Biomechanics of Invasive Hyphal Growth

Filamentous fungi penetrate diverse solid substrates, including plant and animal tissues, by a process called invasive hyphal growth. Extending hyphae overcome the resistance of their food sources by the secretion of lytic enzymes and the exertion of mechanical force. The forces utilized for invasive growth are derived from turgor pressure and are regulated through loosening of the apical cell wall of the hypha. This chapter explains how hyphae are pressurized and how they apply this pressure during invasive growth. Recent experimental work is discussed, including the use of miniature strain gauges and laser tweezers to measure the forces exerted by hyphae, and information on hyphal mechanics obtained by atomic force microscopy. Other topics in this chapter include current thinking on the role of secreted enzymes and the cytoskeleton in the invasive process, and the remarkable mechanism of leaf penetration by melanized appressoria.

[1]  A. D. Bary Morphologie und physiologie der pilze, flechten und myxomyceten , 1866 .

[2]  Bowen,et al.  Direct Quantification of Aspergillus niger Spore Adhesion in Liquid Using an Atomic Force Microscope. , 2000, Journal of colloid and interface science.

[3]  S. Jackson Do hyphae pulse as they grow? , 2001, The New phytologist.

[4]  Katja Sterflinger,et al.  Dematiaceous fungi as a major agent for biopitting on Mediterranean marbles and limestones , 1997 .

[5]  H. Busscher,et al.  How a fungus escapes the water to grow into the air , 1999, Current Biology.

[6]  M. Bonham,et al.  The interrelationships of actin and hyphal tip growth in the ascomycete Geotrichum candidum. , 2003, Fungal genetics and biology : FG & B.

[7]  R. Howard,et al.  Penetration of hard substrates by a fungus employing enormous turgor pressures. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  N. Money To perforate a leaf of grass. , 1999, Fungal genetics and biology : FG & B.

[9]  J. Ortega Governing equations for plant cell growth , 1990 .

[10]  A. Harris,et al.  Silicone rubber substrata: a new wrinkle in the study of cell locomotion. , 1980, Science.

[11]  K. Williams,et al.  Infection of Meloidogyne javanica by Paecilomyces lilacinus , 1999 .

[12]  J. P. Ravishankar,et al.  Biomechanics of stipe elongation in the basidiomycete Coprinopsis cinerea. , 2005, Mycological research.

[13]  A. Geitmann,et al.  The cytoskeleton in plant and fungal cell tip growth , 2000, Journal of microscopy.

[14]  R. Howard,et al.  Confirmation of a Link between Fungal Pigmentation, Turgor Pressure, and Pathogenicity Using a New Method of Turgor Measurement , 1996 .

[15]  R. Lovitt,et al.  Direct quantification of Aspergillus niger spore adhesion to mica in air using an atomic force microscope , 2000 .

[16]  N. Talbot On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. , 2003, Annual review of microbiology.

[17]  N. Talbot,et al.  The molecular biology of appressorium turgor generation by the rice blast fungus Magnaporthe grisea. , 2005, Biochemical Society transactions.

[18]  Gupta,et al.  Actin Disruption by Latrunculin B Causes Turgor-Related Changes in Tip Growth of Saprolegnia ferax Hyphae , 1997, Fungal genetics and biology : FG & B.

[19]  T. Hill,et al.  CORRELATION BETWEEN ENDOGLUCANASE SECRETION AND CELL WALL STRENGTH IN OOMYCETE HYPHAE : IMPLICATIONS FOR GROWTH AND MORPHOGENESIS , 1997 .

[20]  F. Harold,et al.  Molecules into Cells: Specifying Spatial Architecture , 2005, Microbiology and Molecular Biology Reviews.

[21]  M. Plamann,et al.  Cytoskeleton and motor proteins in filamentous fungi. , 2003, Current opinion in microbiology.

[22]  N. P. Money Measurement of hyphal turgor , 1990 .

[23]  L. Vidali,et al.  Polarized cell growth in higher plants. , 2001, Annual review of cell and developmental biology.

[24]  D. L. Taylor,et al.  Traction forces of cytokinesis measured with optically modified elastic substrata , 1997, Nature.

[25]  Money Mechanism linking cellular pigmentation and pathogenicity in rice blast disease , 1997, Fungal genetics and biology : FG & B.

[26]  N. P. Money Mechanics of Invasive Fungal Growth and the Significance of Turgor in Plant Infection , 1998 .

[27]  František Baluška,et al.  Actin: A Dynamic Framework for Multiple Plant Cell Functions , 2000, Developments in Plant and Soil Sciences.

[28]  A. Brown,et al.  Disruption of each of the secreted aspartyl proteinase genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence , 1997, Infection and immunity.

[29]  Jochen Arlt,et al.  Measuring fungal growth forces with optical tweezers , 2005, SPIE Optics + Photonics.

[30]  T. Dahms,et al.  Surface ultrastructure and elasticity in growing tips and mature regions of Aspergillus hyphae describe wall maturation. , 2005, Microbiology.

[31]  R. Howard,et al.  Role of melanin in appressorium function , 1989 .

[32]  F. Harold,et al.  Growth and morphogenesis inSaprolegnia ferax: Is turgor required? , 1996, Protoplasma.

[33]  F. Harold,et al.  Two water molds can grow without measurable turgor pressure , 1993, Planta.

[34]  G. Gierz,et al.  Mapping the growth of fungal hyphae: orthogonal cell wall expansion during tip growth and the role of turgor. , 2000, Biophysical journal.

[35]  H. Wösten,et al.  Structural proteins involved in emergence of microbial aerial hyphae. , 1999, Fungal genetics and biology : FG & B.

[36]  A. Garrill,et al.  Actin microfilaments in fungi , 2006 .

[37]  N. Talbot,et al.  Surface attachment and pre-penetration stage development by plant pathogenic fungi. , 2001, Annual review of phytopathology.

[38]  L. Mahadevan,et al.  Non-equilibration of hydrostatic pressure in blebbing cells , 2005, Nature.

[39]  N. Talbot,et al.  MAP Kinase and Protein Kinase A–Dependent Mobilization of Triacylglycerol and Glycogen during Appressorium Turgor Generation by Magnaporthe grisea , 2000, Plant Cell.

[40]  S. Werner,et al.  The role of fungal appressoria in plant infection. , 2000, Microbes and infection.

[41]  L. Millward,et al.  Biomechanical interaction between hyphae of two Pythium species (Oomycota) and host tissues. , 2002, Fungal genetics and biology : FG & B.

[42]  N. Money,et al.  Turgor pressure and the mechanics of fungal penetration , 1995 .

[43]  N. Gow,et al.  A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence , 1997, Infection and immunity.

[44]  F. Chumley,et al.  A Mechanism for Surface Attachment in Spores of a Plant Pathogenic Fungus , 1988, Science.

[45]  F. Harold,et al.  Extension growth of the water mold Achlya: interplay of turgor and wall strength. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Howard Breaching the Outer Barriers — Cuticle and Cell Wall Penetration , 1997 .

[47]  C. Bracker,et al.  Pulsed growth of fungal hyphal tips. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[48]  R. Bojko,et al.  Deformation of Stomatal Guard Cell Lips and Microfabricated Artificial Topographies during Appressorium Formation by Uromyces , 1993 .

[49]  H. Deising,et al.  Infection structures of fungal plant pathogens - a cytological and physiological evaluation. , 1993, The New phytologist.

[50]  D. Callaham,et al.  Tip-localized calcium entry fluctuates during pollen tube growth. , 1996, Developmental biology.

[51]  F. Schuren,et al.  Research letterTargeted mutation of the SC3 hydrophobin gene of Schizophyllum commune affects formation of aerial hyphae , 1996 .

[52]  J. Walton Deconstructing the Cell Wall , 1994, Plant physiology.

[53]  E. S. Castle Discontinuous growth of single plant cells measured at short intervals, and the theory of intussusception , 1940 .

[54]  N. Talbot,et al.  Advances in Rice Blast Research , 2000, Developments in Plant Pathology.

[55]  P. Leiderer,et al.  Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus , 1999, Science.

[56]  N. Money,et al.  Mechanics of solid tissue invasion by the mammalian pathogen Pythium insidiosum. , 2001, Fungal genetics and biology : FG & B.

[57]  T. Camesano,et al.  Adhesion of Aureobasidium pullulans is controlled by uronic acid based polymers and pullulan. , 2005, Biomacromolecules.

[58]  D. J. Davis,et al.  Relationship between temperature optima and secreted protease activities of three Pythium species and pathogenicity toward plant and animal hosts. , 2006, Mycological research.

[59]  Frank H. J. Schuren,et al.  Targeted mutation of the SC3 hydrophobin gene of Schizophyllum commune affects formation of aerial hyphae , 1996 .

[60]  N. P. Money The fungal dining habit: a biomechanical perspective , 2004 .

[61]  A. G. Klein,et al.  Tip growth in plant cells may be amoeboid and not generated by turgor pressure , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  S Chien,et al.  Locomotion forces generated by a polymorphonuclear leukocyte. , 1992, Biophysical journal.

[63]  M. Hahn,et al.  Molecular and functional characterization of a secreted lipase from Botrytis cinerea. , 2005, Molecular plant pathology.

[64]  N. Talbot,et al.  Glycerol generates turgor in rice blast , 1997, Nature.

[65]  A. Mitchell Dimorphism and virulence in Candida albicans. , 1998, Current opinion in microbiology.

[66]  J. Sweigard,et al.  Cytochalasin A inhibits spore germination and hyphal tip growth inGilbertella persicaria , 1980 .

[67]  Christopher M. Davis,et al.  Pulses in turgor pressure and water potential : resolving the mechanics of hyphal growth , 1999 .

[68]  R. Lew,et al.  Turgor regulation in hyphal organisms. , 2004, Fungal genetics and biology : FG & B.

[69]  N. P. Money On the origin and functions of hyphal walls and turgor pressure , 1999 .

[70]  N. P. Money,et al.  Invasive hyphal growth in Wangiella dermatitidis is induced by stab inoculation and shows dependence upon melanin biosynthesis. , 1999, Fungal genetics and biology : FG & B.

[71]  H. Yamamoto,et al.  Chemical Composition fo the Glue From Appressoria of Magnaporthe grisea. , 1998, Bioscience, biotechnology, and biochemistry.

[72]  N. J. Tonukari,et al.  Cell Wall Degrading Enzymes in HST-Producing Fungal Pathogens , 1998 .

[73]  M. Olsson,et al.  Rock-eating fungi , 1997, Nature.

[74]  A. Geitmann Plant and fungal cytomechanics: quantifying and modeling cellular architecture 1 , 2006 .

[75]  N. P. Money Wishful Thinking of Turgor Revisited: The Mechanics of Fungal Growth , 1997 .

[76]  E. Steudle,et al.  Turgor Changes in Morchella esculenta during Translocation and Sclerotial Formation , 1995 .

[77]  D. Moore,et al.  Evolutionary Biology of the Fungi , 1989 .

[78]  G. Steinberg,et al.  Mechanisms of hyphal tip growth: tube dwelling amebae revisited. , 1999, Fungal genetics and biology : FG & B.

[79]  A. Geitmann,et al.  Cell Biology of Plant and Fungal Tip Growth—Getting to the Point , 2000, Plant Cell.

[80]  O. Yoder,et al.  Molecular Genetics of Host-Specific Toxins in Plant Disease , 1998, Developments in Plant Pathology.

[81]  P. Solomon,et al.  The nutrient supply of pathogenic fungi; a fertile field for study. , 2003, Molecular plant pathology.

[82]  S. Gurr,et al.  The roles of cellulase enzymes and mechanical force in host penetration by Erysiphe graminis f.sp.hordei , 1999 .

[83]  H. Deising,et al.  Genetics of Phytopathology: Fungal Morphogenesis and Plant Infection , 2004 .

[84]  I. Heath Organization and Functions of Actin in Hyphal Tip Growth , 2000 .

[85]  N. Talbot,et al.  The vacuole as central element of the lytic system and sink for lipid droplets in maturing appressoria ofMagnaporthe grisea , 2007, Protoplasma.

[86]  N. Money,et al.  Biochemical and Biomechanical Aspects of Appressorial Development in Magnaporthe Grisea , 2000 .

[87]  I. Heath,et al.  Studies on Saprolegnia ferax suggest the general importance of the cytoplasm in determining hyphal morphology. , 1996 .

[88]  W. Knogge Fungal Infection of Plants. , 1996, The Plant cell.

[89]  Jaideep Mathur,et al.  Local interactions shape plant cells. , 2006, Current opinion in cell biology.

[90]  Alain Goriely,et al.  Estimates of biomechanical forces in Magnaporthe grisea. , 2006, Mycological research.

[91]  G. S. Hoog Ecology and evolution of black yeasts and their relatives , 1999 .

[92]  J. Lockhart An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[93]  Steven Vogel,et al.  Life's Devices , 2020 .

[94]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[95]  R. Howard,et al.  Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. , 1996, Annual review of microbiology.

[96]  Gabrielle M. Christenhusz,et al.  Invasive hyphal growth: an F-actin depleted zone is associated with invasive hyphae of the oomycetes Achlya bisexualis and Phytophthora cinnamomi. , 2006, Fungal genetics and biology : FG & B.

[97]  J. P. Ravishankar,et al.  Biomechanical evidence for convergent evolution of the invasive growth process among fungi and oomycete water molds. , 2004, Fungal genetics and biology : FG & B.

[98]  R. Lew,et al.  Time series analysis demonstrates the absence of pulsatile hyphal growth. , 2003, Microbiology.