Fluorescent markers of the microtubule cytoskeleton in Zymoseptoria tritici

Fungal Genetics and Biology

Volumn 79, Issue , 2015, Pages 141-149

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

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Microtubules; Mitosis; Mycosphaerella graminicola; Septoria tritici blotch; Wheat pathogenic fungi

Indexed keywords

ALPHA TUBULIN; ENHANCED GREEN FLUORESCENT PROTEIN; FUNGAL PROTEIN; GAMMA TUBULIN; MICROTUBULE ASSOCIATED PROTEIN; PEB1 PROTEIN; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; FUNGAL CELL; FUNGAL PLANT DISEASE; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS IDENTIFICATION; IN VIVO STUDY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEPTORIA TRITICI BLOTCH; WHEAT; ZYMOSEPTORIA TRITICI; ASCOMYCETES; CHEMISTRY; FLUORESCENCE IMAGING; GENETICS; PROCEDURES; REPORTER GENE; STAINING;

FUNGI; MAMMALIA; MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

ASCOMYCOTA; CYTOSKELETAL PROTEINS; GENES, REPORTER; LUMINESCENT PROTEINS; MICROTUBULES; OPTICAL IMAGING; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING;

EID: 84937554633     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2015.03.005     Document Type: Article

References (62)

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. 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.
3. Bowler J., Scott E., Tailor R., Scalliet G., Ray J., Csukai M. New capabilities for Mycosphaerella graminicola research. Mol. Plant Pathol. 2010, 11:691-704.
4. Boyle J.S., Lew A.M. An inexpensive alternative to glassmilk for DNA purification. Trends Genet. 1995, 11:8.
5. Clemons G.P., Sisler H.D. Localization of the site of action of a fungitoxic benomyl derivative. Pestic. Biochem. Physiol. 1971, 1:32-43.
6. Desai A., Mitchison T.J. Microtubule polymerization dynamics. Ann. Rev. Cell Dev. Biol. 1997, 13:83-117.
7. Drummond D.R., Cross R.A. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr. Biol. 2000, 10:766-775.
8. Egan M.J., McClintock M.A., Reck-Peterson S.L. Microtubule-based transport in filamentous fungi. Curr. Opin. Microbiol. 2012, 15:637-645.
9. Fink G., Steinberg G. Dynein-dependent motility of microtubules and nucleation sites supports polarization of the tubulin array in the fungus Ustilago maydis. Mol. Biol. Cell 2006, 17:3242-3253.
10. Fink, G., Schuchardt, I., Colombelli, J., Stelzer, E., Steinberg, G., 2006. Dynein-mediated pulling forces drive rapid mitotic spindle elongation in Ustilago maydis. EMBO J.25, pp. 4897-4908.
11. Fuchs U., Manns I., Steinberg G. Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol. Biol. Cell 2005, 16:2746-2758.
12. 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.
13. Higuchi Y., Ashwin P., Roger Y., Steinberg G. Early endosome motility spatially organizes polysome distribution. J. Cell Biol. 2014, 204:343-357.
14. Hirokawa N., Takemura R. Molecular motors in neuronal development, intracellular transport and diseases. Curr. Opin. Neurobiol. 2004, 14:564-573.
15. Hoffman C.S., Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 1987, 57:267-272.
16. Holloman, D.W., Butters, J.A., Barker, H., 1997. Tubulins, a target for anti-fungal agents., London, United Kingdom, Royal Society of Chemistry.
17. 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.
18. Hood E., Gelvin S.B., Melchers L., Hoekema A. New Agrobacterium helper plasmids for gene transter to plants. Transgen. Res. 1993, 2:208-218.
19. Horio T., Oakley B.R. The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol. Biol. Cell 2005, 16:918-926.
20. Horio T., Uzawa S., Jung M.K., Oakley B.R., Tanaka K., Yanagida M. The fission yeast γ-tubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci. 1991, 99:693-700.
21. Job D., Valiron O., Oakley B. Microtubule nucleation. Curr. Opin. Cell Biol. 2003, 15:111-117.
22. Jung M.K., May G.S., Oakley B.R. Mitosis in wild-type and β-tubulin mutant strains of Aspergillus nidulans. Fungal Genet. Biol. 1998, 24:146-160.
23. 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.
24. Kilaru, S., Steinberg, G., 2015. Yeast recombination-based cloning as an efficient way of constructing vectors for Zymoseptoria tritici. Fungal Genet. Biol 79, 76-83.
25. Kilaru, S., Schuster, M., Latz, M., Das Gupta, S., Steinberg, N., Fones, H., Gurr S., Talbot, N.J., Steinberg, G., 2015a. A gene locus for targeted ectopic gene integration in Zymoseptoria tritici. Fungal Genet. Biol 79, 118-124.
26. Kilaru, S., Schuster, M., Latz, M., Guo, M., Steinberg, G., 2015b. Fluorescent markers of the endocytic pathway in Zymoseptoria tritici. Fungal Genet. Biol 79, 150-157.
27. Knop M., Schiebel E. Spc98p and Spc97p of the yeast γ-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J. 1997, 16:6985-6995.
28. Konzack S., Rischitor P.E., Enke C., Fischer R. The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans. Mol. Biol. Cell 2005, 16:497-506.
29. 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.
30. Martin M.A., Osmani S.A., Oakley B.R. The role of γ-tubulin in mitotic spindle formation and cell cycle progression in Aspergillus nidulans. J. Cell Sci. 1997, 110:623-633. Pt. 5.
31. Moritz M., Braunfeld M.B., Sedat J.W., Alberts B., Agard D.A. Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 1995, 378:638-640.
32. Oakley C.E., Oakley B.R. Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 1989, 338:662-664.
33. Oakley B.R., Oakley C.E., Yoon Y., Jung M.K. Γ-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 1990, 61:1289-1301.
34. 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.
35. RAB11 exocytic post-Golgi carriers visualized in vivo. Mol. Biol. Cell 2014, 25:2428-2443.
36. Prigozhina N.L., Walker R.A., Oakley C.E., Oakley B.R. Γ-tubulin and the C-terminal motor domain kinesin-like protein, KLPA, function in the establishment of spindle bipolarity in Aspergillus nidulans. Mol. Biol. Cell 2001, 12:3161-3174.
37. Raymond C.K., Pownder T.A., Sexson S.L. General method for plasmid construction using homologous recombination. BioTechniques 1999, 26:134-141.
38. Riehlman T.D., Olmsted Z.T., Branca C.N., Winnie A.M., Seo L., Cruz L.O., Paluh J.L. Functional replacement of fission yeast γ-tubulin small complex proteins Alp4 and Alp6 by human GCP2 and GCP3. J. Cell Sci. 2013, 126:4406-4413.
39. Rohel E.A., Payne A.C., Hall L., Barker H., Butters J., Hollomon D.W. Isolation and characterization of α-tubulin genes from Septoria tritici and Rhynchosporium secalis, and comparative analyzis of fungal α-tubulin sequences. Cell Motil. Cytoskeleton 1998, 41:247-253.
40. Sambrook J., Russell D.W. Molecular cloning 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
41. Schuchardt I., Assmann D., Thines E., Schuberth C., Steinberg G. Myosin-V, kinesin-1, and kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol. Biol. Cell 2005, 16:5191-5201.
42. Schuster M., Kilaru S., Fink G., Collemare J., Roger Y., Steinberg G. Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array. Mol. Biol. Cell 2011, 22:3645-3657.
43. Schuster M., Treitschke S., Kilaru S., Molloy J., Harmer N.J., Steinberg G. Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J. 2012, 31:214-227.
44. 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.
45. Sims J.J., Mee H., Erwin D.C. Methyl 2-benzimidazolecarbamate, a fungitoxic compound isolated from cotton plants treated with methyl 1-(butylearbamoyl,-2-benzimidazolecarbamate, benomyl. Phytopathology 1969, 59:1775-1776.
46. Steinberg G. Endocytosis and early endosome motility in filamentous fungi. Curr. Opin. Microbiol. 2014, 20:10-18.
47. Steinberg G., Wedlich-Söldner R., Brill M., Schulz I. Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci. 2001, 114:609-622.
48. Straube A., Brill M., Oakley B.R., Horio T., Steinberg G. Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites, polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol. Biol. Cell 2003, 14:642-657.
49. Su W.Q., Li S.H., Oakley B.R., Xiang X. Dual-color Imaging of nuclear division and mitotic spindle elongation in live cells of Aspergillus nidulans. Eukaryot Cell 2004, 3:553-556.
50. Szewczyk E., Oakley B.R. Microtubule dynamics in mitosis in Aspergillus nidulans. Fungal Genet. Biol. 2011, 48:998-999.
51. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5, molecular evolutionary genetics analyzis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
52. 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.
53. Teixido-Travesa N., Roig J., Lüders J. The where, when and how of microtubule nucleation - one ring to rule them all. J. Cell Sci. 2012, 125:4445-4456.
54. Toya M., Sato M., Haselmann U., Asakawa K., Brunner D., Antony C., Toda T. Γ-tubulin complex-mediated anchoring of spindle microtubules to spindle-pole bodies requires Msd1 in fission yeast. Nat. Cell Biol. 2007, 9:646-653.
55. Vale R.D. The molecular motor toolbox for intracellular transport. Cell 2003, 112:467-480.
56. Vardy L., Toda T. The fission yeast γ-tubulin complex is required in G(1, phase and is a component of the spindle assembly checkpoint. EMBO J. 2000, 19:6098-6111.
57. 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.
58. 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.
59. Wiese C., Zheng Y. Microtubule nucleation, γ-tubulin and beyond. J. Cell Sci. 2006, 119:4143-4153.
60. Xiang X., Plamann M. Cytoskeleton and motor proteins in filamentous fungi. Curr. Opin. Microbiol. 2003, 6:628-633.
61. Zheng Y., Jung M.K., Oakley B.R. Γ-tubulin is present in Drosophila melanogaster and Homo sapiens and is associated with the centrosome. Cell 1991, 65:817-823.
62. Zwiers L.H., De Waard M.A. Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr. Genet. 2001, 39:388-393.