How does a hypha grow? the biophysics of pressurized growth in fungi

Nature Reviews Microbiology

Volumn 9, Issue 7, 2011, Pages 509-518

  Lew, Roger R ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MOLECULAR MOTOR;

CALCIUM TRANSPORT; CELL EXPANSION; CELL TURGOR; CYTOPLASM; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; GROWTH RATE; HYDRAULIC CONDUCTIVITY; HYPEROSMOTIC STRESS; MICROFLUIDIC ANALYSIS; NEUROSPORA CRASSA; NONHUMAN; OSMOTIC PRESSURE; PLASMOLYSIS; PRESSURE VOLUME CURVE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THERMODYNAMICS; TURGOR PRESSURE; WATER FLOW;

BIOPHYSICAL PHENOMENA; CYTOPLASM; FUNGI; HYPHAE; NEUROSPORA CRASSA; OSMOTIC PRESSURE;

FUNGI;

EID: 79959281015     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2591     Document Type: Review

References (116)

1. Trail, F. Fungal cannons: explosive spore discharge in the Ascomycota. FEMS Microbiol. Lett. 276, 12-18 (2007). (Pubitemid 47620454)
2. Yafetto, L. et al.The fastest flights in nature: high-speed spore discharge mechanisms among fungi. PLoS ONE 3, e3237 (2008).
3. Bastmeyer, T., Deising, H. B. & Bechinger, C. Force exertion in fungal infection. Annu. Rev. Biophys. Biomol. Struct. 31, 321-341 (2002). (Pubitemid 34666836)
4. Bartnicki-Garcia, S., Bracker, C. E., Gierz, G., Lopez- Franco, R. & Lu, H. Mapping the growth of fungal hyphae: orthogonal cell wall expansion during tip growth and the role of turgor. Biophys. J. 79, 2382-2390 (2000).
5. Shaw, S. L., Dumais, J. & Long, S. R. Cell surface expansion in polarly growing root hairs of Medicago truncatula. Plant Physiol. 124, 959-970 (2000).
6. Reinhardt M, O. Das Wachsthum der pilzhyphen. Jahrbücher für Wissenschaftliche Botanik 23, 479-566 (1892).
7. Money, N. P. in The Mycota. I. Growth, Differentiation and Sexuality (eds Wessels, J. G. H. & Meinhardt, F.) 67-88 (Springer, 1994).
8. Money, N. P. in The Mycota. VIII. Biology of the Fungal Cell 2nd edn (eds Howard, R. J. & Gow, N. A. R.) 237-249 (Springer, 2007).
9. Lew, R. R. & Nasserifar, S. Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa. Microbiology 155, 903-911 (2009).
10. Steudle, E., Zimmerman, U. & Lüttge, U. Effect of turgor pressure and cell size on the wall elasticity of plant cells. Plant Physiol. 59, 285-289 (1977).
11. Steudle, E. Zimmerman, U. & Zillikens, J. Effect of cell turgor on hydraulic conductivity and elastic modulus of Elodea leaf cells. Planta 154, 371-380 (1982).
12. Cosgrove, D. J. In defence of the cell volumetric elastic modulus. Plant Cell Environ. 11, 67-69 (1988).
13. Franks, P. J., Buckley, T. N., Shope, J. C. & Mott, K. A. Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol. 125, 1577-1584 (2001). (Pubitemid 32375742)
14. Ortega, J. K. E., Keanini, R. G. & Manica, K. J. Pressure probe technique to study transpiration in Phycomyces sporangiophore. Plant Physiol. 87, 11-14 (1988).
15. Agre, P. Aquaporin water channels. Nobelprize.org [online], http://nobelprize.org/nobel-prizes/chemistry/laureates/2003/agre-lecture.html (2003).
16. Tyerman, S. D., Bohnert, H. J., Maurel, C., Steudle, E. & Smith, J. A. C. Plant aquaporins: their molecular biology, biophysics and significance for water relations. J. Exp. Bot. 50, 1055-1071 (1999).
17. Tanghe, A., Van Dijck, P. & Thevelein, J. M. Why do microorganisms have aquaporins? Trends Microbiol. 14, 78-85 (2005). (Pubitemid 43190737)
18. Bartnicki-Garcia, S. Chitosomes: past, present and future. FEMS Yeast Res. 6, 957-965 (2006). (Pubitemid 44568852)
19. Money, N. P. & Harold, F. M. Extension growth of the water mold Achlya: interplay of turgor and wall strength. Proc. Natl Acad. Sci. USA 89, 4245-4249 (1992).
20. Lockhart, J. A. An analysis of irreversible plant cell elongation. J. Theor. Biol. 8, 264-275 (1965).
21. Green, P. B. Growth physics in Nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiol. 43, 1169-1184 (1968).
22. Zhu, G. L. & Boyer, J. S. Enlargement in Chara studies by a turgor clamp. Growth rate is not determined by turgor. Plant Physiol. 100, 2071-2080 (1992).
23. Proseus, T. E. & Boyer, J. S. Calcium pectate chemistry controls growth rate of Chara corallina. J. Exp. Bot. 57, 3989-4002 (2006). (Pubitemid 44950399)
24. Proseus, T. E. & Boyer, J. S. Tension required for pectate chemistry to control growth in Chara corallina. J. Exp. Bot. 58, 4283-4292 (2007). (Pubitemid 351323633)
25. Proseus, T. E. & Boyer, J. S. Calcium pectate chemistry causes growth to be stored in Chara corallina: a test of the pectate cycle. Plant Cell Environ. 31, 1147-1155 (2008). (Pubitemid 351962197)
26. Money, N. P. & Hill, T. W. Correlation between endoglucanase secretion and cell wall strength in oomycete hyphae: implications for growth and morphogenesis. Mycologia 89, 777-785 (1997). (Pubitemid 27442079)
27. Benkert, R., Obermeyer, G. & Bentrup, F.-W. The turgor pressure of growing lily pollen tubes. Protoplasma 198, 1-8 (1997). (Pubitemid 27320300)
28. Winship, L. J., Obermeyer, G., Geitmann, A. & Hepler, P. K. Under pressure, cell walls set the pace. Trends Plant Sci. 15, 363-369 (2010).
29. Zerzour, R., Kroeger, J. & Geitmann, A. Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev. Biol. 334, 437-446 (2009).
30. Levina N. N., Lew, R. R. & Heath, I. B. Cytoskeletal regulation of ion channel distribution in the tip-growing organism Saprolegnia ferax. J. Cell Sci. 107, 127-134 (1994). (Pubitemid 24039040)
31. Dutta R. & Robinson, K. R. Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol. 135, 1398-1406 (2004). (Pubitemid 39009387)
32. Lew, R. R. Comparative analysis of Ca2+ and H+ flux magnitude and location along growing hyphae of Saprolegnia ferax and Neurospora crassa. Eur. J. Cell Biol. 78, 892-902 (1999). (Pubitemid 30021270)
33. Lew, R. R. Mapping fungal ion channel distributions. Fungal Genet. Biol. 24, 69-76 (1998). (Pubitemid 28472939)
34. Levina, N. N., Lew, R. R., Hyde, G. J. & Heath, I. B. The roles of calcium ions and plasma membrane ion channels in hyphal tip growth of Neurospora crassa. J. Cell Sci. 108, 3405-3417 (1995).
35. Silverman-Gavrila L. B & Lew, R. R. Calcium and tip growth in Neurospora crassa. Protoplasma 213, 203-217 (2000).
36. Silverman-Gavrila L. B & Lew, R. R. Calcium gradient dependence of Neurospora crassa hyphal growth. Microbiology 149, 2475-2485 (2003). (Pubitemid 37160723)
37. Silverman-Gavrila L. B & Lew, R. R. Regulation of the tip-high [Ca2+] gradient in growing hyphae of the fungus Neurospora crassa. Eur. J. Cell Biol. 80, 379-390 (2001). (Pubitemid 32605781)
38. Silverman-Gavrila L. B & Lew, R. R. An IP3-activated Ca2+ channel regulates fungal tip growth. J. Cell Sci. 115, 5013-5025 (2002). (Pubitemid 36054651)
39. Levina N. N. & Lew, R. R. The role of tip-localized mitochondria in hyphal growth. Fungal Genet. Biol. 43, 65-74 (2006). (Pubitemid 43227992)
40. Bowman, B. J., Abreu, S., Margoles-Clark, E., Draskovic, M. & Bowman, E. J. Role of four calcium transport proteins, encoded by nca-1, nca-2, nca-3, and cax, in maintaining intracellular calcium levels in Neurospora crassa. Eukaryot. Cell 10, 654-661 (2011).
41. Verdín, J., Bartnicki-Garcia, S. & Riquelme, M. Functional stratification of the Spitzenkörper of Neurospora crassa. Mol. Microbiol. 74, 1044-1053 (2009).
42. Riquelme, M. et al. Spitzenkörper localization and intracellular traffic of green fluorescent protein-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot. Cell 6, 1853-1864 (2007). (Pubitemid 47585574)
43. Hilfiker, S., Greengard, P. & Augustine, G. J. Coupling calcium to SNARE-mediated synaptic vesicle fusion. Nature Neurosci. 2, 104-106 (1999). (Pubitemid 30491306)
44. Gupta, G. D. & Heath I. B. A tip-high gradient of a putative plasma membrane SNARE approximates the exocytotic gradient in hyphal apices of the fungus Neurospora crassa. Fungal Genet. Biol. 29, 187-199 (2000). (Pubitemid 30601395)
45. Gupta, G. D., Free, S. J., Levina, N. N., Keränen, S. & Heath, I. B. Two divergent plasma membrane syntaxin-like SNAREs, nsyn and nsyn2, contribute to hyphal tip growth and other developmental processes in Neurospora crassa. Fungal Genet. Biol. 40, 271-286 (2003). (Pubitemid 37346422)
46. Lew R. R., Levina, N. N., Walker, S. K. & Garrill A. Turgor regulation in hyphal organisms. Fungal Genet. Biol. 41, 1007-1015 (2004). (Pubitemid 39304097)
47. Lew R. R., Levina, N. N., Shabala, L., Anderca, M. I. & Shabala, S. N. Role of a mitogen-activated protein kinase cascade in ion flux-mediated turgor regulation in fungi. Eukaryot. Cell 5, 480-487 (2006).
48. Lew R. R. & Nasserifar, S. Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa. Microbiology 155, 903-911 (2009).
49. Lew, R. R. & Levina, N. N. Turgor regulation in the osmosensitive cut mutant of Neurospora crassa. Microbiology 153, 1530-1537 (2007). (Pubitemid 46780008)
50. Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E. & Gustin, M. C. An osmosensing signal transduction pathway in yeast. Science 259, 1760-1763 (1993). (Pubitemid 23114664)
51. Kranz, M., Becit, E. & Hoffmann, S. Comparative genomics of the HOG-signaling system in fungi. Curr. Genet. 49, 137-151 (2006).
52. Maeda, T., Takekawa, M. & Saito, H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3- containing osmosensor. Science 269, 554-558 (1995).
53. Posas F. & Saito, H. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276, 1702-1705 (1997).
54. Alex, L. A., Borkovich, K. A. & Simon, M. I. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc. Natl Acad. Sci. USA 93, 3416-3421 (1996). (Pubitemid 26125635)
55. Schumacher, M. M., Enderlin, C. S. & Selitrennikoff, C. P. The osmotic-1 locus of Neurospora crassa encodes a putative histidine kinase similar to osmosensors of bacteria and yeast. Curr. Microbiol. 34, 340-347 (1997). (Pubitemid 27224987)
56. Jones, C. A., Greer-Philips, S. E. & Borkovich, K. A. The response regulator RRG-1 functions upstream of a mitogen-activated protein kinase pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol. Biol. Cell 18, 2123-2136 (2007). (Pubitemid 46911364)
57. Ellis, S. W., Grindle, M. & Lewis, D. H. Effect of osmotic stress on yield and polyol content of dicoarboximide-sensitive and -resistant strains on Neurospora crassa. Mycol. Res. 95, 457-464 (1991).
58. Youssar, L. & Avalos, J. Genetic basis of the ovc phenotype of Neurospora: identification and analysis of a 77kb deletion. Curr. Genet. 51, 19-30 (2007). (Pubitemid 44873607)
59. Ochiai, N. et al. Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa. Pest Manag. Sci. 57, 437-442 (2001). (Pubitemid 32405599)
60. Motoyama, T. et al. An Os-1 family histidine kinase from a filamentous fungus confers fungicide-sensitivity to yeast. Curr. Genet. 47, 298-306 (2005). (Pubitemid 40723970)
61. Fujimura, M. et al. Sensitivity to phenylpyrrole fungicides and abnormal glycerol accumulation in Os and Cut mutant strains of Neurospora crassa. J. Pesticide Sci. 25, 31-36 (2000).
62. Lew, R. R. Turgor and net ion flux responses to activation of the osmotic MAP kinase cascade by fludioxonil in the filamentous fungus Neurospora crassa. Fungal Genet. Biol. 47, 721-726 (2010).
63. Colot, H. V. et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl Acad. Sci. USA. 103, 10352-10357 (2006). (Pubitemid 44051170)
64. Lew R. R., Abbas, Z., Anderca, M. I. & Free, S. J. Phenotype of a mechanosensitive channel mutant, mid-1, in a filamentous fungus, Neurospora crassa. Eukaryot. Cell 7, 647-655 (2008). (Pubitemid 351959899)
65. Lew R. R., Kapishon, V. Ptk2 contributes to osmoadaptation in the filamentous fungus Neurospora crassa. Fungal Genet. Biol. 46, 949-955 (2009).
66. Kaminskyj, S. G. W., Garrill, A. & Heath, I. B. The relation between turgor and tip growth in Saprolegnia ferax: turgor is necessary, but not sufficient to explain apical extension rates. Exp. Mycol. 16, 64-75 (1992).
67. Harold, R. L., Money, N. P. & Harold, F. M. Growth and morphogenesis in Saprolegnia ferax: is turgor required? Protoplasma 191, 105-114 (1996).
68. Walker, S. K., Chitcholtan, K., Yu, Y.-P., Christenhusz, G. M. & Garrill, A. Invasive hyphal growth: an F-actin depleted zone is associated with invasive hyphae of the oomycetes Achlya bisexualis and Phytophthora cinnamomi. Fungal Genet. Biol. 43, 357-365 (2006).
69. Emerson, S. Slime, a plasmodial variant of Neurospora crassa. Genetica 34, 162-182 (1963).
70. Perkins, D. D., Radford, A., Newmeyer, D. & Björkman M. Chromosomal loci of Neurospora crassa. Microbiol. Rev. 46, 426-570 (1982). (Pubitemid 13142787)
71. Leal-Morales, C. A. & Ruiz-Herrera, J. Alterations in the biosynthesis of chitin and glucan in the slime mutant of Neurospora crassa. Exp. Mycol. 9, 28-38 (1985). (Pubitemid 15140533)
72. Bartnicki-Garcia, S., Bracker, C. E., Lippman, E. & Ruiz-Herrera, J. Chitosomes from the wall-less "slime" mutant of Neurospora crassa. Arch. Microbiol. 139, 105-112 (1984). (Pubitemid 14044989)
73. Heath, I. B. & Steinberg. G. Mechanisms of hyphal tip growth: tube dwelling amebae revisited. Fungal Genet. Biol. 28, 79-93 (1999). (Pubitemid 30025756)
74. Lew, R. R. Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology 151, 2685-2692 (2005). (Pubitemid 41149790)
75. Robertson, N. F. & Rizvi, S. R. H. Some observations on the water-relations of the hyphae of Neurospora crassa. Ann. Bot. 32, 279-291 (1968).
76. Money, N. P. Measurement of hyphal turgor. Exp. Mycol. 14, 416-425 (1990).
77. Ng, S. K., Liu, F., Lai, J., Low, W. & Jedd. G. A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning. PLoS Genet. 6, e1000521 (2009).
78. Plamann, M. Cytoplasmic streaming in Neurospora: disperse the plug to increase the flow? PLoS Genet. 5, e1000526 (2009).
79. Heaton, K. L. M., López, E., Maini, P. K., Fricker, M. D. & Jones, N. S. Growth-induced mass flows in fungal networks. Proc. R. Soc. B 277, 3263-3274 (2010).
80. Sugden, K. E. P., Evans, M. R., Poon, W. C. K. & Read, N. D. Model of hyphal tip growth involving microtubule-based transport. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75, 031909 (2007).
81. Boudaoud, A. Growth of walled cells: from shells to vesicles. Phys. Rev. Lett. 91, 018104 (2003).
82. Freitag, M., Hickey, P. C., Raju, N. B., Selker, E. U. & Read, N. D. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41, 897-910 (2004). (Pubitemid 39165635)
83. Nelson, G. et al. Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol. Microbiol. 52, 1437-1450 (2004). (Pubitemid 38746316)
84. Hickey, P. C., Swift, S. M., Roca, M. G. & Read, N. D. Live-cell imaging of filamentous fungi using vital fluorescent dyes. Methods Microbiol. 34, 63-87 (2005). (Pubitemid 39752868)
85. Virag, A. & Griffiths, A. J. A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet. Biol. 41, 213-225 (2004). (Pubitemid 38058455)
86. Lee, I. H., Kumar, S. & Plamann, M. Null mutants of the Neurospora actin-related protein 1 pointed-end complex show distinct phenotypes. Mol. Biol. Cell 12, 2195-2206 (2001). (Pubitemid 33049709)
87. Riquelme M., Roberson, R. W., McDaniel, D. P. & Bartnicki-Garcia S. The effects of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa. Fungal Genet. Biol. 37, 171-179 (2002). (Pubitemid 35333773)
88. Mourino-Perez, R. R., Roberson, R. W. & Bartnicki-Garcia, S. Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet. Biol. 43, 389-400 (2006).
89. Ramos-Garcia, S. L., Roberson, R. W., Freitag, M., Bartnicki-Garcia, S. & Mourino-Perez, R. R. Cytoplasmic bulk flow propels nuclei in mature hyphae of Neurospora crassa. Eukaryot. Cell 8, 1880-1890 (2009).
90. Roca, M. G., Kuo, H.-C., Lichius, A., Freitag, M. & Read, N. D. Nuclear dynamics, mitosis, and the cytoskeleton during the early stages of colony initiation in Neurospora crassa. Eukaryot. Cell 9, 1171-1183 (2010).
91. Tucker, E. B. Cytoplasmic streaming does not drive intercellular passage in staminal hairs of Setcreasea purpurea. Protoplasma 137, 140-144 (1987).
92. Suei, S. & Garrill, A. An F-actin-depleted zone is present at the hyphal tip of invasive hyphae of Neurospora crassa. Protoplasma 232, 165-172 (2008).
93. Delgado-Álvarez, D. L. et al. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet. Biol. 47, 573-586 (2010).
94. Harris, S. D. et al. Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryot. Cell 4, 225-229 (2005). (Pubitemid 40257122)
95. Gow, N. A. R. Transhyphal electrical currents in fungi. J. Gen. Microbiol. 130, 3313-3318 (1984). (Pubitemid 15160215)
96. McGillviray, A. M. & Gow, N. A. R. The transhyphal electrical current of Neurospora crassa is carried principally by protons. J. Gen. Microbiol. 133, 2875-2881 (1987).
97. Takeuchi Y., Schmid, J., Caldwell, J. H. & Harold, F. M. Transcellular ion currents and extension of Neurospors crassa hyphae. J. Membr. Biol. 101, 33-41 (1988). (Pubitemid 18050653)
98. McGillviray, A. M. & Gow, N. A. R. Applied electrical fields polarize the growth of mycelial fungi. J. Gen. Microbiol. 132, 2515-2525 (1986). (Pubitemid 16019589)
99. Lever, M. C. et al. pH and Ca2+ dependent galvanotropism of filamentous fungi: implications and mechanisms. Mycol. Res. 98, 301-306 (1994). (Pubitemid 2070589)
100. Burstaller, W. Transport of small ions and molecules through the plasma membrane of filamentous fungi. Curr. Rev. Microbiol. 23, 1-46 (1997).
101. Riquelme, M., Freitag, M., León-Hing, E. S. & Bowman, B. Live imaging of the secretory pathway in hyphae of Neurospora crassa. Fungal Genet. Newsl. 52 (Suppl.), 53 (2005).
102. Slayman, C. L. & Slaymen, C. W. Measurement of membrane potentials in Neurospora. Science 136, 876-877 (1962).
103. Potapova, T. V., Aslanidi, K. B., Belozerskaya, T. A. & Levina, N. N. Transcellular ionic currents studied by intracellular potential recordings in Neurospora crassa hyphae. Transfer of energy from proximal to apical cells. FEBS Lett. 241, 173-176 (1988).
104. Zalokar, M. Growth and differentiation of Neurospora crassa. Am. J. Bot. 46, 602-610 (1959).
105. Brody, J. P., Yager, P., Goldstein, R. E. & Austin, R. H. Biotechnology at low Reynolds number. Biophys. J. 71, 3430-3441 (1996).
106. Berg, H. C. & Purcell, E. M. Physics of chemoreception. Biophys. J. 20, 193-219 (1977). (Pubitemid 8220672)
107. Short, M. B. et al. Flows driven by flagella of multicellular organisms enhance long-range molecular transport. Proc. Natl Acad. Sci. USA 103, 8315-8319 (2006). (Pubitemid 43838452)
108. Goldstein, R. E., Tuval, I. & van de Meent, J.-W. Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc. Natl Acad. Sci. USA 105, 3663-3667 (2008). (Pubitemid 351723454)
109. Van de Meent, J.-W., Tuval, I. & Goldstein, R. E. Nature's microfluidic transporter: rotational cytoplasmic streaming at high Péclet numbers. Phys. Rev. Lett. 101, 178102 (2008).
110. Cosgrove, D. J. Analysis of the dynamic and steady-state responses of growth rate and turgor pressure to changes in cell parameters. Plant Physiol. 68, 1439-1446 (1981).
111. Bok, J. W. et al. Structure and function analysis of the calcium-related gene spray in Neurospora crassa. Fungal Genet. Biol. 32, 145-158 (2001).
112. Sanders, D., Slayman, C. L. & Pall, M. L. Stoichiometry of H+/amino acid cotransport in Neurospora crassa revealed by current-voltage analysis. Biochim. Biophys. Acta 735, 67-76 (1983).
113. Schloemer, R. H. & Garrett, R. H. Nitrate transport system in Neuropora crassa. J. Bacteriol. 118, 259-269 (1974).
114. Blatt, M. R., Maurousset, L. & Meharg, A. A. High-affinity NO3-H+ cotransport in the fungus Neurospora: induction and control by pH and membrane voltage. J. Membr. Biol. 160, 59-76 (1997). (Pubitemid 27491722)
115. Versaw, W. K. & Metzenberg, R. L. Repressible cation-phosphate symporter in Neurospora crassa. Proc. Natl Acad. Sci. USA 92, 3884-3887 (1995).
116. Slayman, C. L. & Slayman, C. W. Depolarization of the plasma membrane of Neurospora during active transport of glucose: evidence for a proton-dependent cotransport system. Proc. Natl Acad. Sci. USA 71, 1935-1939 (1974).