Fluorescent markers of the endocytic pathway in Zymoseptoria tritici

Fungal Genetics and Biology

Volumn 79, Issue , 2015, Pages 150-157

  Kilaru, S ^a   Schuster, M ^a   Latz, M ^a   Guo, M ^a   Steinberg, G ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Actin patches; Endosomes; Mycosphaerella graminicola; Pathogenic fungi; Septoria tritici blotch

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; FIMBRIN; RAB PROTEIN; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; PLASTIN;

ARTICLE; CELL LABELING; CELL MEMBRANE; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FUNGAL STRAIN; FUNGUS MUTANT; IMAGING SYSTEM; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; WHEAT; ZYMOSEPTORIA TRITICI; ASCOMYCETES; FLUORESCENCE IMAGING; GENETICS; PHYSIOLOGY; PROCEDURES; REPORTER GENE; STAINING;

FUNGI; MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

ASCOMYCOTA; ENDOCYTOSIS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; OPTICAL IMAGING; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING;

EID: 84937580390     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2015.03.019     Document Type: Article

References (61)

1. Abenza J.F., Pantazopoulou A., Rodriguez J.M., Galindo A., Penalva M.A. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 2009, 10:57-75.
2. Abenza J.F., Galindo A., Pinar M., Pantazopoulou A., de los Rios V., Penalva M.A. Endosomal maturation by Rab conversion in Aspergillus nidulans is coupled to dynein-mediated basipetal movement. Mol. Biol. Cell 2012, 23:1889-1901.
3. Araujo-Bazán L., Peñalva M.A., Espeso E.A. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol. Microbiol. 2008, 67:891-905.
4. Basu R., Munteanu E.L., Chang F. Role of turgor pressure in endocytosis in fission yeast. Mol. Biol. Cell 2014, 25:679-687.
5. Baumann S., Pohlmann T., Jungbluth M., Brachmann A., Feldbrügge M. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J. Cell Sci. 2012, 125:2740-2752.
6. Berepiki A., Lichius A., Shoji J.Y., Tilsner J., Read N.D. F-actin dynamics in Neurospora crassa. Eukaryot. Cell 2010, 9:547-557.
7. Berepiki A., Lichius A., Read N.D. Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 2011, 9:876-887.
8. Bielska E., Higuchi Y., Schuster M., Steinberg N., Kilaru S., Talbot N.J., Steinberg G. Long-distance endosome trafficking drives fungal effector production during plant infection. Nat. Commun. 2014, 5:5097.
9. Bretscher A. Fimbrin is a cytoskeletal protein that crosslinks F-actin in vitro. Proc. Natl. Acad. Sci. USA 1981, 78:6849-6853.
10. Castillo-Lluva S., Alvarez-Tabares I., Weber I., Steinberg G., Perez-Martin J. Sustained cell polarity and virulence in the phytopathogenic fungus Ustilago maydis depends on an essential cyclin-dependent kinase from the Cdk5/Pho85 family. J. Cell Sci. 2007, 120:1584-1595.
11. Chavrier P., Parton R.G., Hauri H.P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 1990, 62:317-329.
12. Dean R., Van Kan J.A., Pretorius Z.A., Hammond-Kosack K.E., Di Pietro A., Spanu P.D., Rudd J.J., Dickman M., Kahmann R., Ellis J., Foster G.D. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 2012, 13:414-430.
13. Delgado-Alvarez D.L., Callejas-Negrete O.A., Gomez N., Freitag M., Roberson R.W., Smith L.G., Mourino-Perez R.R. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet. Biol., FG & B 2010, 47:573-586.
14. Egan M.J., McClintock M.A., Reck-Peterson S.L. Microtubule-based transport in filamentous fungi. Curr. Opin. Microbiol. 2012, 15:637-645.
15. Egan M.J., Tan K., Reck-Peterson S.L. Lis1 is an initiation factor for dynein-driven organelle transport. J. Cell Biol. 2012, 197:971-982.
16. Fischer-Parton S., Parton R.M., Hickey P.C., Dijksterhuis J., Atkinson H.A., Read N.D. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 2000, 198:246-259.
17. Fuchs U., Steinberg G. Endocytosis in the plant-pathogenic fungus Ustilago maydis. Protoplasma 2005, 226:75-80.
18. Fuchs U., Hause G., Schuchardt I., Steinberg G. Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 2006, 18:2066-2081.
19. Goodwin S.B., M'Barek S.B., Dhillon B., Wittenberg A.H., Crane C.F., Hane J.K., et al. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 2011, 7:e1002070.
20. Gurr S.J., Fones H. The impact of Septoria tritici Blotch disease on wheat: an EU perspective. Fungal Genet. Biol. 2015, 79:3-7.
21. Harris S.D., Read N.D., Roberson R.W., Shaw B., Seiler S., Plamann M., Momany M. Polarisome meets spitzenkorper, microscopy, genetics, and genomics converge. Eukaryot. Cell 2005, 4:225-229.
22. Higuchi, Y., Steinberg, G., 2015. Early endosomes motility in filamentous fungi, How and why they move. Fungal Biol. Rev. http://dx.doi.org/10.1016/j.fbr.2015.02.002.
23. Higuchi Y., Shoji J.Y., Arioka M., Kitamoto K. Endocytosis is crucial for cell polarity and apical membrane recycling in the filamentous fungus Aspergillus oryzae. Eukaryot. Cell 2009, 8:37-46.
24. Higuchi Y., Ashwin P., Roger Y., Steinberg G. Early endosome motility spatially organizes polysome distribution. J. Cell Biol. 2014, 204:343-357.
25. Holsters M., de Waele D., Depicker A., Messens E., van Montagu M., Schell J. Transfection and transformation of Agrobacterium tumefaciens. Mol. Gen. Genet. 1978, 163:181-187.
26. Hood E., Gelvin S.B., Melchers L., Hoekema A. New Agrobacterium helper plasmids for gene transfer to plants. Transgen. Res. 1993, 2:208-218.
27. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 2003, 115:475-487.
28. Kema G.H.J., van Silfhout C.H. Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem. III. Comparative seedling and adult plant experiments. Phytopathology 1997, 87:266-272.
29. Kilaru S., Steinberg G. Yeast recombination-based cloning as an efficient way of constructing vectors for Zymoseptoria tritici. Fungal Genet. Biol. 2015, 79:76-83.
30. Kilaru S., Schuster M., Latz M., Das Gupta S., Steinberg N., Fones H., Gurr S., Talbot N.J., Steinberg G. A gene locus for targeted ectopic gene integration in Zymoseptoria tritici. Fungal Genet. Biol. 2015, 79:118-124.
31. Kovar D.R., Sirotkin V., Lord M. Three's company, the fission yeast actin cytoskeleton. Trend Cell Biol. 2011, 21:177-187.
32. Lee S.C., Schmidtke S.N., Dangott L.J., Shaw B.D. Aspergillus nidulans ArfB plays a role in endocytosis and polarized growth. Eukaryot. Cell 2008, 7:1278-1288.
33. Lenz J.H., Schuchardt I., Straube A., Steinberg G. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J. 2006, 25:2275-2286.
34. Mehrabi R., Zwiers L.H., de Waard M.A., Kema G.H. MgHog1 regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola. Mol. Plant Microb. Interact. 2006, 19:1262-1269.
35. Motteram J., Lovegrove A., Pirie E., Marsh J., Devonshire J., van de Meene A., Hammond-Kosack K., Rudd J.J. Aberrant protein N-glycosylation impacts upon infection-related growth transitions of the haploid plant-pathogenic fungus Mycosphaerella graminicola. Mol. Microbiol. 2011, 81:415-433.
36. Penalva M.A. Endocytosis in filamentous fungi, Cinderella gets her reward. Curr. Opin. Microbiol. 2010, 13:684-692.
37. Raymond C.K., Pownder T.A., Sexson S.L. General method for plasmid construction using homologous recombination. Biotechniques 1999, 26:134-141.
38. Riquelme M., Sanchez-Leon E. The Spitzenkörper, a choreographer of fungal growth and morphogenesis. Curr. Opin. Microbiol. 2014, 20:27-33.
39. Sambrook J., Russell D.W. Molecular Cloning 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
40. Schuster M., Kilaru S., Ashwin P., Lin C., Severs N.J., Steinberg G. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J. 2011, 30:652-664.
41. Schuster M., Lipowsky R., Assmann M.A., Lenz P., Steinberg G. Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc. Natl. Acad. Sci. USA 2011, 108:3618-3623.
42. Schuster M., Kilaru S., Latz M., Steinberg G. Fluorescent markers of the microtubule cytoskeleton in Zymoseptoria tritici. Fungal Genet. Biol. 2015, 10.1016/j.fgb.2015.03.005.
43. Seidel C., Moreno-Velasquez S.D., Riquelme M., Fischer R. Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot. Cell 2013, 12:1020-1032.
44. Shaw B.D., Chung D.W., Wang C.L., Quintanilla L.A., Upadhyay S. A role for endocytic recycling in hyphal growth. Fungal Biol. 2011, 115:541-546.
45. Skau C.T., Kovar D.R. Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast. Curr. Biol., CB 2010, 20:1415-1422.
46. Spector I., Shochet N.R., Kashman Y., Groweiss A. Latrunculins, novel marine toxins that disrupt microfilament organization in cultured cells. Science 1983, 219:493-495.
47. Steinberg G. Hyphal growth, a tale of motors, lipids, and the Spitzenkörper. Eukaryot. Cell 2007, 6:351-360.
48. Steinberg G. Endocytosis and early endosome motility in filamentous fungi. Curr. Opin. Microbiol. 2014, 20:10-18.
49. Steinberg G. Cell biology of Zymoseptoria tritici: Pathogen cell organization and wheat infection. Fungal Genet. Biol. 2015, 79:17-23.
50. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5, molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
51. Tang X., Halleck M.S., Schlegel R.A., Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 1996, 272:1495-1497.
52. Upadhyay S., Shaw B.D. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol. Microbiol. 2008, 68:690-705.
53. Warren D.T., Andrews P.D., Gourlay C.W., Ayscough K.R. Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics. J. Cell Sci. 2002, 115:1703-1715.
54. Wedlich-Söldner R., Bölker M., Kahmann R., Steinberg G. A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 2000, 19:1974-1986.
55. Wedlich-Söldner R., Straube A., Friedrich M.W., Steinberg G. A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J. 2002, 21:2946-2957.
56. Wu J.Q., Bähler J., Pringle J.R. Roles of a fimbrin and an alpha-actinin-like protein in fission yeast cell polarization and cytokinesis. Mol. Biol. Cell 2001, 12:1061-1077.
57. Xiang X., Plamann M. Cytoskeleton and motor proteins in filamentous fungi. Curr. Opin. Microbiol. 2003, 6:628-633.
58. Zekert N., Fischer R. The Aspergillus nidulans kinesin-3 UncA motor moves vesicles along a subpopulation of microtubules. Mol. Biol. Cell 2009, 20:673-684.
59. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.
60. Zhang J., Zhuang L., Lee Y., Abenza J.F., Penalva M.A., Xiang X. The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J. Cell Sci. 2010, 123:3596-3604.
61. Zwiers L.H., De Waard M.A. Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr. Genet. 2001, 39:388-393.