google Scholar]
  183. Ware SB. 183.  2006. Aspects of sexual reproduction in Mycosphaerella species on wheat and barley: genetic studies on specificity, mapping and fungicide resistance PhD Thesis, Wageningen Univ., Wageningen, the Neth. [Google Scholar]
  184. Whitaker JW, McConkey GA, Westhead DR. 184.  2009. The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes. Genome Biol. 10:R36 [Google Scholar]
  185. Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M. 185.  et al. 2013. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat. Genet. 45:1092–96 [Google Scholar]
  186. Wolfe KH, Shields DC. 186.  1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–13 [Google Scholar]
  187. Zamocky M, Furtmuller PG, Obinger C. 187.  2009. Two distinct groups of fungal catalase/peroxidases. Biochem. Soc. Trans. 37:772–77 [Google Scholar]
  188. Zhao Z, Liu H, Wang C, Xu JR. 188.  2014. Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 15:6 [Google Scholar]
  189. Zhu B, Zhou Q, Xie G, Zhang G, Zhang X. 189.  et al. 2012. Interkingdom gene transfer may contribute to the evolution of phytopathogenicity in Botrytis cinerea. Evol. Bioinform. 8:105–17 [Google Scholar]
  190. Zhuang JP, Su J, Li XP, Chen WX. 190.  2006. Cloning and expression analysis of β-galactosidase gene related to softening of banana (Musa sp.) fruit. J. Plant Physiol. Mol. Biol. 32:411–19 [Google Scholar]
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