Chapter 22 : Thigmo Responses: The Fungal Sense of Touch

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Thigmo Responses: The Fungal Sense of Touch, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap22-1.gif /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap22-2.gif


The growth and development phases of most fungi take place on a two-dimensional surface or within a three-dimensional matrix. The fungal sense of touch is therefore critical for fungi in the interpretation of their environment and is often involved in the switch to a new developmental state. Contact sensing, or thigmo-based responses, include thigmo differentiation, such as the development of invasion structures by plant pathogens; thigmonasty, where contact with a motile prey rapidly triggers its capture; and thigmotropism, where hyphal growth direction is guided by physical features in the environment. Like plants and some bacteria, fungi grow as walled cells. How do fungi, as walled organisms, not only sense contact, but also interpret the signal in a developmental context?

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Thigmo responses play crucial roles in the fungal lifestyle. Thigmonasty: On sensing exudate from nearby nematode prey, hyphae produce a lateral peg and three consecutive capture cells that grow round until they contact the peg, with which they fuse to form a capture loop ( ) (reprinted from taxusbaccata.hubpages.com with permission of the author). Contact with a nematode entering the aperture of the loop causes immediate swelling of the capture cells to immobilize the prey (reprinted from apsnet.org with permission of the author). Invasive hyphae then germinate from the contact zone of the capture cells to penetrate and digest the nematode. Thigmotropism: Hyphae of the sooty blotch fungus, , follow interepidermal cell depressions on the surface of the host plant, (white clover), to locate a stoma, over which a penetrative appressorium is formed (arrow) (bar, 10 μm) (reprinted from [ ] with permission of the publisher). Germ tubes of the cereal rust fungus, , grow perpendicularly across depressions in the surface of its host barley leaf to locate stomata, which are arranged in staggered arrays, and form appressoria (G, germ tube; A, appressorium; B, branch; bar, 20 μm) (reprinted from [ ] with permission of the publisher). Thigmo differentiation: the differentiation of appressoria by is induced by topography alone when the fungus is grown on an inert polymer with topographical features that precisely mimic the surface of the host plant (bar, 11.8 μm) (reprinted from [ ] with permission of the publisher).

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Contact sensing stands at the threshold of a diverse range of morphological and growth transitions relevant to specific fungal lifestyles. Most transitions require a supporting chemical signal for complete induction of a normal response while, in others, this aspect has not been fully investigated.

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Mechanisms involved in fungal contact resulting in recognition and/or adhesion. Compatible surface chemistry between fungal and substrate surface promotes adhesion. Directional forces generate cell wall stress. Chemical changes sensed within the boundary layer, sometimes as a result of fungal enzyme activity against host exudate. Contact-activated zone defines spatial organization of cell asymmetry. Stretch-activated ion channels. Plasma membrane (PM)-associated cell wall perturbation sensors coupled to intracellular signaling pathways. Sensors of cell wall perturbation. Cytoskeleton-coupled transmembrane proteins.

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Tight contact between fungus and host during fungal mutualism. Host-plant cell growth is thought to be sensed by the endophyte, , through its strong adhesion to the host intercellular matrix (H, hypha; bar, 1 μm) (reprinted from gy [ ] with permission of the publisher). The sense of stretch induces intercalary growth of the endophyte, , so that it elongates at the same rate as the host. Arrows indicate the lateral branches that have moved further apart as a result of intercalary growth (bar, 100 μm) (reprinted from [ ] with permission of the publisher). Arbuscular mycorrhizae form intruding hyphal arbuscules within the root cells of . Host GFP-Mtcp1 localizes to the cell plasma membrane and its derivative that surrounds the arbuscule trunk, but is not expressed in host membrane surrounding arbuscule branches (arrows), which is thought to be involved in nutrient exchange (a, arbuscules; t, arbuscule trunk; ih, intracellular hyphae; n, nucleus; bar, 20 μm) (reprinted from [ ] with permission of the publisher). ectomycorrhizae, labeled with wheat germ agglutininfluorescein isothiocyanate, grow as a dense outer fungal sheath or mantle surrounding the “Hartig net” (arrows) of hyphae growing between outer cortical cells of hazelnut, (m, fungal mantle; bar, 15 μm) (reprinted from [ ] with permission of the publisher). forms a fungal sheath surrounding the Hartig net (arrows) of hyphae that intercalate between the cortical root cells of (CC, cortical cells; black asterisk, fungal sheath; bar, 10 μm) (reprinted from [ ] with permission of the publisher).

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Cell-cell contact marks the developmental tipping point between “homing” and fusion. Healing process between the ends of a severed hypha in mycelia of the arbuscular mycorrhiza, . Severed hyphal compartments (open arrows) are sealed off by the formation of new septa. New hyphae emerge from behind the septa and grow chemotropically toward each other (closed arrows). Hyphal wall contact and fusion (open arrows) permits cytoplasmic flow to be reestablished (open arrowhead). (Bars, 80 μm) (reprinted from [ ] with permission of the publisher). Mating cells of yeast , where the shmoos of two wild-type cells expressing soluble GFP have fused by degrading the cell wall and fusing the plasma membrane. A daughter cell has emerged (top). In the Δ null mutant, which lacks a multispanning transmembrane protein, shmoo-shmoo contact triggered cell wall degradation but not membrane fusion, stalling the mating process (reprinted from the [ ] with permission of the publisher). Conidial anastomosis tubes (CATs) emerge from conidia of and “home” toward each other (c, conidia; gt, germ tube; bar, 6 μm). CATs emerge from germ tubes prior to contact and fusion (bar, 5 μm) (reprinted from [ ] with permission of the publisher).

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Contact-induced hyphal tip responses in ( ). Tip and Spitzenkörper asymmetry induced by contact of a hyphal tip with an obstacle in control cells expressing Mlc1-YFP (bar, 2 μm). Hyphae exhibit contour following, gap penetration, and trajectory maintenance. (B, C, bars, 2 μm; D, bar, 10 μm). In hyphae of the Δ mutant, the Spitzenkörper tends to be centrally positioned with the apex, hyphal tips do not become asymmetrical on contact or respond normally to substrate topography by following contours or penetrating gaps (bars, 2 μm) (reprinted from [ ] with permission of the publisher).

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7
Figure 7

Sensing and signaling pathways that have the potential to be involved in mechanosensing in fungi. For details and references, see the text. PM, plasma membrane.

Citation: Almeida M, Brand A. 2017. Thigmo Responses: The Fungal Sense of Touch, p 487-507. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0040-2016
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Drechsler C . 1937. Some hyphomycetes that prey on free-living terricolous nematodes. Mycologia 29 : 447552.[CrossRef]
2. Muller HG . 1958. The constricting ring mechanism of two predacious hyphomycetes. Trans Br Mycol Soc 41 : 341364.[CrossRef]
3. Hoch HC,, Staples RC,, Whitehead B,, Comeau J,, Wolf ED . 1987. Signaling for growth orientation and cell differentiation by surface topography in Uromyces . Science 235 : 16591662.[CrossRef] [PubMed]
4. Kwon YH,, Hoch HC . 1991. Temporal and spatial dynamics of appressorium formation in Uromyces appendiculatus . Exp Mycol 15 : 116131.[CrossRef]
5. Yaar L,, Mevarech M,, Koltin Y . 1997. A Candida albicans RAS-related gene (CaRSR1) is involved in budding, cell morphogenesis and hypha development. Microbiology 143 : 30333044.[CrossRef] [PubMed]
6. Brand A,, Vacharaksa A,, Bendel C,, Norton J,, Haynes P,, Henry-Stanley M,, Wells C,, Ross K,, Gow NAR,, Gale CA . 2008. An internal polarity landmark is important for externally induced hyphal behaviors in Candida albicans . Eukaryot Cell 7 : 712720.[CrossRef]
7. Thomson DD,, Wehmeier S,, Byfield FJ,, Janmey PA,, Caballero-Lima D,, Crossley A,, Brand AC . 2015. Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae. Cell Microbiol 17 : 342354.[CrossRef]
8. Hawksworth DL . 2012. Global species numbers of fungi: are tropical studies and molecular approaches contributing to a more robust estimate? Biodivers Conserv 21 : 24252433.[CrossRef]
9. Talbot NJ,, Kershaw MJ,, Wakley GE,, De Vries O,, Wessels J,, Hamer JE . 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Maganaporthe grisea . Plant Cell 8 : 985999.[CrossRef]
10. Wösten HA,, Schuren FH,, Wessels JG . 1994. Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13 : 58485854.[PubMed]
11. Grünbacher A,, Throm T,, Seidel C,, Gutt B,, Röhrig J,, Strunk T,, Vincze P,, Walheim S,, Schimmel T,, Wenzel W,, Fischer R . 2014. Six hydrophobins are involved in hydrophobin rodlet formation in Aspergillus nidulans and contribute to hydrophobicity of the spore surface. PLoS One 9 : e94546.[CrossRef]
12. Boucias DG,, Pendland JC,, Latge JP . 1988. Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol 54 : 17951805.[PubMed]
13. Wessels JGH, . 1996. Hydrophobins: proteins that change the nature of the fungal surface, p 145. In Poole RK (ed), Advances in Microbial Physiology, vol 38. Academic Press, Amsterdam, Netherlands.[CrossRef]
14. Hamer JE,, Howard RJ,, Chumley FG,, Valent B . 1988. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239 : 288290.[CrossRef]
15. Smith PJS,, Collis LP,, Messerli MA . 2010. Windows to cell function and dysfunction: signatures written in the boundary layers. BioEssays 32 : 514523.[CrossRef] [PubMed]
16. Skamnioti P,, Gurr SJ . 2007. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19 : 26742689.[CrossRef]
17. Deising H,, Nicholson RL,, Haug M,, Howard RJ,, Mendgen K . 1992. Adhesion pad formation and the involvement of cutinase and esterases in the attachment of Uredospores to the host cuticle. Plant Cell 4 : 11011111.[CrossRef] [PubMed]
18. Feng J,, Wang F,, Liu G,, Greenshields D,, Shen W,, Kaminskyj S,, Hughes GR,, Peng Y,, Selvaraj G,, Zou J,, Wei Y . 2009. Analysis of a Blumeria graminis-secreted lipase reveals the importance of host epicuticular wax components for fungal adhesion and development. Mol Plant Microbe Interact 22 : 16011610.[CrossRef]
19. Hegde Y,, Kolattukudy PE . 1997. Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea . Physiol Mol Plant Pathol 51 : 7584.[CrossRef]
20. Mankau R . 1980. Biological control of nematode pests by natural enemies. Annu Rev Phytopathol 18 : 415440.[CrossRef]
21. Howard RJ,, Ferrari MA,, Roach DH,, Money NP . 1991. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA 88 : 1128111284.[CrossRef] [PubMed]
22. Apoga D,, Barnard J,, Craighead HG,, Hoch HC . 2004. Quantification of substratum contact required for initiation of Colletotrichum graminicola appressoria. Fungal Genet Biol 41 : 112.[CrossRef] [PubMed]
23. Roderick HW . 1993. The infection of white clover (Trifolium repens) by conidia of Cymadothea trifolii . Mycol Res 97 : 227232.[CrossRef]
24. Kämper J , , et al . 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis . Nature 444 : 97101.[CrossRef] [PubMed]
25. Hoch HC,, Staples RC,, Whitehead B,, Comeau J,, Wolf ED . 1987. Signaling for growth orientation and cell differentiation by surface topography in Uromyces . Science 235 : 16591662.[CrossRef] [PubMed]
26. Bolton MD,, Kolmer JA,, Garvin DF . 2008. Wheat leaf rust caused by Puccinia triticina . Mol Plant Pathol 9 : 563575.[CrossRef] [PubMed]
27. Bush LP,, Wilkinson HH,, Schardl CL . 1997. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114 : 17.[CrossRef] [PubMed]
28. Christensen MJ,, Bennett RJ,, Ansari HA,, Koga H,, Johnson RD,, Bryan GT,, Simpson WR,, Koolaard JP,, Nickless EM,, Voisey CR . 2008. Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45 : 8493.[CrossRef]
29. Jaffe MJ,, Leopold AC,, Staples RC . 2002. Thigmo responses in plants and fungi. Am J Bot 89 : 375382.[PubMed] [CrossRef]
30. Voisey CR . 2010. Intercalary growth in hyphae of filamentous fungi. Fungal Biol Rev 24 : 123131.[CrossRef]
31. Bécard G,, Piché Y . 1989. Fungal growth stimulation by CO2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Appl Environ Microbiol 55 : 23202325.[PubMed]
32. Horan DP,, Chilvers GA . 1990. Chemotropism – the key to ectomycorrhizal formation? New Phytol 116 : 297301.[CrossRef]
33. Sbrana C,, Giovannetti M . 2005. Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae . Mycorrhiza 15 : 539545.[CrossRef] [PubMed]
34. Pumplin N,, Harrison MJ . 2009. Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151 : 809819.[CrossRef]
35. Doré J,, Marmeisse R,, Combier J-P,, Gay G . 2014. A fungal conserved gene from the basidiomycete Hebeloma cylindrosporum is essential for efficient ectomycorrhiza formation. Mol Plant Microbe Interact 27 : 10591069.[CrossRef]
36. Betz R,, Crabb JW,, Meyer HE,, Wittig R,, Duntze W . 1987. Amino acid sequences of a-factor mating peptides from Saccharomyces cerevisiae . J Biol Chem 262 : 546548.[PubMed]
37. Stötzler D,, Kiltz H-H,, Duntze W . 1976. Primary structure of α-factor peptides from Saccharomyces cerevisiae . Eur J Biochem 69 : 397400.[CrossRef]
38. Fricker M,, Boddy L,, Bebber D, . 2007. Network organisation of mycelial fungi, p 309330. In Gow NAR (ed), Biology of the Fungal Cell. Springer, Berlin.[CrossRef]
39. de la Providencia IE,, de Souza FA,, Fernández F,, Delmas NS,, Declerck S . 2005. Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol 165 : 261271.[CrossRef]
40. Sbrana C,, Fortuna P,, Giovannetti M . 2011. Plugging into the network: belowground connections between germlings and extraradical mycelium of arbuscular mycorrhizal fungi. Mycologia 103 : 307316.[CrossRef] [PubMed]
41. Croll D,, Giovannetti M,, Koch AM,, Sbrana C,, Ehinger M,, Lammers PJ,, Sanders IR . 2009. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices . New Phytol 181 : 924937.[CrossRef]
42. Badalyan SM,, Polak E,, Hermann R,, Aebi M,, Kües U . 2004. Role of peg formation in clamp cell fusion of homobasidiomycete fungi. J Basic Microbiol 44 : 167177.[CrossRef] [PubMed]
43. Nordbring-Hertz B,, Friman FE,, Veenhuis M . 1989. Hyphal fusion during initial stages of trap formation in Arthorbotrys oligospora . Antonie van Leeuwenhoek 55 : 237244.[PubMed]
44. Gabriela Roca M,, Read ND,, Wheals AE . 2005. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol Lett 249 : 191198.[CrossRef] [PubMed]
45. Fleissner A,, Leeder AC,, Roca MG,, Read ND,, Glass NL . 2009. Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci USA 106 : 1938719392.[CrossRef]
46. Read ND,, Lichius A,, Shoji JY,, Goryachev AB . 2009. Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12 : 608615.[CrossRef] [PubMed]
47. Uchida K,, Ishitani C,, Ikeda Y,, Sakaguchi K . 1958. An attempt to produce interspecific hybrids between Aspergillus oryzae and Asp. Sojae . J Gen Appl Microbiol 4 : 3138.[CrossRef]
48. de Hoog GS,, Takeo K . 1991. Karyology and the possible function of the dual conidia of Dissoconium (Hyphomycetes). Antonie van Leeuwenhoek 59 : 285291.[PubMed]
49. Roca MG,, Davide LC,, Mendes-Costa MC,, Wheals A . 2003. Conidial anastomosis tubes in Colletotrichum . Fungal Genet Biol 40 : 138145.[CrossRef]
50. Brown GD,, Denning DW,, Gow NA,, Levitz SM,, Netea MG,, White TC . 2012. Hidden killers: human fungal infections. Sci Transl Med 4 : 165rv113.[CrossRef] [PubMed]
51. Kozinn PJ,, Taschdjian CL,, Burchall JJ,, Wiener H . 1960. Transmission of P32-labeled Candida albicans to newborn mice at birth. AMA J Dis Child 99 : 3134.[PubMed]
52. Degreef H . 2008. Clinical forms of dermatophytosis (ringworm infection). Mycopathologia 166 : 257265.[CrossRef] [PubMed]
53. Richardson M,, Edward M, . 2000. Model systems for the study of dermatophyte and non-dermatophyte invasion of human keratin, p 115121. In Kushwaha RKS,, Guarro J (ed), Biology of Dermatophytes and Other Keratinophilic Fungi. Revista Iberoamericana de Micología, Bilbao.
54. McCourtie J,, Douglas LJ . 1985. Extracellular polymer of Candida albicans: isolation, analysis and role in adhesion. J Gen Microbiol 131 : 495503.[PubMed]
55. Esquenazi D,, Alviano CS,, de Souza W,, Rozental S . 2004. The influence of surface carbohydrates during in vitro infection of mammalian cells by the dermatophyte Trichophyton rubrum . Res Microbiol 155 : 144153.[CrossRef]
56. Odds FC . 1994. Pathogenesis of Candida infections. J Am Acad Dermatol 31 : S2S5.[CrossRef]
57. Tronchin G,, Bouchara JP,, Robert R,, Senet JM . 1988. Adherence of Candida albicans germ tubes to plastic: ultrastructural and molecular studies of fibrillar adhesins. Infect Immun 56 : 19871993.[PubMed]
58. Staab JF,, Bradway SD,, Fidel PL,, Sundstrom P . 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283 : 15351538.[CrossRef]
59. Esquenazi D,, de Souza W,, Alviano CS,, Rozental S . 2003. The role of surface carbohydrates on the interaction of microconidia of Trichophyton mentagrophytes with epithelial cells. FEMS Immunol Med Microbiol 35 : 113123.[CrossRef]
60. Bitencourt TA,, Macedo C,, Franco ME,, Assis AF,, Komoto TT,, Stehling EG,, Beleboni RO,, Malavazi I,, Marins M,, Fachin AL . 2016. Transcription profile of Trichophyton rubrum conidia grown on keratin reveals the induction of an adhesin-like protein gene with a tandem repeat pattern. BMC Genomics 17 : 249.[CrossRef]
61. Schild L,, Heyken A,, de Groot PWJ,, Hiller E,, Mock M,, de Koster C,, Horn U,, Rupp S,, Hube B . 2011. Proteolytic cleavage of covalently linked cell wall proteins by Candida albicans Sap9 and Sap10. Eukaryot Cell 10 : 98109.[CrossRef]
62. Peres NT,, Sanches PR,, Falcão JP,, Silveira HC,, Paião FG,, Maranhão FC,, Gras DE,, Segato F,, Cazzaniga RA,, Mazucato M,, Cursino-Santos JR,, Aquino-Ferreira R,, Rossi A,, Martinez-Rossi NM . 2010. Transcriptional profiling reveals the expression of novel genes in response to various stimuli in the human dermatophyte Trichophyton rubrum . BMC Microbiol 10 : 39.[CrossRef]
63. Peres NT,, da Silva LG,, Santos RS,, Jacob TR,, Persinoti GF,, Rocha LB,, Falcão JP,, Rossi A,, Martinez-Rossi NM . 2016. In vitro and ex vivo infection models help assess the molecular aspects of the interaction of Trichophyton rubrum with the host milieu. Med Mycol 54 : 420427.[CrossRef]
64. Elving GJ,, van der Mei HC,, van Weissenbruch R,, Busscher HJ,, Albers FWJ . 2002. Comparison of the microbial composition of voice prosthesis biofilms from patients requiring frequent versus infrequent replacement. Ann Otol Rhinol Laryngol 111 : 200203.[CrossRef]
65. Leonhard M,, Tobudic S,, Moser D,, Zatorska B,, Bigenzahn W,, Schneider-Stickler B . 2013. Growth kinetics of Candida biofilm on medical polymers: a long-term in vitro study. Laryngoscope 123 : 732737.[CrossRef]
66. Bowen AD,, Davidson FA,, Keatch R,, Gadd GM . 2007. Induction of contour sensing in Aspergillus niger by stress and its relevance to fungal growth mechanics and hyphal tip structure. Fungal Genet Biol 44 : 484491.[CrossRef]
67. Watts HJ,, Véry AA,, Perera TH,, Davies JM,, Gow NA . 1998. Thigmotropism and stretch-activated channels in the pathogenic fungus Candida albicans . Microbiology 144 : 689695.[CrossRef]
68. Gonia S,, Norton J,, Watanaskul L,, Pulver R,, Morrison E,, Brand A,, Gale CA . 2013. Rax2 is important for directional establishment of growth sites, but not for reorientation of growth axes, during Candida albicans hyphal morphogenesis. Fungal Genet Biol 56 : 116124.[CrossRef] [PubMed]
69. Ueno K,, Matsumoto Y,, Uno J,, Sasamoto K,, Sekimizu K,, Kinjo Y,, Chibana H . 2011. Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS One 6 : e24759.[CrossRef]
70. Ene IV,, Adya AK,, Wehmeier S,, Brand AC,, MacCallum DM,, Gow NAR,, Brown AJP . 2012. Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14 : 13191335.[CrossRef]
71. Brand A,, Lee K,, Veses V,, Gow NA . 2009. Calcium homeostasis is required for contact-dependent helical and sinusoidal tip growth in Candida albicans hyphae. Mol Microbiol 71 : 11551164.[CrossRef] [PubMed]
72. Brand A,, Shanks S,, Duncan VMS,, Yang M,, Mackenzie K,, Gow NAR . 2007. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17 : 347352.[CrossRef] [PubMed]
73. Brand AC,, Morrison E,, Milne S,, Gonia S,, Gale CA,, Gow NAR . 2014. Cdc42 GTPase dynamics control directional growth responses. Proc Natl Acad Sci USA 111 : 811816.[CrossRef] [PubMed]
74. Sukharev SI,, Martinac B,, Arshavsky VY,, Kung C . 1993. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J 65 : 177183.[CrossRef]
75. Pivetti CD,, Yen M-R,, Miller S,, Busch W,, Tseng Y-H,, Booth IR,, Saier MH Jr . 2003. Two families of mechanosensitive channel proteins. Microbiol Mol Biol Rev 67 : 6685.[CrossRef]
76. Teng J,, Loukin S,, Anishkin A,, Kung C . 2015. The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflugers Arch 467 : 2737.[CrossRef] [PubMed]
77. Rasmussen T,, Rasmussen A,, Singh S,, Galbiati H,, Edwards MD,, Miller S,, Booth IR . 2015. Properties of the mechanosensitive channel MscS pore revealed by tryptophan scanning mutagenesis. Biochemistry 54 : 45194530.[CrossRef]
78. Brohawn SG,, Su Z,, MacKinnon R . 2014. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci USA 111 : 36143619.[CrossRef] [PubMed]
79. Gustin MC,, Zhou XL,, Martinac B,, Kung C . 1988. A mechanosensitive ion channel in the yeast plasma membrane. Science 242 : 762765.[CrossRef]
80. Levina N,, Tötemeyer S,, Stokes NR,, Louis P,, Jones MA,, Booth IR . 1999. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18 : 17301737.[CrossRef] [PubMed]
81. Miyamoto T,, Morita K,, Takemoto D,, Takeuchi K,, Kitano Y,, Miyakawa T,, Nakayama K,, Okamura Y,, Sasaki H,, Miyachi Y,, Furuse M,, Tsukita S . 2005. Tight junctions in Schwann cells of peripheral myelinated axons. J Cell Biol 169 : 527538.[CrossRef]
82. Zhou XL,, Stumpf MA,, Hoch HC,, Kung C . 1991. A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces . Science 253 : 14151417.[CrossRef] [PubMed]
83. Hamam A,, Lew RR . 2012. Electrical phenotypes of calcium transport mutant strains of a filamentous fungus, Neurospora crassa . Eukaryot Cell 11 : 694702.[CrossRef]
84. Nakayama Y,, Hirata A,, Iida H . 2014. Mechanosensitive channels Msy1 and Msy2 are required for maintaining organelle integrity upon hypoosmotic shock in Schizosaccharomyces pombe . FEMS Yeast Res 14 : 992994.[CrossRef]
85. Ozeki-Miyawaki C,, Moriya Y,, Tatsumi H,, Iida H,, Sokabe M . 2005. Identification of functional domains of Mid1, a stretch-activated channel component, necessary for localization to the plasma membrane and Ca2+ permeation. Exp Cell Res 311 : 8495.[CrossRef]
86. Iida H,, Nakamura H,, Ono T,, Okumura MS,, Anraku Y . 1994. MID1, a novel Saccharomyces cerevisiae gene encoding a plasma membrane protein, is required for Ca2+ influx and mating. Mol Cell Biol 14 : 82598271.[CrossRef]
87. Iida H,, Yagawa Y,, Anraku Y . 1990. Essential role for induced Ca2+ influx followed by [Ca2+]i rise in maintaining viability of yeast cells late in the mating pheromone response pathway. J Biol Chem 265 : 1339113399.[PubMed]
88. Kanzaki M,, Nagasawa M,, Kojima I,, Sato C,, Naruse K,, Sokabe M,, Iida H . 1999. Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285 : 882886.[CrossRef]
89. Lew RR,, Abbas Z,, Anderca MI,, Free SJ . 2008. Phenotype of a mechanosensitive channel mutant, mid-1, in a filamentous fungus, Neurospora crassa . Eukaryot Cell 7 : 647655.[CrossRef]
90. Bormann J,, Tudzynski P . 2009. Deletion of Mid1, a putative stretch-activated calcium channel in Claviceps purpurea, affects vegetative growth, cell wall synthesis and virulence. Microbiology 155 : 39223933.[CrossRef]
91. Jiang H,, Shen Y,, Liu W,, Lu L . 2014. Deletion of the putative stretch-activated ion channel Mid1 is hypervirulent in Aspergillus fumigatus . Fungal Genet Biol 62 : 6270.[CrossRef] [PubMed]
92. Cavinder B,, Hamam A,, Lew RR,, Trail F . 2011. Mid1, a mechanosensitive calcium ion channel, affects growth, development, and ascospore discharge in the filamentous fungus Gibberella zeae . Eukaryot Cell 10 : 832841.[CrossRef]
93. Fischer M,, Schnell N,, Chattaway J,, Davies P,, Dixon G,, Sanders D . 1997. The Saccharomyces cerevisiae CCH1 gene is involved in calcium influx and mating. FEBS Lett 419 : 259262.[CrossRef] [PubMed]
94. Paidhungat M,, Garrett S . 1997. A homolog of mammalian, voltage-gated calcium channels mediates yeast pheromone-stimulated Ca2+ uptake and exacerbates the cdc1(Ts) growth defect. Mol Cell Biol 17 : 63396347.[CrossRef]
95. Muller EM,, Locke EG,, Cunningham KW . 2001. Differential regulation of two Ca(2+) influx systems by pheromone signaling in Saccharomyces cerevisiae . Genetics 159 : 15271538.[PubMed]
96. Locke EG,, Bonilla M,, Liang L,, Takita Y,, Cunningham KW . 2000. A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol 20 : 66866694.[CrossRef] [PubMed]
97. Dolphin AC . 2013. The α2δ subunits of voltage-gated calcium channels. Biochim Biophys Acta 1828 : 15411549.[CrossRef]
98. Ghezzi A,, Liebeskind BJ,, Thompson A,, Atkinson NS,, Zakon HH . 2014. Ancient association between cation leak channels and Mid1 proteins is conserved in fungi and animals. Front Mol Neurosci 7 : 15.[CrossRef]
99. Muller EM,, Mackin NA,, Erdman SE,, Cunningham KW . 2003. Fig1p facilitates Ca2+ influx and cell fusion during mating of Saccharomyces cerevisiae . J Biol Chem 278 : 3846138469.[CrossRef]
100. Yang M,, Brand A,, Srikantha T,, Daniels KJ,, Soll DR,, Gow NAR . 2011. Fig1 facilitates calcium influx and localizes to membranes destined to undergo fusion during mating in Candida albicans . Eukaryot Cell 10 : 435444.[CrossRef]
101. Martin DC,, Kim H,, Mackin NA,, Maldonado-Báez L,, Evangelista CC Jr,, Beaudry VG,, Dudgeon DD,, Naiman DQ,, Erdman SE,, Cunningham KW . 2011. New regulators of a high affinity Ca2+ influx system revealed through a genome-wide screen in yeast. J Biol Chem 286 : 1074410754.[CrossRef]
102. Kock C,, Dufrêne YF,, Heinisch JJ . 2015. Up against the wall: is yeast cell wall integrity ensured by mechanosensing in plasma membrane microdomains? Appl Environ Microbiol 81 : 806811.[CrossRef]
103. Dichtl K,, Samantaray S,, Wagener J . 2016. Cell wall integrity signalling in human pathogenic fungi. Cell Microbiol 18 : 12281238.[CrossRef] [PubMed]
104. Kumamoto CA . 2005. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci USA 102 : 55765581.[CrossRef]
105. Dupres V,, Alsteens D,, Wilk S,, Hansen B,, Heinisch JJ,, Dufrêne YF . 2009. The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat Chem Biol 5 : 857862.[PubMed] [CrossRef]
106. Davenport KR,, Sohaskey M,, Kamada Y,, Levin DE,, Gustin MC . 1995. A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270 : 3015730161.[CrossRef]
107. Delley P-A,, Hall MN . 1999. Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J Cell Biol 147 : 163174.[CrossRef] [PubMed]
108. Krantz M,, Becit E,, Hohmann S . 2006. Comparative genomics of the HOG-signalling system in fungi. Curr Genet 49 : 137151.[CrossRef] [PubMed]
109. Tatebayashi K,, Tanaka K,, Yang HY,, Yamamoto K,, Matsushita Y,, Tomida T,, Imai M,, Saito H . 2007. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26 : 35213533.[CrossRef]
110. Yamamoto K,, Tatebayashi K,, Saito H . 2016. Binding of the extracellular eight-cysteine motif of Opy2 to the putative osmosensor Msb2 is essential for activation of the yeast high-osmolarity glycerol pathway. Mol Cell Biol 36 : 475487.[CrossRef]
111. Swidergall M,, van Wijlick L,, Ernst JF . 2015. Signaling domains of mucin Msb2 in Candida albicans . Eukaryot Cell 14 : 359370.[CrossRef] [PubMed]
112. Levitin F,, Stern O,, Weiss M,, Gil-Henn C,, Ziv R,, Prokocimer Z,, Smorodinsky NI,, Rubinstein DB,, Wreschner DH . 2005. The MUC1 SEA module is a self-cleaving domain. J Biol Chem 280 : 3337433386.[CrossRef]
113. Szafranski-Schneider E,, Swidergall M,, Cottier F,, Tielker D,, Román E,, Pla J,, Ernst JF . 2012. Msb2 shedding protects Candida albicans against antimicrobial peptides. PLoS Pathog 8 : e1002501.[CrossRef]
114. Román E,, Cottier F,, Ernst JF,, Pla J . 2009. Msb2 signaling mucin controls activation of Cek1 mitogen-activated protein kinase in Candida albicans . Eukaryot Cell 8 : 12351249.[CrossRef]
115. Pérez-Nadales E,, Di Pietro A . 2011. The membrane mucin Msb2 regulates invasive growth and plant infection in Fusarium oxysporum . Plant Cell 23 : 11711185.[CrossRef]
116. Lanver D,, Mendoza-Mendoza A,, Brachmann A,, Kahmann R . 2010. Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis . Plant Cell 22 : 20852101.[CrossRef] [PubMed]
117. Liu W,, Zhou X,, Li G,, Li L,, Kong L,, Wang C,, Zhang H,, Xu J-R . 2011. Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7 : e1001261.[CrossRef]
118. Leroch M,, Mueller N,, Hinsenkamp I,, Hahn M . 2015. The signalling mucin Msb2 regulates surface sensing and host penetration via BMP1 MAP kinase signalling in Botrytis cinerea . Mol Plant Pathol 16 : 787798.[CrossRef]
119. Xue C,, Hsueh Y-P,, Heitman J . 2008. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32 : 10101032.[CrossRef]
120. Maidan MM,, Thevelein JM,, Van Dijck P . 2005. Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem Soc Trans 33 : 291293.[CrossRef]
121. Turrà D,, El Ghalid M,, Rossi F,, Di Pietro A . 2015. Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527 : 521524.[CrossRef]
122. Maidan MM,, De Rop L,, Serneels J,, Exler S,, Rupp S,, Tournu H,, Thevelein JM,, Van Dijck P . 2005. The G protein-coupled receptor Gpr1 and the Gα protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans . Mol Biol Cell 16 : 19711986.[CrossRef]
123. Sciascia QL,, Sullivan PA,, Farley PC . 2004. Deletion of the Candida albicans G-protein-coupled receptor, encoded by orf19.1944 and its allele orf19.9499, produces mutants defective in filamentous growth. Can J Microbiol 50 : 10811085.[CrossRef]
124. Xu JR,, Hamer JE . 1996. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea . Genes Dev 10 : 26962706.[CrossRef]
125. D’Souza CA,, Heitman J . 2001. Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev 25 : 349364.[CrossRef] [PubMed]
126. Dürrenberger F,, Wong K,, Kronstad JW . 1998. Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis . Proc Natl Acad Sci USA 95 : 56845689.[CrossRef] [PubMed]
127. Chen T-H,, Hsu C-S,, Tsai P-J,, Ho Y-F,, Lin N-S . 2001. Heterotrimeric G-protein and signal transduction in the nematode-trapping fungus Arthrobotrys dactyloides . Planta 212 : 858863.[CrossRef]
128. DeZwaan TM,, Carroll AM,, Valent B,, Sweigard JA . 1999. Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11 : 20132030.[CrossRef]
129. Kulkarni RD,, Thon MR,, Pan H,, Dean RA . 2005. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea . Genome Biol 6 : R24.[CrossRef] [PubMed]
130. Chachisvilis M,, Zhang Y-L,, Frangos JA . 2006. G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci USA 103 : 1546315468.[CrossRef]
131. Makino A,, Prossnitz ER,, Bünemann M,, Wang JM,, Yao W,, Schmid-Schönbein GW . 2006. G protein-coupled receptors serve as mechanosensors for fluid shear stress in neutrophils. Am J Physiol Cell Physiol 290 : C1633C1639.[CrossRef]
132. Shyy JY-J,, Chien S . 2002. Role of integrins in endothelial mechanosensing of shear stress. Circ Res 91 : 769775.[CrossRef] [PubMed]
133. Pan L,, Zhao Y,, Yuan Z,, Qin G . 2016. Research advances on structure and biological functions of integrins. Springerplus 5 : 1094.[CrossRef] [PubMed]
134. Knechtle P,, Kaufmann A,, Cavicchioli D,, Philippsen P . 2008. The Paxillin-like protein AgPxl1 is required for apical branching and maximal hyphal growth in A. uthgossypii . Fungal Genet Biol 45 : 829838.[CrossRef]
135. Mackin NA,, Sousou TJ,, Erdman SE . 2004. The PXL1 gene of Saccharomyces cerevisiae encodes a paxillin-like protein functioning in polarized cell growth. Mol Biol Cell 15 : 19041917.[CrossRef] [PubMed]
136. Ge W,, Balasubramanian MK . 2008. Pxl1p, a paxillin-related protein, stabilizes the actomyosin ring during cytokinesis in fission yeast. Mol Biol Cell 19 : 16801692.[CrossRef]
137. Pinar M,, Coll PM,, Rincón SA,, Pérez P . 2008. Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol Biol Cell 19 : 17271738.[CrossRef] [PubMed]
138. Santoni G,, Gismondi A,, Liu JH,, Punturieri A,, Santoni A,, Frati L,, Piccoli M,, Djeu JY . 1994. Candida albicans expresses a fibronectin receptor antigenically related to α5β1 integrin. Microbiology 140 : 29712979.[CrossRef]
139. Corrêa A Jr,, Staples RC,, Hoch HC . 1996. Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194 : 91102.[CrossRef]
140. Marcantonio EE,, Hynes RO . 1988. Antibodies to the conserved cytoplasmic domain of the integrin beta 1 subunit react with proteins in vertebrates, invertebrates, and fungi. J Cell Biol 106 : 17651772.[CrossRef]
141. Santoni G,, Spreghini E,, Lucciarini R,, Amantini C,, Piccoli M . 2001. Involvement of α(v)β3 integrin-like receptor and glycosaminoglycans in Candida albicans germ tube adhesion to vitronectin and to a human endothelial cell line. Microb Pathog 31 : 159172.[CrossRef]
142. Spreghini E,, Gismondi A,, Piccoli M,, Santoni G . 1999. Evidence for αvβ3 and αvβ5 integrin-like vitronectin (VN) receptors in Candida albicans and their involvement in yeast cell adhesion to VN. J Infect Dis 180 : 156166.[CrossRef] [PubMed]
143. Klotz SA,, Pendrak ML,, Hein RC . 2001. Antibodies to α5β1 and α(v)β3 integrins react with Candida albicans alcohol dehydrogenase. Microbiology 147 : 31593164.[CrossRef]
144. Gozalbo D,, Gil-Navarro I,, Azorín I,, Renau-Piqueras J,, Martínez JP,, Gil ML . 1998. The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect Immun 66 : 20522059.[PubMed]
145. Gale C,, Finkel D,, Tao N,, Meinke M,, McClellan M,, Olson J,, Kendrick K,, Hostetter M . 1996. Cloning and expression of a gene encoding an integrin-like protein in Candida albicans . Proc Natl Acad Sci USA 93 : 357361.[CrossRef] [PubMed]
146. Gale CA,, Bendel CM,, McClellan M,, Hauser M,, Becker JM,, Berman J,, Hostetter MK . 1998. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1 . Science 279 : 13551358.[CrossRef]
147. Gale C,, Gerami-Nejad M,, McClellan M,, Vandoninck S,, Longtine MS,, Berman J . 2001. Candida albicans Int1p interacts with the septin ring in yeast and hyphal cells. Mol Biol Cell 12 : 35383549.[CrossRef] [PubMed]
148. Read ND,, Kellock LJ,, Collins TJ,, Gundlach AM . 1997. Role of topography sensing for infection-structure differentiation in cereal rust fungi. Planta 202 : 163170.[CrossRef]
149. Balestrini R,, Bonfante P . 2014. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5 : 237.[CrossRef] [PubMed]
150. Heiman MG,, Walter P . 2000. Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J Cell Biol 151 : 719730.[CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error