How filamentous pathogens co-opt plants: The ins and outs of fungal effectors

Current Opinion in Plant Biology

Volumn 14, Issue 4, 2011, Pages 400-406

  De Jonge, Ronnie ^a   Bolton, Melvin D ^b   Thomma, Bart PHJ ^a,c  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

DISEASE RESISTANCE; FUNGUS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PLANT; PLANT CELL; PLANT DISEASE; REVIEW; SECRETION; VIRULENCE;

DISEASE RESISTANCE; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; HOST-PATHOGEN INTERACTIONS; MOLECULAR BIOLOGY; PLANT CELLS; PLANT DISEASES; PLANTS; VIRULENCE;

BACTERIA (MICROORGANISMS); OOMYCETES;

EID: 79958072903     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2011.03.005     Document Type: Review

References (53)

1. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 2010, 11:539-548.
2. Bolton M.D., Thomma B.P.H.J. The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiol Mol Pathol 2008, 72:104-110.
3. Michielse C.B., van Wijk R., Reijnen L., Manders E.M.M., Boas S., Olivain C., Alabouvette C., Rep M. The nuclear protein Sge1 of Fusarium oxysporum is required for parasitic growth. PLoS Pathog 2009, 5:e1000637.
4. Kim S., Hu J., Oh Y., Park J., Choi J., Lee Y.H., Dean R.A., Mitchell T.K. Combining ChIP-chip and expression profiling to model the MoCRZ1 mediated circuit for Ca/calcineurin signaling in the rice blast fungus. PLoS Pathog 2010, 20:e1000909.
5. Schumacher J., de Larrinoa I.F., Tudzynski B. Calcineurin-responsive zinc finger transcription factor CRZ1 of Botrytis cinerea is required for growth, development, and full virulence on bean plants. Eukaryot Cell 2008, 7:584-601.
6. Soriani F.M., Malavazi I., da Silva Ferreira M.E., Salvoldi M., Von Zeska Kress M.R., de Souza Goldman M.H.M., Loss O., Bignell E., Goldman G.H. Functional characterization of the Aspergillus fumigatus CRZ1 homologue, CrzA. Mol Microbiol 2008, 67:1274-1291.
7. 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.
8. Panstruga R., Dodds P.N. Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 2009, 324:748-750.
9. Kankanala P., Czymmek K., Valent B. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 2007, 19:706-724.
10. Khang C.H., Berruyer R., Giraldo M.C., Kankanala P., Park S.Y., Czymmek K., Kang S., Valent B. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 2010, 22:1388-1403.
11. Spanu P.D., Abbott J.C., Amselem J., Burgis T.A., Soanes D.M., Stüber K., Ver Loren van Themaat E., Brown J.K., Butcher S.A., Gurr S.J., et al. Genome expansion and gene loss in powdery mildew reveal tradeoffs in extreme parasitism. Science 2010, 330:1543-1546.
12. 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.
13. Tonukari N.J., Scott-Craig J.S., Walton J.D. The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell 2000, 12:237-248.
14. Ottmann C., Luberacki B., Küfner I., Koch W., Brunner F., Weyand M., Mattinen L., Pirhonen M., Anderluh G., Seitz H.U., et al. A common toxic fold mediates microbial attack and plant defense. Proc Natl Acad Sci U S A 2009, 106:10359-10364.
15. Motteram J., Küfner I., Deller S., Brunner F., Hammond-Kosack K.E., Nürnberger T., Rudd J.J. 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 2009, 22:790-799.
16. van Esse H.P., van 't Klooster J.W., Bolton M.D., Yadeta K.A., van Baarlen P., Boeren S., Vervoort J., de Wit P.J.G.M., Thomma B.P.H.J. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 2008, 20:1948-1963.
17. Shabab M., Shindo T., Gu C., Kaschani F., Pansuriya T., Chintha R., Harzen A., Colby T., Kamoun S., van der Hoorn R.A.L. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 2008, 20:1169-1183.
18. Song J., Win J., Tian M., Schornack S., Kaschani F., Ilyas M., van der Hoorn R.A.L., Kamoun S. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci U S A 2009, 106:1654-1659.
19. van den Burg H.A., Harrison S.J., Joosten M.H.A.J., Vervoort J., de Wit P.J.G.M. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 2006, 19:1420-1430.
20. de Jonge R., van Esse H.P., Kombrink A., Shinya T., Desaki Y., Bours R., van der Krol S., Shibuya N., Joosten M.H.A.J., Thomma B.P.H.J. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329:953-955.
21. Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., Minami E., Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A 2006, 103:11086-11091.
22. Shimizu T., Nakano T., Takamizawa D., Desaki Y., Ishii-Minami N., Nishizawa Y., Minami E., Okada K., Yamane H., Kaku H., Shibuya N. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 2010, 64:204-214.
23. Miya A., Albert P., Shinya T., Desaki Y., Ichimura K., Shirasu K., Narusaka Y., Kawakami N., Kaku H., Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 2007, 104:19613-19618.
24. Bolton M.D., van Esse H.P., Vossen J.H., de Jonge R., Stergiopoulos I., Stulemeijer I.J., van den Berg G.C., Borrás-Hidalgo O., Dekker H.L., de Koster C.G., et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 2008, 69:119-136.
25. de Jonge R., Thomma B.P.H.J. Fungal LysM effectors: extinguishers of host immunity?. Trends Microbiol 2009, 17:151-157.
26. Stergiopoulos I., van den Burg H.A., Okmen B., Beenen H.G., van Liere S., Kema G.H., de Wit P.J.G.M. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci U S A 2010, 107:7610-7615.
27. Ellis J.G., Dodds P.N., Lawrence G.J. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu Rev Phytopathol 2007, 45:289-306.
28. Rafiqi M., Gan P.H., Ravensdale M., Lawrence G.J., Ellis J.G., Jones D.A., Hardham A.R., Dodds P.N. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 2010, 22:2017-2032.
29. Kale S.D., Gu B., Capelluto D.G., Dou D., Feldman E., Rumore A., Arredondo F.D., Hanlon R., Fudal I., Rouxel T., et al. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 2010, 142:981-983.
30. Rehmany A.P., Gordon A., Rose L.E., Allen R.L., Armstrong M.R., Whisson S.C., Kamoun S., Tyler B.M., Birch P.R., Beynon J.L. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 2005, 17:1839-1850.
31. Whisson S.C., Boevink P.C., Moleleki L., Avrova A.O., Morales J.G., Gilroy E.M., Armstrong M.R., Grouffaud S., van West P., Chapman S., et al. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 2007, 450:115-118.
32. Dou D., Kale S.D., Wang X., Jiang R.H., Bruce N.A., Arredondo F.D., Zhang X., Tyler B.M. RXLR mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 2008, 20:1930-1947.
33. Gan P.H., Rafiqi M., Ellis J.G., Jones D.A., Hardham A.R., Dodds P.N. Lipid binding activities of flax rust AvrM and AvrL567 effectors. Plant Signal Behav 2010, 5:10.
34. 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 U S A 2010, 107:17421-17426.
35. Godfrey D., Böhlenius H., Pedersen C., Zhang Z., Emmersen J., Thordal-Christensen H. Powdery mildew fungal effectors candidates share N-terminal Y/F/WxC-motif. BMC Genomics 2010, 11:317.
36. Houterman P.M., Cornelissen B.J.C., Rep M. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 2008, 4:e1000061.
37. 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, 468:527-532.
38. Bolton M.D. Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 2009, 22:487-497.
39. Wahl R., Wippel K., Goos S., Kämper J., Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Pathog 2010, 8:e1000303.
40. Stukenbrock E.H., McDonald B.A. Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol Plant Microbe Interact 2009, 22:371-380.
41. Van de Wouw A.P., Cozijnsen A.J., Hane J.K., Brunner P.C., McDonald B.A., Oliver R.P., Howlett B.J. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLos Pathog 2010, 6:e1001180.
42. Rouxel T., Grandaubert J., Hane J.K., Hoede C., van de Wouw A.P., Couloux A., Dominguez V., Anthouard V., Bally P., Bourras S., et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2011, 2:202.
43. Raffaele S., Win J., Cano L.M., Kamoun S. Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genomics 2010, 11:637.
44. Raffaele S., Farrer R.A., Cano L.M., Studholme D.J., MacLean D., Thines M., Jiang R.H., Zody M.C., Kunjeti S.G., Donofrio N.M., et al. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 2010, 330:1540-1543.
45. Stukenbrock E.H., Jørgensen 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.
46. 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. Genomics islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 2008, 4:e1000046.
47. Lum G., Min X.J. FunSec KB: the Fungal Secretome Knowledge Base. Database 2011, 2011:bar001.
48. 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.
49. Schirawski J., Mannhaupt G., Münch K., Brefort T., Schipper K., Doehlemann G., Di Stasio M., Rössel N., Mendoza-Mendoza A., Pester D., et al. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 2010, 330:1546-1548.
50. Lorang J.M., Sweat T.A., Wolpert T.J. Plant disease susceptibility conferred by a " resistance" gene. Proc Natl Acad Sci U S A 2007, 104:14861-14866.
51. Nagy E.D., Bennetzen J.L. Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 2008, 18:1918-1923.
52. Faris J.D., Zhang Z., Lu H., Lu S., Reddy L., Cloutier S., Fellers J.P., Meinhardt S.W., Rasmussen J.B., Xu S.S., et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci U S A 2010, 107:13544-13549.
53. Thomma B.P.H.J., Nürnberger T., Joosten M.H.A.J. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 2011, 23:4-15.