In vitro translocation experiments with RxLR-reporter fusion proteins of avr1b from phytophthora sojae and AVR3a from phytophthora infestans fail to demonstrate specific autonomous uptake in plant and animal cells

Molecular Plant-Microbe Interactions

Volumn 26, Issue 5, 2013, Pages 528-536

  Wawra, Stephan ^a   Djamei, Armin ^b   Albert, Isabell ^c   Nürnberger, Thorsten ^c   Kahmann, Regine ^b   Van West, Pieter ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN;

ANIMAL; ARTICLE; GENETICS; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; RECOMBINANT FUSION PROTEINS;

ANIMALIA; EUKARYOTA; OOMYCETES; PHYTOPHTHORA INFESTANS; PHYTOPHTHORA SOJAE;

EID: 84875972308     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-08-12-0200-R     Document Type: Article

References (34)

1. Baxter. L., Tripathy. S., Ishaque. N., Boot. N., Cabral, A., Kemen, E., Thines, M., Ah-Fong, A., Anderson, R., Badejoko, W., Bittner-Eddy, P., Boore, J. L., Chibucos, M. C., Coates, M., Dehal, P., Delehaunty, K., Dong, S., Downton, P., Dumas, B., Fabro, G., Fronick, C., Fuerstenberg, S. I., Fulton, L., Gaulin, E., Govers, F., Hughes, L., Humphray, S., Jiang, R. H. Y., Judelson, H., Kamoun, S., Kyung, K., Meijer, H., Minx, P., Morris, P., Nelson, J., Phuntumart, V., Qutob, D., Rehmany, A., Rougon- Cardoso, A., Ryden, P., Torto-Alalibo, T., Studholme, D., Wang, Y., Win, J., Wood, J., Clifton, S. W., Rogers, J., Van den Ackerveken, G., Jones, J. D. G., McDowell, J. M., Beynon, J., and Tyler, B. M. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:1549-1551.
2. Bernoux, M., Ellis, J. G., and Dodds, P. N. 2011. New insights in plant immunity signaling activation. Curr. Opin. Plant Biol. 14:512-518.
3. Birch, P. R., Armstrong, M., Bos, J., Boevink, P., Gilroy, E. M., Taylor, R. M., Wawra, S., Pritchard, L., Conti, L., Ewan, R., Whisson, S. C., van West, P., Sadanandom, A., and Kamoun, S. 2009. Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J. Exp. Bot. 60:1133-1140.
4. Bos J. I., Kanneganti, T. D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M. R., Birch, P. R., and Kamoun, S. 2006. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J. 48:165-176.
5. Bos, J. I., Armstrong, M. R., Gilroy, E. M., Boevink, P. C., Hein, I., Taylor, R. M., Zhendong, T., Engelhardt, S., Vetukuri, R. R., Harrower, B., Dixelius, C., Bryan, G., Sadanandom, A., Whisson, S. C., Kamoun, S., and Birch, P. R. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc. Natl. Acad. Sci. U.S.A. 107:9909-9914.
6. Boutemy, L. S., King, S. R., Win, J., Hughes, R. K., Clarke, T. A., Blumenschein, T. M., Kamoun, S., and Banfield, M. J. 2011. Structures of Phytophthora RXLR effector proteins: A conserved but adaptable fold underpins functional diversity. J. Biol. Chem. 286:35834- 35842.
7. Bozkurt, T. O., Schornack, S., Banfield, M. J., and Kamoun, S. 2012. Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15:483- 492.
8. Djamei, A., Schipper, K., Rabe, F., Ghosh, A., Vincon, V., Kahnt, J., Osorio, S., Tohge, T., Fernie, A. R., Feussner, I., Feussner, K., Meinicke, P., Stierhof, Y. D., Schwarz, H., Macek, B., Mann, M., and Kahmann, R. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395- 398.
9. Dou, D., Kale, S. D., Wang, X., Chen, Y., Wang, Q., Jiang, R. H., Arredondo, F. D., Anderson, R. G., Thakur, P. B., McDowell, J. M., Wang, Y., Tyler, B. M. 2008a. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20:1118-1133.
10. Dou, D., Kale, S. D., Wang, X., Jiang, R. H., Bruce, N. A., Arredondo, F. D., Zhang, X., and Tyler, B. M. 2008b. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20:1930-1947.
11. Ellis, J. G., and Dodds, P. N. 2011. Showdown at the RXLR motif: Serious differences of opinion in how effector proteins from filamentous eukaryotic pathogens enter plant cells. Proc. Natl. Acad. Sci. U.S.A. 108:14381-14382.
12. Grouffaud, S., van West, P., Avrova, A. O., Birch, P. R., and Whisson, S. C. 2008. Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154:3743-3751.
13. Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M. A., Fugelstad, J., Gilroy, E. M., Gnerre, S., Green, P. J., Grenville-Briggs, L. J., Griffith, J., Grunwald, N. J., Horn, K., Horner, N. R., Hu, C. H., Huitema, E., Jeong, D. H., Jones, A. M., Jones, J. D., Jones, R. W., Karlsson, E. K., Kunjeti, S. G., Lamour, K., Liu, Z., Ma, L., Maclean, D., Chibucos, M. C., McDonald, H., McWalters, J., Meijer, H. J., Morgan, W., Morris, P. F., Munro, C. A., O'Neill, K., Ospina- Giraldo, M., Pinzon, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D. C., Schumann, U. D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D. J., Sykes, S., Thines, M., van de Vondervoort, P. J., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zhou, S., Fry, W., Meyers, B. C., van West, P., Ristaino, J., Govers, F., Birch, P. R., Whisson, S. C., Judelson, H. S., and Nusbaum, C.. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398.
14. He, S. Y., Nomura, K., and Whittam, T. S. 2004. Type III protein secretion mechanism in mammalian and plant pathogens. Biochim. Biophys. Acta 1694:181-206.
15. Heim, R., Prasher, D. C., and Tsien, R. Y. 1994. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 91:12501-12504.
16. Hiller, G., and Weber, K. 1978. Radioimmunoassay for tubulin: A quantitative comparison of the tubulin content of different established tissue culture cells and tissues. Cell 14:795-804.
17. Kale, S. D., and Tyler, B. M. 2011. Entry of oomycete and fungal effectors into plant and animal host cells. Cell. Microbiol. 13:1839-1848.
18. Kale, S. D., Gu, B., Capelluto, D. G., Dou, D., Feldman, E., Rumore, A., Arredondo, F. D., Hanlon, R., Fudal, I., Rouxel, T., Lawrence, C. B., Shan, W., and Tyler, B. M. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284-295.
19. Kerrigan, A. M., and Brown, G. D. 2009. C-type lectins and phagocytosis. Immunobiology 214:562-575.
20. Liu, S.-L., Zhang, Z.-L., Sun, E.-Z., Peng, J., Xie, M., Tian, Z.-Q., Lin, Y., and Pang, D.-W. 2011. Visualizing the endocytic and exocytic processes of wheat germ agglutinin by quantum dot-based single-particle tracking. Biomaterials 32:7616-7624.
21. Malmstrom, J., Beck, M., Schmidt, A., Lange, V., Deutsch, E. W., and Aebersold, R. 2009. Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460:762-765.
22. Mattoo, S., Lee, Y. M., and Dixon, J. E. 2007. Interactions of bacterial effector proteins with host proteins. Curr. Opin. Immunol. 19:392- 401.
23. Paungfoo-Lonhienne, C., Lonhienne, T. G., Rentsch, D., Robinson, N., Christie, M., Webb, R. I., Gamage, H. K., Carroll, B. J., Schenk, P. M., and Schmidt, S. 2008. Plants can use protein as a nitrogen source without assistance from other organisms. Proc. Natl. Acad. Sci. U.S.A. 105:4524-4529.
24. Plett, J. M., Kemppainen, M., Kale, S. D., Kohler, A., Legue, V., Brun, A., Tyler, B. M., Pardo, A. G., and Martin, F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21:1197-1203.
25. Ravensdale, M., Nemri, A., Thrall, P. H., Ellis, J. G., and Dodds, P. N. 2011. Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Mol. Plant Pathol. 12:93-102.
26. 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., and Beynon, J. L. 2005. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839-1850.
27. Reid, B. G., and Flynn, G. C. 1997. Chromophore formation in green fluorescent protein. Biochemistry 36:6786-6791.
28. Sharon, N. 1984. Carbohydrates as recognition determinants in phagocytesis and in lectin-mediated killing of target cells. Biol. Cell 51:239-245.
29. Stergiopoulos, I., and de Wit, P. J. 2009. Fungal effector proteins. Annu. Rev. Phytopathol. 47:233-263.
30. van West, P., de Bruijn, I., Minor, K. L., Phillips, A. J., Robertson, E. J., Wawra, S., Bain, J., Anderson, V. L., and Secombes, C. J. 2010. The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiol. Lett. 310:127-137.
31. Verkhusha, V. V., Kuznetsova, I. M., Stepanenko, O. V., Zaraisky, A. G., Shavlovsky, M. M., Turoverov, K. K., and Uversky, V. N. 2003. High stability of Discosoma DsRed as compared to Aequorea EGFP. Biochemistry 42:7879-7884.
32. Wawra, S., Bain, J., Durward, E., de Bruijn, I., Minor, K. L., Matena, A., Löbach, L., Whisson, S. C., Bayer, P., Porter, A. J., Birch, P. R. J., Secombes, C. J., and van West, P. 2012. Host-targeting protein 1 (SpHtp1) from the oomycete Saprolegnia parasitica translocates specifically into fish cells in a tyrosine-O-sulphate-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 109:2096-2101.
33. 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., Hein, I., Toth, I. K., Pritchard, L., and Birch, P. R. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115-118.
34. Yaeno, T., Li, H., Chaparro-Garcia, A., Schornack, S., Koshiba, S., Watanabe, S., Kigawa, T., Kamoun, S., and Shirasu, K. 2011. Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc. Natl. Acad. Sci. U.S.A. 108:14682-14687.