The availability of genomic sequences of several species triggered an explosion of genome-scale investigations of mechanisms fundamental to the life cycle and disease process. Comparative genomics studies have revealed evolutionary mechanisms, such as hybridization and interchromosomal rearrangements, that have shaped these genomes. Functional analyses of a diverse group of genes encoding virulence factors indicate that successful host xylem colonization relies on specific responses to various stresses, including nutrient deficiency and host defense–derived oxidative stress. Regulatory pathways that control responses to changes in nutrient availability also appear to positively control resting structure development. Conversely, resting structure development seems to be repressed by pathways, such as those involving effector secretion, which promote responses to host defenses. The genomics-enabled functional characterization of responses to the challenges presented by the xylem environment, accompanied by identification of novel virulence factors, has rapidly expanded our understanding of niche adaptation in species.


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Literature Cited

  1. Amyotte SG, Tan X, Pennerman K, Jimenez-Gasco MDM, Klosterman SJ. 1.  et al. 2012. Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 13:1314 [Google Scholar]
  2. Andersen PC, Brodbeck BV, Mizell RF. 2.  1995. Diurnal vitiations in tension, osmolarity, and the composition of nitrogen and carbon assimilates in xylem fluid of Prunus persica, Vitis hybrid, and Pyrus communis. J. Am. Soc. Hortic. Sci. 120:4600–6 [Google Scholar]
  3. Avrova AO, Venter E, Birch PR, Whisson SC. 3.  2003. Profiling and quantifying differential gene transcription in Phytophthora infestans prior to and during the early stages of potato infection. Fungal Genet. Biol. 40:4–14 [Google Scholar]
  4. Bontemps-Gallo S, Madec E, Lacroix J-M. 4.  2014. Inactivation of pecS restores the virulence of mutants devoid of osmoregulated periplasmic glucans in the phytopathogenic bacterium Dickeya dadantii. Microbiology 160:Pt. 4766–77 [Google Scholar]
  5. Bourges N, Groppi A, Barreau C, Clavé C, Bégueret J. 5.  1998. Regulation of gene expression during the vegetative incompatibility reaction in Podospora anserina: characterization of three induced genes. Genetics 150:633–41 [Google Scholar]
  6. Cabiscol E, Belli G, Tamarit J, Echave P, Herrero E, Ros J. 6.  2002. Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. J. Biol. Chem. 277:44531–38 [Google Scholar]
  7. Calonje M, Bernardo D, Novaes-Ledieu M, Mendoza CG. 7.  2002. Properties of a hydrophobin isolated from the mycoparasitic fungus Verticillium fungicola. Can. J. Microbiol. 48:1030–34 [Google Scholar]
  8. Clérivet A, Déon V, Alami I, Lopez F, Geiger J-P, Nicole M. 8.  2000. Tyloses and gels associated with cellulose accumulation in vessels are responses of plane tree seedlings (Platanus × acerifolia) to the vascular fungus Ceratocystis fimbriata f. sp. platani Trees 15:125–31 [Google Scholar]
  9. De Jonge R, Bolton MD, Kombrink A, van den Berg GCM, Yadeta KA, Thomma BPHJ. 9.  2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23:81271–82 [Google Scholar]
  10. De Jonge R, Bolton MD, Thomma BPHJ. 10.  2011. How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr. Opin. Plant Biol. 14:4400–6 [Google Scholar]
  11. De Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y. 11.  et al. 2010. Conserved fungal lysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–55 [Google Scholar]
  12. De Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P. 12.  et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA 109:135110–15 [Google Scholar]
  13. Duressa D, Anchieta A, Chen D, Klimes A, Garcia-Pedrajas MD. 13.  et al. 2013. RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae. BMC Genomics 14:607 [Google Scholar]
  14. Faino L, Thomma BPHJ. 14.  2014. Get your high-quality low-cost genome sequence. Trends Plant Sci. 19:288–91 [Google Scholar]
  15. Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GCM, Joosten MHAJ, Thomma BPHJ. 15.  2011. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156:42255–65 [Google Scholar]
  16. Fradin EF, Thomma BPHJ. 16.  2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 7:271–86 [Google Scholar]
  17. Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CDM, Nazar RN. 17.  et al. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150:1320–32 [Google Scholar]
  18. Gan P, Ikeda K, Irieda H, Narusaka M, O'Connell RJ. 18.  et al. 2013. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol. 197:41236–49 [Google Scholar]
  19. Gao F, Zhou B-J, Li G-Y, Jia P-S, Li H. 19.  et al. 2010. A glutamic acid–rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity. PLOS ONE 5:12e15319 [Google Scholar]
  20. Glass NL, Dementhon K. 20.  2006. Non-self recognition and programmed cell death in filamentous fungi. Curr. Opin. Microbiol. 9:553–58 [Google Scholar]
  21. Griffiths DA. 21.  1970. The fine structure of developing microsclerotia of Verticillium dahliae Kleb. Arch. Mikrobiol. 74:3207–12 [Google Scholar]
  22. Griffiths DA. 22.  1970. Paramural bodies in hyphae of Verticillium dahliae Kleb. revealed by freeze etching. Arch. Mikrobiol. 73:4331–36 [Google Scholar]
  23. Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB. 23.  2014. Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLOS Genet. 10:5e1004281 [Google Scholar]
  24. Hoppenau CE, Tran V-T, Kusch H, Abhauer KP, Landesfeind M. 24.  et al. 2014. Verticillium dahliae Vdthi4, involved in thiazole biosynthesis, stress response and DNA repair functions, is required for vascular disease induction in tomato. Environ. Exp. Bot. 108:14–22 [Google Scholar]
  25. Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW. 25.  et al. 2009. Colletotrichum: names in current use. Fungal Divers. 39:147–82 [Google Scholar]
  26. Inderbitzin P, Bostock RM, Davis RM, Usami T, Platt HW, Subbarao KV. 26.  2011. Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLOS ONE 6:12e28341 [Google Scholar]
  27. Inderbitzin P, Davis RM, Bostock RM, Subbarao KV. 27.  2011. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLOS ONE 6:3e18260 [Google Scholar]
  28. Karapapa VK, Bainbridge BW, Heale JB. 28.  1997. Morphological and molecular characterization of Verticillium longisporum comb. nov., pathogenic to oilseed rape. Mycol. Res. 101:1281–94 [Google Scholar]
  29. Khoshraftar S, Hung S, Khan S, Gong Y, Tyagi V. 29.  et al. 2013. Sequencing and annotation of the Ophiostoma ulmi genome. BMC Genomics 14:1162 [Google Scholar]
  30. Klimes A, Amyotte SG, Grant S, Kang S, Dobinson KF. 30.  2008. Microsclerotia development in Verticillium dahliae: regulation and differential expression of the hydrophobin gene VDH1. Fungal Genet. Biol. 45:121525–32 [Google Scholar]
  31. Klimes A, Dobinson KF. 31.  2006. A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae. Fungal Genet. Biol. 43:4283–94 [Google Scholar]
  32. Klosterman SJ, Anchieta A, Garcia-Pedrajas MD, Maruthachalam K, Hayes RJ, Subbarao KV. 32.  2011. SSH reveals a linkage between a senescence-associated protease and Verticillium wilt symptom development in lettuce (Lactuca sativa). Physiol. Mol. Plant Pathol. 76:48–58 [Google Scholar]
  33. Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV. 33.  2009. Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 47:139–62 [Google Scholar]
  34. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE. 34.  et al. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLOS Pathog. 7:7e1002137 [Google Scholar]
  35. Kombrink A, Thomma BPHJ. 35.  2013. LysM effectors: secreted proteins supporting fungal life. PLOS Pathog. 9:12e1003769 [Google Scholar]
  36. Lamb C, Dixon RA. 36.  1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251–75 [Google Scholar]
  37. Lionetti V, Cervone F, Bellincampi D. 37.  2012. Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J. Plant Physiol. 169:161623–30 [Google Scholar]
  38. Liu S, Chen J, Wang J, Li L, Xiao H. 38.  et al. 2013. Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae. Gene 529:2307–16 [Google Scholar]
  39. Liu T, Song T, Zhang X, Yuan H, Su L. 39.  et al. 2014. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686 [Google Scholar]
  40. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J. 40.  et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:7287367–73 [Google Scholar]
  41. Maruthachalam K, Klosterman SJ, Kang S, Hayes RJ, Subbarao KV. 41.  2011. Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens–mediated T-DNA insertional mutagenesis. Mol. Biotechnol. 49:3209–21 [Google Scholar]
  42. Milgroom MG, del Mar Jiménez-Gasco M, Olivares García C, Drott MT, Jiménez-Díaz RM. 41a.  2014. Recombination between clonal lineages of the asexual fungus Verticillium dahliae detected by genotyping by sequencing. PLOS ONE 9:9e106740 [Google Scholar]
  43. Mohnen D. 42.  2008. Pectin structure and biosynthesis. Curr. Opin. Plant Biol. 11:3266–77 [Google Scholar]
  44. Page F, Altabe S, Hugouvieux-Cotte-Pattat N, Lacroix J-M, Robert-Baudouy J, Bohin J-P. 43.  2001. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J. Bacteriol. 183:103134–41 [Google Scholar]
  45. Pantelides IS, Tjamos SE, Paplomatas EJ. 44.  2010. Insights into the role of ethylene perception in tomato resistance to vascular infection by Verticillium dahliae. Plant Pathol. 59:130–38 [Google Scholar]
  46. Pantelides IS, Tjamos SE, Paplomatas EJ. 45.  2010. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol. Plant Pathol. 11:2191–202 [Google Scholar]
  47. Pegg GF. 46.  1989. Pathogenesis in vascular diseases of plants. Vascular Wilt Diseases of Plants EC Tjamos, C Beckman 51–94 Berlin: Springer-Verlag [Google Scholar]
  48. Pegg GF, Brady BL. 47.  2002. Verticillium Wilts London: CABI
  49. Raffaele S, Kamoun S. 48.  2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10:417–30 [Google Scholar]
  50. Rauyaree P, Ospina-Giraldo MD, Kang S, Bhat RG, Subbarao KV. 49.  et al. 2005. Mutations in VMK1, a mitogen-activated protein kinase gene, affect microsclerotia formation and pathogenicity in Verticillium dahliae. Curr. Genet. 48:2109–16 [Google Scholar]
  51. Rovenich H, Boshoven JC, Thomma BPHJ. 50.  2014. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr. Opin. Plant Biol. 20:96–103 [Google Scholar]
  52. Sánchez-Vallet A, Saleem-Batcha R, Kombrink A, Hansen G, Valkenburg D-J. 51.  et al. 2013. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2:2e00790 [Google Scholar]
  53. Santhanam P, Thomma BPHJ. 52.  2013. Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Mol. Plant-Microbe Interact. 26:2249–56 [Google Scholar]
  54. Santhanam P, van Esse HP, Albert I, Faino L, Nürnberger T, Thomma BPHJ. 53.  2013. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant-Microbe Interact. 26:3278–86 [Google Scholar]
  55. Seidl MF, Thomma BPHJ. 54.  2014. Sex or no sex: evolutionary adaptation occurs regardless. Bioessays 36:335–45 [Google Scholar]
  56. Singh S, Braus-Stromeyer SA, Timpner C, Tran VT, Lohaus G. 55.  et al. 2010. Silencing of Vlaro2 for chorismate synthase revealed that the phytopathogen Verticillium longisporum induces the cross-pathway control in the xylem. Appl. Microbiol. Biotechnol. 85:61961–76 [Google Scholar]
  57. Singh S, Braus-Stromeyer SA, Timpner C, Valerius O, von Tiedemann A. 56.  et al. 2012. The plant host Brassica napus induces in the pathogen Verticillium longisporum the expression of functional catalase peroxidase which is required for the late phase of disease. Mol. Plant-Microbe Interact. 25:4569–81 [Google Scholar]
  58. Thomma BPHJ, Nürnberger T, Joosten MHAJ. 57.  2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15 [Google Scholar]
  59. Tian L, Xu J, Zhou L, Guo W. 58.  2014. VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae. Gene 550:2238–44 [Google Scholar]
  60. Timpner C, Braus-Stromeyer SA, Tran VT, Braus GH. 59.  2013. The Cpc1 regulator of the cross-pathway control of amino acid biosynthesis is required for pathogenicity of the vascular pathogen Verticillium longisporum. Mol. Plant-Microbe Interact. 26:111312–24 [Google Scholar]
  61. Tran V, Braus-Stromeyer SA, Kusch H, Reusche M, Kaever A. 60.  et al. 2014. Verticillium transcription activator of adhesion Vta2 suppresses microsclerotia formation and is required for systemic infection of plant roots. New Phytol. 11:565–81 [Google Scholar]
  62. Tzima A, Paplomatas EJ, Rauyaree P, Kang S. 61.  2010. Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae. Fungal Genet. Biol. 47:5406–15 [Google Scholar]
  63. Tzima AK, Paplomatas EJ, Rauyaree P, Ospina-Giraldo MD, Kang S. 62.  2011. VdSNF1, the sucrose nonfermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell-wall degradation. Mol. Plant-Microbe Interact. 24:1129–42 [Google Scholar]
  64. Tzima AK, Paplomatas EJ, Tsitsigiannis DI, Kang S. 63.  2012. The G protein β subunit controls virulence and multiple growth- and development-related traits in Verticillium dahliae. Fungal Genet. Biol. 49:4271–83 [Google Scholar]
  65. Usami T, Itoh M, Amemiya Y. 64.  2009. Asexual fungus Verticillium dahliae is potentially heterothallic. J. Gen. Plant Pathol. 75:6422–27 [Google Scholar]
  66. Vallad GE, Subbarao KV. 65.  2008. Colonization of resistant and susceptible lettuce cultivars by a green fluorescent protein-tagged isolate of Verticillium dahliae. Phytopathology 98:8871–85 [Google Scholar]
  67. Wang C, St. Leger RJ. 66.  2007. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot. Cell 6:5808–16 [Google Scholar]
  68. Wulff EG, Sørensen JL, Lübeck M, Nielsen KF, Thrane U, Torp J. 67.  2010. Fusarium spp. associated with rice bakanae: ecology, genetic diversity, pathogenicity and toxigenicity. Environ. Microbiol. 12:3649–57 [Google Scholar]
  69. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A. 68.  et al. 2012. Legume pectate lyase required for root infection by rhizobia. Proc. Natl. Acad. Sci. USA 109:2633–38 [Google Scholar]
  70. Xin M, Wang X, Peng H, Yao Y, Xie C. 69.  et al. 2012. Transcriptome comparison of susceptible and resistant wheat in response to powdery mildew infection. Genomics Proteomics Bioinform. 10:294–106 [Google Scholar]
  71. Xiong D, Wang Y, Ma J, Klosterman SJ, Xiao S, Tian C. 70.  2014. Deep mRNA sequencing reveals stage-specific transcriptome alterations during microsclerotia development in the smoke tree vascular wilt pathogen, Verticillium dahliae. BMC Genomics 15:1324 [Google Scholar]
  72. Yadeta K, Thomma B. 71.  2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97 [Google Scholar]
  73. Yang X, Ben S, Sun Y, Fan X, Tian C, Wang Y. 72.  2013. Genome-wide identification, phylogeny and expression profile of vesicle fusion components in Verticillium dahliae. PLOS ONE 8:7e68681 [Google Scholar]
  74. Zhang Z, van Esse HP, van Damme M, Fradin EF, Liu C-M, Thomma BPHJ. 73.  2013. Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol. Plant Pathol. 14:7719–27 [Google Scholar]
  75. Zhou B-J, Jia P-S, Gao F, Guo H-S. 74.  2012. Molecular characterization and functional analysis of a necrosis- and ethylene-inducing, protein-encoding gene family from Verticillium dahliae. Mol. Plant-Microbe. Interact. 25:7964–75 [Google Scholar]
  76. Zhou L, Zhao J, Guo W, Zhang T. 75.  2013. Functional analysis of autophagy genes via Agrobacterium-mediated transformation in the vascular wilt fungus Verticillium dahliae. J. Genet. Genomics 40:8421–31 [Google Scholar]

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