Oomycete and fungal effector entry, a microbial Trojan horse

New Phytologist

Volumn 193, Issue 4, 2012, Pages 874-881

  Kale, Shiv D ^a  

^a VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

Effectors; Endocytosis; Fungi; Mutualists; Oomycetes; Pathogens; Phospholipids; RXLR and RXLR like

Indexed keywords

FUNGAL PROTEIN; PHOSPHOLIPID; POLYPHOSPHOINOSITIDE;

FUNGUS; HOST-PATHOGEN INTERACTION; INHIBITION; PHOSPHOLIPID; PROTEIN; SECRETION; SYMBIOSIS; TRANSLOCATION;

AMINO ACID SEQUENCE; CROP; FUNGUS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OOMYCETES; PATHOGENICITY; PHYSIOLOGY; PLANT; PLANT DISEASE; PROTEIN MOTIF; SHORT SURVEY; SYMBIOSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CROPS, AGRICULTURAL; FUNGAL PROTEINS; FUNGI; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; OOMYCETES; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOLIPIDS; PLANT DISEASES; PLANTS; SYMBIOSIS;

CERVIDAE; EQUIDAE; FUNGI; OOMYCETES;

EID: 84856520044     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03968.x     Document Type: Short Survey

References (42)

1. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
2. Boothroyd JC, Dubremetz JF. 2008. Kiss and spit: the dual roles of Toxoplasma rhoptries. Nature Reviews. Microbiology 6: 79-88.
3. E3 ligase CMPG1. Proceedings of the National Academy of Sciences, USA 107: 9909-9914.
4. Doherty GJ, McMahon HT. 2009. Mechanisms of endocytosis. Annual Review of Biochemistry 78: 857-902.
5. Dominguez V, Raimondi C, Somanath S, Bugliani M, Loder MK, Edling CE, Divecha N, da Silva-Xavier G, Marselli L, Persaud SJ et al. 2011. Class II phosphoinositide 3-kinase regulates exocytosis of insulin granules in pancreatic β cells. Journal of Biological Chemistry 286: 4216-4225.
6. Dou D, Kale SD, Wang X, Chen Y, Wang Q, Jiang RH, Arredondo FD, Anderson RG, Thakur PB, McDowell JM et al. 2008a. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20: 1118-1133.
7. Dou D, Kale SD, Wang X, Jiang RH, Bruce NA, Arredondo FD, Zhang X, Tyler BM. 2008b. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930-1947.
8. Falasca M, Maffucci T. 2009. Rethinking phosphatidylinositol 3-monophosphate. Biochimica et Biophysica Acta 1793: 1795-1803.
9. Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent MH, Rouxel T. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Molecular Plant-Microbe Interactions 20: 459-470.
10. Gan PH, Rafiqi M, Ellis JG, Jones DA, Hardham AR, Dodds PN. 2010. Lipid binding activities of flax rust AvrM and AvrL567 effectors. Plant Signaling and Behavior 5: 1272-1275.
11. Godfrey D, Bohlenius H, Pedersen C, Zhang Z, Emmersen J, Thordal-Christensen H. 2010. Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11: 317.
12. Grouffaud S, van West P, Avrova AO, Birch PR, Whisson SC. 2008. Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154: 3743-3751.
13. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
14. Heitman J. 2011. Microbial pathogens in the fungal kingdom. Fungal Biology Reviews 25: 48-60.
15. Houterman PM, Cornelissen BJ, Rep M. 2008. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 4: e1000061.
16. Jiang RH, Tripathy S, Govers F, Tyler BM. 2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences, USA 105: 4874-4879.
17. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
18. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T et al. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284-295.
19. Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, Maclean D et al. 2011. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biology 9: e1001094.
20. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388-1403.
21. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, Papenfuss AT, Sanders PR, Lundie RJ, Maier AG, Cowman AF et al. 2009. A newly discovered protein export machine in malaria parasites. Nature 459: 945-949.
22. Krag C, Malmberg EK, Salcini AE. 2010. PI3KC2α, a class II PI3K, is required for dynamin-independent internalization pathways. Journal of Cell Science 123: 4240-4250.
23. Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J et al. 2010. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biology 11: R73.
24. Lou Y, Ma H, Lin WH, Chu ZQ, Mueller-Roeber B, Xu ZH, Xue HW. 2006. The highly charged region of plant β-type phosphatidylinositol 4-kinase is involved in membrane targeting and phospholipid binding. Plant Molecular Biology 60: 729-746.
25. Mendoza L, Hernandez F, Ajello L. 1993. Life cycle of the human and animal oomycete pathogen Pythium insidiosum. Journal of Clinical Microbiology 31: 2967-2973.
26. Meng S, Torto-Alalibo T, Chibucos MC, Tyler BM, Dean RA. 2009. Common processes in pathogenesis by fungal and oomycete plant pathogens, described with Gene Ontology terms. BMC Microbiology 9(Suppl. 1): S7.
27. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333: 596-601.
28. Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, Cano LM, Win J, Bos JI, Liu HY, van Damme M et al. 2009. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928-2947.
29. Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, Brun A, Tyler BM, Pardo AG, Martin F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21: 1-7.
30. Rafiqi M, Gan PH, Ravensdale M, Lawrence GJ, Ellis JG, Jones DA, Hardham AR, Dodds PN. 2010. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22: 2017-2032.
31. Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JD, Brown JK. 2006. Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18: 2402-2414.
32. Sandvig K, van Deurs B. 2005. Delivery into cells: lessons learned from plant and bacterial toxins. Gene Therapy 12: 865-872.
33. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Gaulin E, Kamoun S, Huitema E. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proceedings of the National Academy of Sciences, USA 107: 17421-17426.
34. Shan W, Cao M, Leung D, Tyler BM. 2004. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions 17: 394-403.
35. Tseng TT, Tyler BM, Setubal JC. 2009. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiology 9(Suppl 1): S2.
36. Tyler BM 2011. Entry of oomycete and fungal effectors into host cells. In: Martin F, Kamoun S, eds. Effectors in plant-microbe interactions. Hoboken, NJ, USA: John Wiley & Sons, 245-277.
37. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.
38. Wang Q, Han C, Ferreira AO, Yu X, Ye W, Tripathy S, Kale SD, Gu B, Sheng Y, Sui Y et al. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23: 2064-2086.
39. van West P, de Bruijn I, Minor KL, Phillips AJ, Robertson EJ, Wawra S, Bain J, Anderson VL, Secombes CJ. 2010. The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS (Federation of European Microbiological Societies) Microbiology Letters 310: 127-137.
40. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115-118.
41. 3a is required for its stability in host cells to modulate plant immunity. Proceedings of the National Academy of Sciences, USA 108: 14682-14687.
42. Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Tosa Y, Chuma I, Takano Y, Win J, Kamoun S et al. 2009. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21: 1573-1591.