Pathogenomics of fungal plant parasites: What have we learnt about pathogenesis?

Current Opinion in Plant Biology

Volumn 14, Issue 4, 2011, Pages 392-399

  Schmidt, Sarah Maria ^a   Panstruga, Ralph ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

FUNGAL GENE; FUNGUS; GENE EXPRESSION REGULATION; GENETICS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HOST RANGE; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PLANT; PLANT DISEASE; REVIEW; VIRULENCE;

EVOLUTION, MOLECULAR; FUNGAL PROTEINS; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; GENE TRANSFER, HORIZONTAL; GENES, FUNGAL; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANTS; VIRULENCE;

ERYSIPHALES; FUNGI; OOMYCETES;

EID: 79961171580     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2011.03.006     Document Type: Review

References (64)

1. Lévesque C.A., Brouwer H., Cano L., Hamilton J.P., Holt C., Huitema E., Raffaele S., Robideau G.P., Thines M., Win J., et al. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 2010, 11:R73.
2. Hane J.K., Lowe R.G.T., Solomon P.S., Tan K.C., Schoch C.L., Spatafora J.W., Crous P.W., Kodira C., Birren B.W., Galagan J.E., et al. Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 2007, 19:3347-3368.
3. Ellwood S.R., Liu Z.H., Syme R.A., Lai Z., Hane J.K., Keiper F., Moffat C.S., Oliver R.P., Friesen T.L. A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol 2010, 11:R109.
4. Han Y.N., Liu X.G., Benny U., Kistler H.C., VanEtten H.D. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 2001, 25:305-314.
5. Kämper J., Kahmann R., Bolker M., Ma L.J., Brefort T., Saville B.J., Banuett F., Kronstad J.W., Gold S.E., Muller O., et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444:97-101.
6. Spanu P.D., Abbott J.C., Amselem J., Burgis T.A., Soanes D.M., Stüber K., van Themaat E.V.L., Brown J.K.M., Butcher S.A., Gurr S.J., et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 2010, 330:1543-1546.
7. Martin F., Kohler A., Murat C., Balestrini R., Coutinho P.M., Jaillon O., Montanini B., Morin E., Noel B., Percudani R., et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038.
8. Martin F., Aerts A., Ahren D., Brun A., Danchin E.G.J., Duchaussoy F., Gibon J., Kohler A., Lindquist E., Pereda V., et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
9. Dean R.A., Talbot N.J., Ebbole D.J., Farman M.L., Mitchell T.K., Orbach M.J., Thon M., Kulkarni R., Xu J.R., Pan H.Q., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
10. Ma L.J., van der Does H.C., Borkovich K.A., Coleman J.J., Daboussi M.J., Di Pietro A., Dufresne M., Freitag M., Grabherr M., Henrissat B., et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373.
11. Cuomo C.A., Gueldener U., Xu J.R., Trail F., Turgeon B.G., Di Pietro A., Walton J.D., Ma L.J., Baker S.E., Rep M., et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
12. Coleman J.J., Rounsley S.D., Rodriguez-Carres M., Kuo A., Wasmann C.C., Grimwood J., Schmutz J., Taga M., White G.J., Zhou S.G., et al. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 2009, 5:e1000618.
13. Baxter L., Tripathy S., Ishaque N., Boot N., Cabral A., Kemen E., Thines M., Ah-Fong A., Anderson R., Badejoko W., et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 2010, 330:1549-1551.
14. Yoshida K., Saitoh H., Fujisawa S., Kanzaki H., Matsumura H., Yoshida K., Tosa Y., Chuma I., Takano Y., Win J., et al. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 2009, 21:1573-1591.
15. Hatta R., Ito K., Hosaki Y., Tanaka T., Tanaka A., Yamamoto M., Akimitsu K., Tsuge T. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 2002, 161:59-70.
16. Tzeng T.H., Lyngholm L.K., Ford C.F., Bronson C.R. A restriction-fragment-length-polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 1992, 130:81-96.
17. Leclair S., AnsanMelayah D., Rouxel T., Balesdent M.H. Meiotic behaviour of the minichromosome in the phytopathogenic ascomycete Leptosphaeria maculans. Curr Genet 1996, 30:541-548.
18. Chuma I., Tosa Y., Taga M., Nakayashiki H., Mayama S. Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Curr Genet 2003, 43:191-198.
19. Covert S.F. Supernumerary chromosomes in filamentous fungi. Curr Genet 1998, 33:311-319.
20. Wittenberg A.H.J., van der Lee T.A.J., Ben M'Barek S., Ware S.B., Goodwin S.B., Kilian A., Visser R.G.F., Kema G.H.J., Schouten H.J. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 2009, 4:e5863.
21. de Wit P., Mehrabi R., van den Burg H.A., Stergiopoulos I. Fungal effector proteins: past, present and future. Mol Plant Pathol 2009, 10:735-747.
22. Stukenbrock E.H., Jorgensen F.G., Zala M., Hansen T.T., McDonald B.A., Schierup M.H. Whole genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet 2010, 6:e1001189.
23. Temporini E.D., VanEtten H.D. 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 2004, 46:29-36.
24. Rodriguez-Carres A., White G., Tsuchiya D., Taga M., VanEtten H.D. The supernumerary chromosome of Nectria haematococca that carries pea-pathogenicity-related genes also carries a trait for pea rhizosphere competitiveness. Appl Environ Microbiol 2008, 74:3849-3856.
25. Proctor R.H., McCormick S.P., Alexander N.J., Desjardins A.E. Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 2009, 74:1128-1142.
26. Yu J.H., Keller N. Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 2005, 43:437-458.
27. Akagi Y., Akamatsu H., Otani H., Kodama M. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 2009, 8:1732-1738.
28. Walton J.D. Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 2000, 30:167-171.
29. Haas B.J., Kamoun S., Zody M.C., Jiang R.H.Y., Handsaker R.E., Cano L.M., Grabherr M., Kodira C.D., Raffaele S., Torto-Alalibo T., et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461:393-398.
30. Win J., Morgan W., Bos J., Krasileva K.V., Cano L.M., Chaparro-Garcia A., Ammar R., Staskawicz B.J., Kamoun S. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 2007, 19:2349-2369.
31. Schirawski J., Mannhaupt G., Munch K., Brefort T., Schipper K., Doehlemann G., Di Stasio M., Rossel N., Mendoza-Mendoza A., Pester D., et al. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 2010, 330:1546-1548.
32. Chen Q.H., Wang Y.C., Li A.N., Zhang Z.G., Zheng X.B. Molecular mapping of two cultivar-specific avirulence genes in the rice blast fungus Magnaporthe grisea. Mol Genet Genomics 2007, 277:139-148.
33. Gout L., Fudal I., Kuhn M.L., Blaise F., Eckert M., Cattolico L., Balesdent M.H., Rouxel T. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 2006, 60:67-80.
34. Fudal I., Ross S., Gout L., Blaise F., Kuhn M.L., Eckert M.R., Cattolico L., Bernard-Samain S., Balesdent M.H., Rouxel T. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant Microbe Interact 2007, 20:459-470.
35. Parlange F., Daverdin G., Fudal I., Kuhn M.L., Balesdent M.H., Blaise F., Grezes-Besset B., Rouxel T. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 2009, 71:851-863.
36. Fedorova N.D., Khaldi N., Joardar V.S., Maiti R., Amedeo P., Anderson M.J., Crabtree J., Silva J.C., Badger J.H., Albarraq A., et al. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 2008, 4:e1000046.
37. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
38. Barry J.D., Ginger M.L., Burton P., McCulloch R. Why are parasite contingency genes often associated with telomeres?. Int J Parasitol 2003, 33:29-45.
39. Thon M.R., Pan H.Q., Diener S., Papalas J., Taro A., Mitchell T.K., Dean R.A. The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae. Genome Biol 2006, 7:R16.
40. Daboussi M.J., Capy P. Transposable elements in filamentous fungi. Annu Rev Microbiol 2003, 57:275-299.
41. Friesen T.L., Stukenbrock E.H., Liu Z.H., Meinhardt S., Ling H., Faris J.D., Rasmussen J.B., Solomon P.S., McDonald B.A., Oliver R.P. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 2006, 38:953-956.
42. Novo M., Bigey F., Beyne E., Galeote V., Gavory F., Mallet S., Cambon B., Legras J.L., Wincker P., Casaregola S., et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci USA 2009, 106:16333-16338.
43. Schmitt I., Lumbsch H.T. Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 2009, 4:e4437.
44. Richards T.A., Dacks J.B., Jenkinson J.M., Thornton C.R., Talbot N.J. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 2006, 16:1857-1864.
45. Boto L. Horizontal gene transfer in evolution: facts and challenges. Proc R Soc B Biol Sci 2010, 277:819-827.
46. Rep M. Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 2005, 253:19-27.
47. Choi J., Park J., Kim D., Jung K., Kang S., Lee Y.H. Fungal secretome database: integrated platform for annotation of fungal secretomes. BMC Genomics 2010, 11:105.
48. Skibbe D.S., Doehlemann G., Fernandes J., Walbot V. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 2010, 328:89-92.
49. Marcel S., Sawers R., Oakeley E., Angliker H., Paszkowski U. Tissue-adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 2010, 22:3177-3187.
50. Panstruga R., Dodds P.N. Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 2009, 324:748-750.
51. Birch P.R.J., Boevink P.C., Gilroy E.M., Hein I., Pritchard L., Whisson S.C. Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr Opin Plant Biol 2008, 11:373-379.
52. Schornack S., van Damme M., Bozkurt T.O., Cano L.M., Smoker M., Thines M., Gaulin E., Kamoun S., Huitema E. Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci USA 2010, 107:17421-17426.
53. Godfrey D., Bohlenius H., Pedersen C., Zhang Z.G., Emmersen J., Thordal-Christensen H. Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 2010, 11:317.
54. Soanes D.M., Alam I., Cornell M., Wong H.M., Hedeler C., Paton N.W., Rattray M., Hubbard S.J., Oliver S.G., Talbot N.J. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One 2008, 3:e2300.
55. Mueller O., Kahmann R., Aguilar G., Trejo-Aguilar B., Wu A., de Vries R.P. The secretome of the maize pathogen Ustilago maydis. Fungal Genet Biol 2008, 45:S63-S70.
56. Hahn M., Mendgen K. Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact 1997, 10:427-437.
57. Struck C., Ernst M., Hahn M. Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol 2002, 3:23-30.
58. Voegele R.T., Struck C., Hahn M., Mendgen K. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 2001, 98:8133-8138.
59. Wahl R., Wippel K., Goos S., Kamper J., Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 2010, 8:1000303.
60. Chen L.Q., Hou B.H., Lalonde S., Takanaga H., Hartung M.L., Qu X.Q., Guo W.J., Kim J.G., Underwood W., Chaudhuri B., et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468. 527-U199.
61. Bhadauria V., Banniza S., Wei Y.D., Peng Y.L. Reverse genetics for functional genomics of phytopathogenic fungi and oomycetes. Comp Funct Genom 2009, 2009:380719.
62. Bignell D.R.D., Huguet-Tapia J.C., Joshi M.V., Pettis G.S., Loria R. What does it take to be a plant pathogen: genomic insights from Streptomyces species. Ant Leeuw Int J Gen Mol Microbiol 2010, 98:179-194.
63. Butler G., Rasmussen M.D., Lin M.F., Santos M.A.S., Sakthikumar S., Munro C.A., Rheinbay E., Grabherr M., Forche A., Reedy J.L., et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459:657-662.
64. Van De Wouw AP, Howlett HP: Fungal pathogenicity genes in the age of 'omics'. Mol Plant Pathol (in press). doi:10.1111/j.1364-3703.2010.00680.x.