Chapter 22 : Thigmo Responses: The Fungal Sense of Touch

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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
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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
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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
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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
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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
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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
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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
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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
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