1932

Abstract

Fungi are the dark matter of biology, typically leading cryptic lives, buried in soil or inside of plants or other organisms, and emerging into the light only when they build their elegantly engineered fruiting bodies. Ecological success across so many niches has required that they solve many challenging fluid mechanical problems of growth, dispersal, and transport of fluids across networks. Study of fungal life histories by fluid mechanicians has shown their exquisite capability for engineering and revealed new organizing ideas for understanding fungal diversity.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-fluid-122316-045308
2019-01-05
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/fluid/51/1/annurev-fluid-122316-045308.html?itemId=/content/journals/10.1146/annurev-fluid-122316-045308&mimeType=html&fmt=ahah

Literature Cited

  1. Abadeh A, Lew RR 2013. Mass flow and velocity profiles in Neurospora hyphae: Partial plug flow dominates intra-hyphal transport. Microbiology 159:2386–94
    [Google Scholar]
  2. Alim K, Amselem G, Peaudecerf F, Brenner MP, Pringle A 2013. Random network peristalsis in Physarum polycephalum organizes fluid flows across an individual. PNAS 110:13306–11
    [Google Scholar]
  3. Almeida MC, Brand AC 2017. Thigmo responses: the fungal sense of touch. Microbiol. Spectr. 5:2FUNK–0040-2016
    [Google Scholar]
  4. Alpin PS, Hill DJ 1979. Growth analysis of circular lichen thalli. J. Theor. Biol. 78:347–63
    [Google Scholar]
  5. Armstrong RA 1979. Growth and regeneration of lichen thalli with the central portions artificially removed. Environ. Exp. Bot. 19:175–78
    [Google Scholar]
  6. Armstrong RA, Bradwell T 2011. Growth of foliose lichens: a review. Symbiosis 53:1 https://doi.org/10.1007/s13199-011-0108-4
    [Crossref] [Google Scholar]
  7. Aylor D 1999. Biophysical scaling and the passive dispersal of fungus spores: relationship to integrated pest management strategies. Agric. For. Meteorol. 97:275–92
    [Google Scholar]
  8. Bartnicki-Garcia S, Hergert F, Gierz G 1989. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153:46–57
    [Google Scholar]
  9. Bäuerle FK, Kramar M, Alim K 2017. Spatial mapping reveals multi-step pattern of wound healing in Physarum polycephalum. J. Phys. D 50:434005
    [Google Scholar]
  10. Bebber DP, Hynes J, Darrah PR, Boddy L, Fricker MD 2007. Biological solutions to transport network design. Proc. R. Soc. Lond. B 274:2307–15
    [Google Scholar]
  11. Bergman K, Burke PV, Cerdá-Olmedo E, David CN, Delbrück M et al. 1969. Phycomyces. Bacteriol. Rev. 33:199–157
    [Google Scholar]
  12. Blackwell M 2011. The fungi: 1, 2, 3 … 5.1 million species?. Am. J. Bot. 98:426–38
    [Google Scholar]
  13. Boddy L 2000. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol. 31:185–94
    [Google Scholar]
  14. Boddy L, Wood J, Redman E, Hynes J, Fricker MD 2010. Fungal network responses to grazing. Fungal Genet. Biol. 47:522–30
    [Google Scholar]
  15. Bonner JT, Kane KK, Levey RH 1956. Studies on the mechanics of growth in the common mushroom, Agaricus campestris. Mycologia 48:13–19
    [Google Scholar]
  16. Boreyko JB, Chen C-H 2009. Self-propelled dropwise condensate on superhydrophobic surfaces. Phys. Rev. Lett. 103:184501
    [Google Scholar]
  17. Boudaoud A 2003. Growth of walled cells: from shells to vesicles. Phys. Rev. Lett. 91:018104
    [Google Scholar]
  18. Brodo IM, Sharnoff SD, Sharnoff S 2001. Lichens of North America New Haven, CT: Yale Univ. Press
    [Google Scholar]
  19. Brown JKM, Hovmoller MS 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–41
    [Google Scholar]
  20. Buller AHR 1909–1950. Researches on Fungi Vols. 1–7. London: Longmans, Green, and Co.
    [Google Scholar]
  21. Campàs O, Mahadevan L 2009. Shape and dynamics of tip-growing cells. Curr. Biol. 19:2102–7
    [Google Scholar]
  22. Campàs O, Rojas E, Dumais J, Mahadevan L 2012. Strategies for cell shape control in tip-growing cells. Am. J. Bot. 99:1577–82
    [Google Scholar]
  23. Cavinder B, Hamam A, Lew R, Trail F 2011. Mid1, a mechanosensitive calcium ion channel, affects growth, development, and ascospore discharge in the filamentous fungus Gibberella zeae. Eukaryot. Cell 10:832–41
    [Google Scholar]
  24. Childress S, Keller J 1980. Lichen growth. J. Theor. Biol. 82:157–65
    [Google Scholar]
  25. Craig GD, Gull K, Wood DA 1977. Stipe elongation in Agaricus bisporus. J. Gen. Microbiol. 102:337–47
    [Google Scholar]
  26. Davidson JM, Rizzo DM, Garbelotto M, Tjosvold S, Slaughter GW 2002. Phytophthora ramorum and sudden oak death in California: II. Transmission and survival. Proceedings of the Fifth Symposium on Oak Woodlands: Oaks in California's Challenging Landscape RB Standiford, D McCreary, KL Purcell741–50 Albany, CA: Pac. Southwest Res. Stn., U.S. Dep. Agric. For. Serv.
    [Google Scholar]
  27. de Bary HA 1887. Comparative Morphology and Biology of the Fungi, Mycetozoa and Bacteria Oxford: Clarendon
    [Google Scholar]
  28. Deegan RF, Bakajin O, Dupont TF, Huber G, Nagel SR, Witten TA 1997. Capillary flow as the cause of ring stains from dried liquid drops. Nature 389:827–29
    [Google Scholar]
  29. Deering RF, Dong F, Rambo D, Money N 2001. Airflow patterns around mushrooms and their relationship to spore dispersal. Mycologia 93:732–36
    [Google Scholar]
  30. Dennison DS, Foster KW 1977. Intracellular rotation and the phototropic response of Phycomyces. Biophys. J. 18:103–23
    [Google Scholar]
  31. Drescher K, Goldstein RE, Tuval I 2010. Fidelity of adaptive phototaxis. PNAS 107:11171–76
    [Google Scholar]
  32. Dressaire E, Yamada L, Song B, Roper M 2016. Mushrooms use convectively created airflows to disperse their spores. PNAS 113:2833–38
    [Google Scholar]
  33. Eilers FI 1974. Growth regulation in Coprinus radiatus. Arch. Microbiol. 96:353–64
    [Google Scholar]
  34. Fischer MW, Cox J, Davis D, Wagner A, Taylor R et al. 2004. New information on the mechanism of forcible ascospore discharge from Ascobolus immersus. Fungal Genet. Biol. 41:698–707
    [Google Scholar]
  35. Fischer MW, Money NP 2010. Why mushrooms form gills: efficiency of the lamellate morphology. Fungal Biol. 114:57–63
    [Google Scholar]
  36. Fischer MW, Stolze-Rybczynski JL, Cui Y, Money NP 2010. How far and how fast can mushroom spores fly? Physical limits on ballistospore size and discharge distance in the Basidiomycota. Fungal Biol. 114:669–75
    [Google Scholar]
  37. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC et al. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–94
    [Google Scholar]
  38. Fleißner A, Simonin AR, Glass NL 2008. Cell fusion in the filamentous fungus, Neurospora crassa. Cell Fusion EH Chen21–38 New York: Humana
    [Google Scholar]
  39. Fritz J, Seminara A, Roper M, Pringle A, Brenner M 2013. A natural O-ring optimizes the dispersal of fungal spores. J. R. Soc. Interface 10:20130187
    [Google Scholar]
  40. Goriely A, Tabor M 2011. Spontaneous rotational inversion in Phycomyces. Phys. Rev. Lett. 106:138103
    [Google Scholar]
  41. Goyal A, Manoharachary C 2014. Future Challenges in Crop Protection Against Fungal Pathogens New York: Springer Sci. Bus. Media
    [Google Scholar]
  42. Greene DF 2005. The role of abscission in long-distance seed dispersal by the wind. Ecology 86:3105–10
    [Google Scholar]
  43. Gregory P, Lacey ME 1963. Liberation of spores from mouldy hay. Trans. Br. Mycol. Soc. 46:73–80
    [Google Scholar]
  44. Gruen HE 1963. Endogenous growth regulation in carpophores of Agaricus bisporus. Plant Physiol. 38:652–66
    [Google Scholar]
  45. Guo X, Fernando W 2005. Seasonal and diurnal patterns of spore dispersal by Leptosphaeria maculans from canola stubble in relation to environmental conditions. Plant Disease 89:97–104
    [Google Scholar]
  46. Hallen H, Trail F 2008. The L-type calcium ion channel, Cch1, affects ascospore discharge and mycelial growth in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot. Cell 7:415–24
    [Google Scholar]
  47. Hanson KL, Nicolau DV, Filipponi L, Wang L, Lee AP, Nicolau DV 2006. Fungi use efficient algorithms for the exploration of microfluidic networks. Small 2:1212–20
    [Google Scholar]
  48. Hawksworth DL 1991. The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol. Res. 95:641–55
    [Google Scholar]
  49. Henkel Corp 2014. Loctite® super glue ultra gel control® Tech. Data Sheet, Henkel Corp., Rocky Hill, CT. http://www.loctiteproducts.com/tds/SG_UG_CNTRL_tds.pdf
    [Google Scholar]
  50. Hickey PC, Dou H, Foshe S, Roper M 2016. Anti-jamming in a fungal transport network. arXiv:1601.06097 [physics.bio-ph]
  51. Hill D 1981. The growth of lichens with special reference to the modelling of circular thalli. Lichenologist 13:265–87
    [Google Scholar]
  52. Hofmeister W 1867. Die Lehre von der Pflanzenzelle Leipzig, Ger.: Engelmann
    [Google Scholar]
  53. Howard RJ, Ferrari MA, Roach DH, Money NP 1991. Penetration of hard substrates by a fungus employing enormous turgor pressures. PNAS 88:11281–84
    [Google Scholar]
  54. Husher J, Cesarov S, Davis CM, Fletcher TS, Mbuthia K et al. 1999. Evaporative cooling of mushrooms. Mycologia 91:351–52
    [Google Scholar]
  55. Hussein T, Norros V, Hakala J, Petaia T, Aalto PP et al. 2013. Species traits and inertial deposition of fungal spores. J. Aerosol Sci. 61:81–98
    [Google Scholar]
  56. Ingold CT 1928. Spore discharge in Podospora curvula. Ann. Bot. 42:567–70
    [Google Scholar]
  57. Ingold CT 1933. Spore discharge in the Ascomycetes. New Phytol. 32:175–96
    [Google Scholar]
  58. Ingold CT 1939. Spore Discharge in Land Plants Oxford: Clarendon
    [Google Scholar]
  59. Ingold CT 1956. A gas phase in viable fungal spores. Nature 177:1242–43
    [Google Scholar]
  60. Ingold CT 1971. Fungal Spores: Their Liberation and Dispersal Oxford: Clarendon
    [Google Scholar]
  61. Ingold CT 1992. The basidium: a spore gun of precise range. Mycologist 6:111–13
    [Google Scholar]
  62. Jackson JD 2001. Classical Electrodynamics New York: Wiley
    [Google Scholar]
  63. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V et al. 2006. Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:812–22
    [Google Scholar]
  64. Keith AD, Snipes W 1974. Viscosity of cellular protoplasm. Science 183:666–68
    [Google Scholar]
  65. King AL 1944. The spore discharge mechanism of common ferns. PNAS 30:155–61
    [Google Scholar]
  66. Koufopanou V, Burt A, Taylor JW 1997. Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidiodes immitis. PNAS 94:5478–82
    [Google Scholar]
  67. Kuparinen A 2006. Mechanistic models for wind dispersal. Trends Plant Sci. 11:296–301
    [Google Scholar]
  68. Lacey J 1996. Spore dispersal—its role in ecology and disease: the British contribution to fungal aerobiology. Mycol. Res. 100:641–60
    [Google Scholar]
  69. Langdon EM, Qiu Y, Niaki AG, McLaughlin GA, Weidmann C et al. 2018. mRNA structure determines specificity of a polyQ-driven phase separation. Science 360:6391922–27
    [Google Scholar]
  70. Lee C, Zhang H, Baker AE, Occhipinti P, Borsuk ME, Gladfelter AS 2013. Protein aggregation behavior regulates cyclin transcript localization and cell-cycle control. Dev. Cell 25:572–84
    [Google Scholar]
  71. Lew RR 2005. Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology 151:2685–92
    [Google Scholar]
  72. Lew RR 2011. How does a hypha grow? The biophysics of pressurized growth in fungi. Nat. Rev. Microbiol. 9:509–18
    [Google Scholar]
  73. Lew RR, Nasserifar S 2009. Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa. Microbiology 155:903–11
    [Google Scholar]
  74. Liu F, Chavez RL, Patek SN, Pringle A, Feng JJ, Chen CH 2017. Asymmetric drop coalescence launches fungal ballistospores with directionality. J. R. Soc. Interface 14:20170083
    [Google Scholar]
  75. Liu F, Ghigliotti G, Feng J, Chen CH 2014. Numerical simulations of self-propelled jumping upon drop coalescence on non-wetting surfaces. J. Fluid Mech. 752:39–65
    [Google Scholar]
  76. Lopez-Franco R, Bartnicki-Garcia S, Bracker CE 1994. Pulsed growth of fungal hyphal tips. PNAS 91:12228–32
    [Google Scholar]
  77. Maheshwari R 2005. Nuclear behavior in fungal hyphae. FEMS Microbiol. Lett. 249:7–14
    [Google Scholar]
  78. Marbach S, Alim K, Andrew N, Pringle A, Brenner MP 2016. Pruning to increase Taylor dispersion in Physarum polycephalum networks. Phys. Rev. Lett. 117:178103
    [Google Scholar]
  79. Meredith D 1961. Spore discharge in Deightoniella torulosa (Syd.) Ellis. Ann. Bot. 25:271–78
    [Google Scholar]
  80. Meredith D 1962. Spore discharge in Cordana musae (Zimm.) Höhnel and Zygosporium oscheoides Mont. Ann. Bot. 26:233–41
    [Google Scholar]
  81. Meredith D 1963. Violent spore release in some fungi imperfecti. Ann. Bot. 27:39–47
    [Google Scholar]
  82. Meredith D 1965. Violent spore release in Helminthosporium turcicum. Phytopathology 55:1099–102
    [Google Scholar]
  83. Micheli P 1729. Nova Plantarum Genera Vol. 3. Florence, Italy: Typis Bernardi Paperinii
    [Google Scholar]
  84. Minter D, Cannon D 1984. Ascospore discharge in some members of the Rhytismataceae. Trans. Br. Mycol. Soc. 83:65–92
    [Google Scholar]
  85. Moffatt HK 1964. Viscous and resistive eddies near a sharp corner. J. Fluid Mech. 18:1–18
    [Google Scholar]
  86. Mondal S, Gottwald T, Timmer L 2003. Environmental factors affecting the release and dispersal of ascospores of Mycosphaerella citri. Phytopathology 93:1031–36
    [Google Scholar]
  87. Money NP 1997. Wishful thinking of turgor revisited: the mechanics of fungal growth. Fungal Genet. Biol. 21:173–87
    [Google Scholar]
  88. Money NP 1998. More g's than the space shuttle: ballistospore discharge. Mycologia 90:547–58
    [Google Scholar]
  89. Money NP, Fischer MWF 2009. Biomechanics of spore release in phytopathogens. Plant Relationships HB Deising115–133 Berlin: Springer-Verlag
    [Google Scholar]
  90. Money NP, Harold FM 1993. Two water molds can grow without measurable turgor pressure. Planta 190:426–30
    [Google Scholar]
  91. Nagarajan S, Singh DV 1990. Long-distance dispersion of rust pathogens. Annu. Rev. Phytopathol. 28:139–53
    [Google Scholar]
  92. Nathan R, Katul GG, Bohrer G, Kuparinen A, Soons MB et al. 2011. Mechanistic models of seed dispersal by wind. Theor. Ecol. 4:113–32
    [Google Scholar]
  93. Nazockdast E, Rahimian A, Needleman D, Shelley M 2017. Cytoplasmic flows as signatures for the mechanics of mitotic positioning. Mol. Biol. Cell 28:3261–70
    [Google Scholar]
  94. Niksic M, Hadzic I, Glisic M 2004. Is. Phallus impudicus a mycological giant? Mycologist 18:21–22
    [Google Scholar]
  95. Noblin X, Rojas NO, Westbrook J, Llorens C, Argentina M, Dumais J 2012. The fern sporangium: a unique catapult. Science 335:1322–22
    [Google Scholar]
  96. Noblin X, Yang S, Dumais J 2009. Surface tension propulsion of fungal spores. J. Exp. Biol. 212:2835–43
    [Google Scholar]
  97. Norros V, Penttila R, Suominen M, Ovaskainen O 2012. Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121:961–74
    [Google Scholar]
  98. Norros V, Rannik U, Hussein T, Petaja T, Vesala T, Ovaskainen O 2014. Do small spores disperse further than large spores?. Ecology 95:1612–21
    [Google Scholar]
  99. Parguey-Leduc A, Janex-Favre M 1982. La paroi des asques chez les Pyrénomycètes: étude ultrastructurale. I. Les asques bituniqués typiques. Can. J. Bot. 60:1222–30
    [Google Scholar]
  100. Peay K, Bruns T, Kennedy P, Bergemann S, Garbelotto M 2007. A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol. Lett. 10:470–80
    [Google Scholar]
  101. Philibert A, Desprez-Loustau ML, Fabre B, Frey P, Halkett F et al. 2011. Predicting invasion success of forest pathogenic fungi from species traits. J. Appl. Ecol. 48:1381–90
    [Google Scholar]
  102. Pieuchot L, Lai J, Loh R, Leong F, Chiam K et al. 2015. Cellular subcompartments through cytoplasmic streaming. Dev. Cell 34:410–20
    [Google Scholar]
  103. Pliny the Elder 1634. The History of the World, Commonly Called the Naturall Historie of C. Plinius Secundus Vol. 2, transl. P Holland. London: A. Islip
    [Google Scholar]
  104. Plunkett B 1958. Translocation and pileus formation in Polyporus brumalis. Ann. Bot. 22:237–49
    [Google Scholar]
  105. Pringle A, Baker D, Platt J, Wares J, Latge J, Taylor JW 2005.a Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–99
    [Google Scholar]
  106. Pringle A, Brenner M, Fritz J, Roper M, Seminara A 2017. Reaching the wind: boundary layer escape as a constraint on ascomycete spore dispersal. The Fungal Community: Its Organization and Role in the Ecosystem J Dighton, JF White309–20 Boca Raton, FL: CRC. 4th ed.
    [Google Scholar]
  107. Pringle A, Patek S, Fischer M, Stolze J, Money N 2005.b The captured launch of a ballistospore. Mycologia 97:866–71
    [Google Scholar]
  108. Read N, Beckett A 1996. Ascus and ascospore morphogenesis. Mycol. Res. 100:1281–314
    [Google Scholar]
  109. Reid C, MacDonald H, Mann R, Marshall J, Latty T, Garnier S 2016. Decision-making without a brain: how an amoeboid organism solves the two-armed bandit. J. R. Soc. Interface 13:20160030
    [Google Scholar]
  110. Reynolds D 1981. Wall structure of a bitunicate ascus. Planta 98:244–57
    [Google Scholar]
  111. Riquelme M, Martínez-Núñez L 2016. Hyphal ontogeny in Neurospora crassa: a model organism for all seasons. F1000Research 5:2801
    [Google Scholar]
  112. Roper M, Ellison C, Taylor JW, Glass NL 2011. Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr. Biol. 21:R786–93
    [Google Scholar]
  113. Roper M, Lee CH, Hickey PC, Gladfelter A 2015. Life as a moving fluid: fate of cytoplasmic macromolecules in dynamic fungal syncytia. Curr. Opin. Microbiol. 26:116–22
    [Google Scholar]
  114. Roper M, Pepper R, Brenner M, Pringle A 2008. Explosively launched spores of ascomycete fungi have drag minimizing shapes. PNAS 105:20583
    [Google Scholar]
  115. Roper M, Seminara A, Bandi M, Cobb A, Dillard H, Pringle A 2010. Dispersal of fungal spores on a cooperatively generated wind. PNAS 107:17474
    [Google Scholar]
  116. Roper M, Simonin A, Hickey PC, Leeder A, Glass NL 2013. Nuclear dynamics in a fungal chimera. PNAS 110:12875–80
    [Google Scholar]
  117. Rossi V, Ponti I, Marinelli M, Giosue S, Bugiani R 2001. Environmental factors influencing the dispersal of Venturia inaequalis ascospores in the orchard air. J. Phytopathol. 149:11–19
    [Google Scholar]
  118. Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P 2002. A minimal system allowing tubulation with molecular motors pulling on giant liposomes. PNAS 99:5394–99
    [Google Scholar]
  119. Rowat AC, Jaalouk DE, Zwerger M, Ung WL, Eydelnant IA et al. 2013. Nuclear envelope composition determines the ability of neutrophil-type cells to passage through micron-scale constrictions. J. Biol. Chem. 288:8610–18
    [Google Scholar]
  120. Ruiz-Roldán MC, Köhli M, Roncero MIG, Philippsen P, Di Pietro A, Espeso EA 2010. Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum. Eukaryot. Cell 9:1216–24
    [Google Scholar]
  121. Saffman P 1960. Dispersion due to molecular diffusion and macroscopic mixing in flow through a network of capillaries. J. Fluid Mech. 7:194–208
    [Google Scholar]
  122. Savage D, Barbetti MJ, MacLeod WJ, Salam MU, Renton M 2013. Temporal patterns of ascospore release in Leptosphaeria maculans vary depending on geographic region and time of observation. Microb. Ecol. 65:584–92
    [Google Scholar]
  123. Schuchardt I, Aßmann D, Thines E, Schuberth C, Steinberg G 2005. Myosin-v, kinesin-1, and kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol. Biol. Cell 16:5191–201
    [Google Scholar]
  124. Schütte KH 1956. Translocation in the fungi. New Phytol. 55:164–82
    [Google Scholar]
  125. Seminara A, Fritz J, Brenner MP, Pringle A 2018. A universal growth limit for circular lichens. J. R. Soc. Interface 15:20180063
    [Google Scholar]
  126. Shahidzadeh-Bonn N, Rafai S, Azouni A, Bonn D 2006. Evaporating droplets. J. Fluid Mech. 549:307–13
    [Google Scholar]
  127. Sikhakolli U, Lopez-Giraldez F, Li N, Common R, Townsend J, Trail F 2012. Transcriptome analyses during fruiting body formation in Fusarium graminearum and F. verticillioides reflect species life history and ecology. Fungal Genet. Biol. 49:663–73
    [Google Scholar]
  128. Smith ML, Bruhn JN, Anderson JB 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–31
    [Google Scholar]
  129. Smith SE, Read DJ 2002. Mycorrhizal Symbiosis New York: Academic
    [Google Scholar]
  130. Smyth DR 2016. Helical growth in plant organs: mechanisms and significance. Development 143:3272–82
    [Google Scholar]
  131. Steinberg G 2007. Hyphal growth: a tale of motors, lipids, and the Spitzenkörper. Eukaryot. Cell 6:351–60
    [Google Scholar]
  132. Stiles W 1994. Principles of Plant Physiology New Delhi, India: Discovery
    [Google Scholar]
  133. Stolze-Rybczynski JL, Cui Y, Henry M, Stevens H, Davis D et al. 2009. Adaptation of the spore discharge mechanism in the Basidiomycota. PLOS ONE 4:e4163
    [Google Scholar]
  134. Tero A, Takagi S, Saigusa T, Ito K, Bebber DP et al. 2010. Rules for biologically inspired adaptive network design. Science 327:439–42
    [Google Scholar]
  135. Thomson DD, Wehmeier S, Byfield FJ, Janmey PA, Caballero-Lima D et al. 2014. Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae. Cell. Microbiol. 17:342–54
    [Google Scholar]
  136. Trail F, Common R 2000. Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92:130–38
    [Google Scholar]
  137. Trail F, Gaffoor I, Vogel S 2005. Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fusarium graminearum). Genet. Biol. 42:528–33
    [Google Scholar]
  138. Trail F, Seminara A 2014. The mechanism of ascus firing: merging biophysical and mycological viewpoints. Fungal Biol. Rev. 28:70–76
    [Google Scholar]
  139. Treiber M, Hennecke A, Helbing D 2000. Congested traffic states in empirical observations and microscopic simulations. Phys. Rev. E 62:1805–24
    [Google Scholar]
  140. Turner J, Webster J 1991. Mass and momentum transfer on the small scale: How do mushrooms shed their spores?. Chem. Eng. Sci. 46:1145–49
    [Google Scholar]
  141. Vogel S 2005. Living in a physical world II. The bio-ballistics of small projectiles. J. Biosci. 30:167
    [Google Scholar]
  142. Webster J, Davey R, Ingold C 1984. Origin of the liquid in Buller's drop. Trans. Br. Mycol. Soc. 83:524–27
    [Google Scholar]
  143. Webster J, Davey R, Smirnoff N, Fricke W, Hinde P et al. 1995. Mannitol and hexoses are components of Buller's drop. Mycol. Res. 99:833–38
    [Google Scholar]
  144. Webster J, Weber R 2007. Introduction to Fungi Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  145. Whitaker DL, Edwards J 2010. Sphagnum moss disperses spores with vortex rings. Science 329:406
    [Google Scholar]
  146. Wilson RA, Talbot NJ 2009. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol. 7:185–95
    [Google Scholar]
  147. Woronin M 1870. Zur Entwicklungsgeschichte des Ascobolus pulcherrimus Cr. und einiger Pezizen. Beiträge zur Morphologie und Physiologie der Pilze A de Bary, MS Woronin Frankfurt, Ger.: Christian Winter
    [Google Scholar]
  148. Xu N, Hu X, Xu W, Li X, Zhou L et al. 2017. Mushrooms as efficient solar steam-generation devices. Adv. Mater. 29:1606762
    [Google Scholar]
  149. Yafetto L, Carroll L, Cui Y, Davis DJ, Fischer MW et al. 2008. The fastest flights in nature: high-speed spore discharge mechanisms among fungi. PLOS ONE 3:e3237
    [Google Scholar]
  150. Zhang H, Elbaum-Garfinkle S, Langdon EM, Taylor N, Occhipinti P et al. 2015. RNA controls polyQ protein phase transitions. Mol. Cell 60:2220–30
    [Google Scholar]
/content/journals/10.1146/annurev-fluid-122316-045308
Loading
/content/journals/10.1146/annurev-fluid-122316-045308
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error