Live-cell imaging of endocytosis during conidial germination in the rice blast fungus, Magnaporthe grisea

Fungal Genetics and Biology

Volumn 37, Issue 3, 2002, Pages 233-244

  Atkinson, Helen A ^a   Daniels, Alison ^b   Read, Nick D ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Aventis Crop Science   (United Kingdom)

Author keywords

Confocal microscopy; Conidia; Endocytosis; FM4 64; Fungal spore; Germination; Live cell imaging; Magnaporthe grisea; Rice blast

Indexed keywords

BIOLOGICAL MARKER; DEXTRAN; DYE; LUCIFER YELLOW;

ARTICLE; CONFOCAL MICROSCOPY; CONIDIUM; ENDOCYTOSIS; FUNGAL CELL; FUNGUS SPORE; GERMINATION; HYDRATION; MAGNAPORTHE GRISEA; NONHUMAN; PRIORITY JOURNAL; RICE BLAST; TEMPERATURE;

ENDOCYTOSIS; FLUORESCENT DYES; MAGNAPORTHE; MICROSCOPY, CONFOCAL; ORYZA SATIVA; PLANT DISEASES; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; SPORES, FUNGAL;

FUNGI; MAGNAPORTHE; MAGNAPORTHE GRISEA;

EID: 0036438765     PISSN: 10871845     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1087-1845(02)00535-2     Document Type: Article

References (55)

1. Ashford, A.E., 1998. Dynamic pleiomorphic vacuole systems: Are they endosomes and transport compartments in fungal hyphae? Adv. Bot. Res. 28, 119-159.
2. Atkinson, H.A., 2001. Spore Germination in the Rice Blast Fungus, Magnaporthe grisea. Ph.D. Thesis, University of Edinburgh.
3. Ballatori, N., Hager, D.N., Nundy, S., Miller, D.S., Boyer, J.L., 1999. Carrier-mediated uptake of Lucifer Yellow in skate and rat hepatocytes: A fluid-phase marker revisited. Am. J. Physiol. Gastrointest. Liver Physiol. 277, G896-G904.
4. Betz, W.J., Mao, F., Orlovich, D.A., 1996. Imaging exocytosis and endocytosis. Fungal Genet. Biol. 6, 365-371.
5. Bourett, T.M., Howard, R., 1990. In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Can. J. Bot. 68, 329-342.
6. Bourett, T.M., Howard, R.J., 1994. Enhanced labelling of concanavalin A binding sites in fungal endomembranes using a double-sided, indirect method. Mycol. Res. 98, 769-775.
7. Braun, E.J., Howard, R.J., 1994. Adhesion of fungal spores and germlings to host surfaces. Protoplasma 181, 202-212.
8. Clague, M., 1998. Molecular aspects of the endocytic pathway. Biochem. J. 336, 271-282.
9. Cole, L., Coleman, J., Kearns, A., Morgan, G., Hawes, C., 1991. The organic anion transport inhibitor, probenecid inhibits the transport of Lucifer Yellow at the plasma membrane and the tonoplast in suspension cultured plant cells. J. Cell Sci. 99, 545-555.
10. Cole, L., Hyde, G.J., Ashford, A.E., 1997. Uptake and compartmentalisation of fluorescent probes by Pisolithus tinctorius hyphae: Evidence for an anion transport mechanism at the tonoplast but not for fluid-phase endocytosis. Protoplasma 199, 18-29.
11. Cole, L., Orlovich, D.A., Ashford, A.E., 1998. Structure, function and motility of vacuoles in filamentous fungi. Fungal Genet. Biol. 24, 86-100.
12. Deli, M.A., Abraham, C.S., Takahata, H., Katamine, S., Niwa, M., 2000. Pentosan polysulfate regaultes scavenger receptor-mediated, but not fluid-phase, endocytosis in immortalized cerebral endothelial cells. Cell. Mol. Neurobiol. 20, 731-745.
13. DeZwaan, T.M., Carroll, A.M., Valent, B., Sweigard, J.A., 1999. Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11, 2013-2030.
14. D'Hondt, K., Heese-Peck, A., Riezman, H., 2000. Protein and lipid requirements for endocytosis. Annu. Rev. Genet. 34, 225-295.
15. Emans, N., Zimmerman, S., Fischer, R., 2002. Uptake of a fluorescent marker in plant cells is sensitive to Brefeldin A and Wortmannin. Plant Cell 14, 71-86.
16. Epstein, L., Nicholson, R.L., 1997. Adhesion of spores and hyphae to plant surfaces. In: Carroll, G.C., Tudzynski, P. (Eds.), The Mycota. Vol. V. Plant Relationships Part A. Springer-Verlag, Berlin, pp. 11-25.
17. Fischer-Parton, S., Parton, R.M., Hickey, P.C., Dijksterhuis, J., Atkinson, H.A., Read, N.D., 2000. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 198, 246-259.
18. Gilbert, R.D., Johnson, A.M., Dean, R.A., 1996. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol. Mol. Plant Pathol. 48, 335-346.
19. Goldstein, J.L., Brown, M.S., Anderson, R.G.W., Russell, D.W., Schneider, W.J., 1985. Receptor mediated endocytosis. Annu. Rev. Cell Biol. 1, 1-39.
20. Gull, K., Trinci, A.P.J., 1971. Fine structure of spore germination in Botrytis cinerea. J. Gen. Microbiol. 68, 207-220.
21. Hamer, J.E., Howard, R.J., Chumley, F.G., 1988. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239, 288-290.
22. Hawes, C., Crooks, K., Coleman, J., Satiat-Jeunemaitre, B., 1995. Endocytosis in plants: Fact or artefact? Plant Cell Environ. 18, 1245-1252.
23. Hoffman, J., Mendgen, K., 1998. Endocytosis and membrane turnover in the germ tube of Uromyces fabae. Fungal Genet. Biol. 24, 77-85.
24. Howard, R.J., Valent, B., 1996. Breaking and entering: Host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 50, 491-512.
25. Jelitto, T.C., Page, H.A., Read, N.D., 1994. Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus, Magnaporthe grisea. Planta 194, 471-477.
26. Jitsuyama, Y., Suzuki, T., Harada, T., Fujikawa, S., 2001. Loading process of sugars into cabbage petiole and asparagus shoot apex cells by incubation with hypertonic sugar solution. Protoplasma 217, 205-216.
27. Jones, G.L., Bailey, J.A., O'Connell, R.J., 1995. Sensitive staining of fungal extracellular matrices using colloidal gold. Mycol. Res. 99, 567-573.
28. Klein, M., Martinoia, E., Weissenböck, G., 1997. Transport of Lucifer Yellow CH into plant vacuoles evidence for direct energization of a sulphonated substance and implications for the design of new molecular probes. FEBS Lett. 420, 86-92.
29. Klionsky, D.J., 1997. Protein transport from the cytoplasm into the vacuole. J. Membr. Biol. 157, 105-115.
30. Klionsky, D.J., Herman, P.K., Emr, S.D., 1990. The fungal vacuole: Composition, function, and biogenesis. Microbiol. Rev. 54, 266-292.
31. Marcote, M.J., Gu, F., Gruenberg, J., Aniento, F., 2000. Membrane transport in the endocytic pathway: Animal versus plant cells. Protoplasma 210, 123-132.
32. Mellman, I., 1996. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
33. Nielsen, K.A., Nicholson, R.L., Carver, T.L.W., Kunoh, H., Oliver, R.P., 2000. First touch: An immediate response to surface recognition in conidia of Blumeria graminis. Physiol. Mol. Plant Pathol. 56, 63-70.
34. O'Driscoll, D., Wilson, G., Steer, M.W., 1991. Lucifer Yellow and fluorescein isothiocyanate uptake by cells of Morinda citrifolia in suspension-cultures is not confined to the endocytic pathway. J. Cell. Sci. 100, 237-241.
35. Oparka, K.J., Murant, E.A., Wright, K.M., Prior, D.A.M., Harris, N., 1991. The drug probenecid inhibits the transport of fluorescent anions across the tonoplast of onion epidermal cells. J. Cell Sci. 99, 557-563.
36. Ou, S.H., 1980. A look at worldwide rice blast disease control. Plant Dis. 64, 439-445.
37. Padron, D., Bizeau, M.E., Hazel, J.R., 2000. Is fluid-phase endocytosis conserved in hepatocytes of species acclimated and adapted to different temperatures? Am. J. Physiol. Regulat. Integrat. Compar. Physiol. 278, R529-R536.
38. Parton, R.M., Fischer-Parton, S., Watahiki, M.K., Trewavas, A.J., 2001. Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J. Cell Sci. 114, 2685-2695.
39. Punnonen, E.-L., Ryhänen, K., Marojomäki, V.S., 1998. At reduced temperature, endocytic membrane traffic is blocked in multivesicular carrier endosomes in rat cardiac myocytes. Eur. J. Cell Biol. 75, 344-352.
40. Read, N.D., Hickey, P.C., 2001. The vesicle trafficking network and tip growth in fungal hyphae. In: Geitmann, A., Cresti, M., Heath, I.B. (Eds.), Cell Biology of Plant and Fungal Tip Growth. IOS Press, Amsterdam, pp. 137-148.
41. Reizman, H., 1985. Endocytosis in yeast: Several of the yeast secretory mutants are defective in endocytosis. Cell 40, 1001-1009.
42. Steinberg, G., Schliwa, M., Lehmler, C., Bölker, M., Kahmann, R., McIntosh, J.R., 1998. Kinesin from the plant pathogenic fungus Ustilago maydis in vacuole formation and cytoplasmic migration. J. Plant Sci. 111, 2235-2246.
43. Steinberg, T.H., Swanson, J.A., Silverstein, S.C., 1987. A prelysosomal compartment sequesters membrane-impermeant fluorescent dyes from the cytoplasmic matrix of J774 macrophages. J. Cell Biol. 107, 887-897.
44. Sweigard, J.A., Chumley, F.G., Valent, B., 1992. Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 232, 183-190.
45. Tyteca, D., Van Der Smisson, P., Vam Bambeke, F., Leys, K., Tulkens, P.M., Courtoy, P.J., Mingeot-Leclerq, M.P., 2001. Azithromycin, a lysosomotropic antibiotic, impairs fluid-phase pinocytosis in cultured fibroblasts. Eur. J. Cell Biol. 80, 466-478.
46. Valent, B., Farral, L., Chumley, F.G., 1991. Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127, 87-101.
47. Van Dyke, G.C., Mims, C.W., 1991. Ultrastructure of conidia germination, and appressorium development in the plant pathogenic fungus Colletotrichum truncatum. Can. J. Bot. 69, 2455-2467.
48. Vida, T.A., Emr, S.D., 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792.
49. Weber, R.W.S., Wakley, G.E., Thines, E., Talbot, N.J., 2001. The vacuole as central element of the lytic system and sink for lipid droplets in maturing appressoria of Magnaporthe grisea. Protoplasma 216, 101-112.
50. Weiderkehr, A., Meier, K.D., Reizman, H., 2001. Identification and characterization of Saccharomyces cerevisiae mutants defective in fluid-phase endocytosis. Yeast 18, 759-773.
51. Wendland, B., Emr, S.D., Riezman, H., 1998. Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 10, 513-522.
52. Xiao, J., Ohshima, A., Kamakura, T., Ishiyama, T., Yamaguchi, I., 1994a. Extracellular glycoprotein(s) associated with cellular differentiation in Magnaporthe grisea. Mol. Plant Microbe Interact. 7, 639-644.
53. Xiao, J.-Z., Watanabe, T., Kamakura, T., Ohshima, A., Yamaguchi, I., 1994b. Studies on cellular differentiation of Magnaporthe grisea. Physicochemical aspects of substratum surfaces in relation to appressorium formation. Physiol. Mol. Plant Pathol. 44, 227-236.
54. Zeigler, R.S., Leong, S.A., Teng, P.S., 1994. Rice Blast Disease. CAB International with International Rice Research Institute, Oxon, UK.
55. Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., Fan, J., Yang, S., Hu, L., Leung, H., Mew, T.W., Teng, P.S., Wang, Z., Mundt, C.C., 2000. Genetic diversity and disease control in rice. Nature 406, 718-722.