Mechanisms of hypha orientation of fungi

Current Opinion in Microbiology

Volumn 12, Issue 4, 2009, Pages 350-357

  Brand, Alexandra ^a   Gow, Neil AR ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; KINESIN;

ASPERGILLUS NIDULANS; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANDIDA ALBICANS; CYTOSKELETON; ENDOPHYTE; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; MICROTUBULE; MORPHOGENESIS; MUTATIONAL ANALYSIS; MYCELIAL GROWTH; NONHUMAN; REVIEW; SAPROTROPH;

ENVIRONMENT; FUNGI; HYPHAE; MODELS, BIOLOGICAL; STRESS, PHYSIOLOGICAL;

FUNGI;

EID: 68049137459     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2009.05.007     Document Type: Review

References (56)

1. Gow N.A., Brown A.J., and Odds F.C. Fungal morphogenesis and host invasion. Curr Opin Microbiol 5 (2002) 366-371
2. Virag A., and Harris S.D. The Spitzenkörper: a molecular perspective. Mycol Res 110 (2006) 4-13. An excellent overview of the process of hyphal tip growth covering the main protein molecular complexes that are required for polarised tip growth.
3. Steinberg G. Hyphal growth: a tale of motors, lipids, and the Spitzenkörper. Eukaryot Cell 6 (2007) 351-360
4. Machesky L.M., and Gould K.L. The Arp2/3 complex: a multifunctional actin organizer. Curr Opin Cell Biol 11 (1999) 117-121
5. Lipschutz J., and Mostov K. Exocytosis: the many masters of the exocyst. Curr Biol 1 (2002) 212-214
6. Sudbery P., and Court H. Polarised growth in fungi. In: Howard R.J., and Gow N.A.R. (Eds). The Mycota VIII. edn 2 (2007), Springer-Verlag 137-166
7. Martin S.W., and Konopka J.B. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 3 (2004) 675-684. Here the authors show the apical distribution of sterol-rich membranes in the germ tubes of C. albicans and that pharmacological disruption of sphingolipid or sterol biosynthesis caused abnormal hyphal development.
8. Pearson C.L., Xu K., Sharpless K.E., and Harris S.D. MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans. Mol Biol Cell 15 (2004) 3658-3672
9. Alvarez J.F., Douglas L.M., and Konopka J. Sterol-rich plasma membrane domains in fungi. Eukaryot Cell 6 (2007) 755-763
10. Irazoqui J.E., Gladfelter A.S., and Lew D.J. Cdc42p, GTP hydrolysis, and the cell's sense of direction. Cell Cycle 3 (2004) 861-864
11. Harris S.D., Read N.D., Roberson R.W., Shaw B., Seiler S., Plamann M., and Momany M. Polarisome meets Spitzenkörper: microscopy, genetics and genomics coverage. Eukaryot Cell 4 (2005) 225-229
12. Steinberg G. On the move: endosomes in fungal growth and pathogenicity. Nat Rev Microbiol 5 (2007) 309-316
13. Fischer R., Zekert N., and Takeshita N. Polarized growth in fungi - interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68 (2008) 813-826. This is an excellent review of polarised growth in fungi, with particular emphasis on hyphal growth in Aspergillus.
14. Roca M.G., Artl J., Jeffree C.E., and Read N.D. Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4 (2005) 911-919
15. Roca M.G., Read N.D., and Wheals A.E. The conidial anastomosis tubes in filamentous fungi. FEMS Microbiol Lett 249 (2005) 191-198
16. Gooday G.W., and Adams D.J. Sex hormones and fungi. Adv Microb Physiol 34 (1993) 69-145
17. Daniels K.J., Srikantha T., Lockhart S.R., Pujol C., and Soll D.R. Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J 25 (2006) 2240-2252
18. Gooday G.W. Chemotaxis and chemotropism in fungi and algae. In: Carlile M.J. (Ed). Primitive Sensory and Communication Systems (1975), Academic Press 155-204
19. Jansson H.-B., Johansson T., Nordbring-Herts B., Tunlid A., and Odham G. Chemotropic growth of germ tubes of Cochliobolus sativus to barley roots or root exudates. Trans Br Mycol Soc 90 (1988) 647-650
20. De Silva L., Youatt J., Gooday G.W., and Gow N.A.R. Inwardly directed ionic currents of Allomyces macrogynus and other water moulds indicate sites of proton-driven nutrient transport but are incidental to tip growth. Mycol Res 96 (1992) 925-931
21. Christensen M.J., Bennett R.J., Ansari H.A., Koga H., Johnson R.D., Bryan G.T., Simpson W.R., Koolaard J.P., Nickless E.M., and Voisey C.R. Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45 (2008) 84-93. In this paper the authors demonstrate that plant epiphytes have to undergo intercalary growth in order to be able to be maintained within the growing meristematic regions of plants. This paper therefore points to a notable departure from the dogma of apical hyphal growth in fungi.
22. Rolke Y., and Tudzynski P. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol Microbiol 68 (2008) 405-423
23. Allen E.A., Hoch H.C., Stavely J.R., and Steadman J.R. Uniformity among races of Uromyces appendiculatus in response to topographical signalling for appressorium formation. Phytopathology 81 (1991) 883-887
24. Collins T.J., and Read N.D. Appressorium induction by topographical signals from six cereal rusts. Physiol Mol Plant Pathol 51 (1997) 169-179
25. Gow N.A.R. Nonchemical signals used for host location and invasion by fungal pathogens. Trends Microbiol 1 (1993) 45-50
26. Zhou X.-L., Stumpf M.A., Hoch H.C., and Kung C. A mechanosensitive channel in whole cells and membrane patches of the fungus Uromyces. Science 253 (1991) 1415-1417
27. Aoki A., Ito-Kuwa S., Nakamura K., Vidotta V., and Takeo K. Oxygen as a possible tropic factor in hyphal growth of Candida albicans. Mycoscience 39 (1998) 231-238
28. Davies J.M., Stacey A.J., and Gilligan C.A. Candida albicans hyphal invasion: thigmotropism or chemotropism?. FEMS Microbiol Lett 171 (1999) 245-249
29. Brand A., Vacharaksa A., Bendel C., Norton J., Haynes P., Henry-Stanley M., Wells C., Ross K., Gow N.A.R., and Gale C.A. An internal polarity landmark is important for externally induced hyphal behaviors in Candida albicans. Eukaryot Cell 7 (2008) 712-720. The authors show evidence for the internal polarity landmark proteins - the Bud1/Rsr1 Ras-GTPase and its GAP, Bud2, are required for the normal thigmotropic and galvanotropic orientation of germ tubes of C. albicans. It is also shown that mutants lacking these proteins are less able to penetrate into oral epithelial cells and kidneys of experimental animals.
30. Sherwood J., Gow N.A.R., Gooday G.W., Gregory D., and Marshall D. Contact sensing in Candida albicans: a possible aid to epithelial penetration. J Med Vet Mycol 30 (1992) 461-469
31. Perera T.H.S., Gregory D.W., Marshall D., and Gow N.A.R. Contact sensing in hyphae of dermatophytic and saprophytic fungi. J Med Vet Mycol 35 (1997) 289-294
32. Brand A., Shanks S., Duncan V.M.S., Yang M., Mackenzie K., and Gow N.A.R. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17 (2007) 347-352. Using a range of mutants in calcium transport systems this article shows that galvanotropism and thigmotropism of C. albicans requires the high and low affinity uptake mechanisms and components of the underlying calcium-signalling pathways.
33. Brasch J., and Menz A. UV susceptibility and negative phototropism of dermatophytes. Mycoses 38 (1995) 197-203
34. Hutton R.D., Kerbs S., and Yee K. Scanning electron microscopy of experimental Trichophyton mentagrophytes infections in guinea pig skin. Infect Immun 21 (1978) 247-253
35. Sherwood-Higham J., Zhu W.-Y., Devine C.A., Gooday G.W., Gow N.A.R., and Gregory D.W. Helical growth of Candida albicans. J Med Vet Mycol 32 (1995) 437-445
36. Brand A., Lee K., Veses V., and Gow N.A.R. Calcium homeostasis is required for contact-dependent helical and sinusoidal tip growth in Candida albicans hyphae. Mol Microbiol 71 (2009) 1155-1164
37. Crombie T., Gow N.A.R., and Gooday G. Influence of applied electrical fields on yeast and hyphal growth of Candida albicans. J Gen Microbiol 136 (1990) 311-317
38. Casamayor A., and Snyder M. Bud-site selection and cell polarity in budding yeast. Curr Opin Microbiol 5 (2002) 179-186
39. Herrero A.B., López M.C., Fernández-Lago L., and Domínguez A. Candida albicans and Yarrowia lipolytica as alternative models for analysing pudding patterns and germ tube formation in dimorphic fungi. Microbiology 145 (1999) 2727-2737
40. Chaffin W.L. Site selection for bud and germ tube emergence in Candida albicans. J Gen Microbiol 130 (1984) 431-440
41. Kumamoto C., and Vinces M.D. Alternative Candida albicans lifestyles: growth on surfaces. Annu Rev Microbiol 59 (2005) 113-133. Excellent supplementary information looking specifically at the role of mechanosensitive phenomena in fungal physiology, including aspects not covered in the present review on cell wall stress regulation and the electrophysiology of mechanosensitive ion channels.
42. McGillivray A.M., and Gow N.A.R. Applied electrical fields polarize the growth of mycelial fungi. J Gen Microbiol 132 (1986) 2515-2525
43. Pu R., and Robinson K.R. Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid algs Pelvetia compressa. J Cell Sci 111 (1998) 3197-3207
44. 2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136 (2004) 3562-3571
45. 2+ dependent galvanotropism of filamentous fungi: implications and mechanisms. Mycol Res 98 (1994) 301-306
46. Kumamoto C. Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat Rev Microbiol 6 (2008) 667-673
47. Watts H.J., Véry A.-A., Perera T.H.S., Davies J.M., and Gow N.A.R. Thigmotropism and stretch-activated channels in the pathogenic fungus Candida albicans. Microbiology 144 (1998) 689-695
48. Bowen A.D., Davidson F.A., Keatch R., and Gadd G.M. Induction of contour sensing in Aspergillus niger by stress and its relevance to fungal growth mechanics and hyphal tip structure. Fungal Genet Biol 44 (2007) 484-491
49. Read N.D., Kellock L.K., Knight H., and Trewavas A.J. Contact sensing during infection by fungal pathogens. In: Callow J.A., and Green J.R. (Eds). Perspectives in Plant Cell Recognition 48 (1992), Cambridge University Press 137-172
50. Hausauer D.L., Gerami-Nejad M., Kistler-Anderson C., and Gale C.A. Hyphal guidance and invasive growth in Candida albicans require the Ras-like GTPase Rsr1p and its GTPase-activating protein Bud2p. Eukaryot Cell 4 (2005) 1273-1286
51. Steinberg G. Tracks for traffic: microtubules in the plant pathogen Ustilago maydis. New Phytol 174 (2007) 721-733
52. Takeshita N., Higashitsuji Y., Konzack S., and Fischer R. Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19 (2008) 339-351. The authors characterise the roles of two cell-end marker proteins, TeaA and TeaR, and the CENP-E kinesin KipA in hyphal orientation and in microtubule architecture. The Tea mutants have meandering or zig-zag hyphae. KipA is shown to be important for the localisation of TeaA and TeaR, but not for their cytoplasmic transport. In addition they present evidence that the sterol-rich apical membrane domain is vital for the localisation of the Tea proteins and for hyphal polarity.
53. Higashitsuji Y, Herrero S, Takeshita N, Fischer R: The cell end marker protein TeaC determines growth directionality and is involved in cell septation in Aspergillus nidulans. Eukaryot Cell 2009, doi:10.1128/EC.00251-08, in press.
54. Wu Q., Sandrock T.M., Turgeon B.G., Yoder O.C., Wirsel S.G., and Aist J.R. A fungal kinesin required for organelle motility, hyphal growth, and morphogenesis. Mol Biol Cell 9 (1998) 89-101
55. Konzack S., Rischitor P.E., Enke C., and Fischer R. The role of the kinesin motor KipA in microtubule organization and polarised growth of Aspergillus nidulans. Mol Biol Cell 16 (2005) 497-506
56. Côte P., and Whiteway M. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol Microbiol 68 (2008) 392-404