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Penetration of Hard Substrates by a Fungus Employing Enormous Turgor Pressures (Appressorium/Biodeterioration/Magnaporthe Gnsea/Plant Pathogen/Rice Blast) RICHARD J

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Penetration of Hard Substrates by a Fungus Employing Enormous Turgor Pressures (Appressorium/Biodeterioration/Magnaporthe Gnsea/Plant Pathogen/Rice Blast) RICHARD J Proc. Natd. Acad. Sci. USA Vol. 88, pp. 11281-11284, December 1991 Microbiology Penetration of hard substrates by a fungus employing enormous turgor pressures (appressorium/biodeterioration/Magnaporthe gnsea/plant pathogen/rice blast) RICHARD J. HOWARD*t, MARGARET A. FERRARI*, DAVID H. ROACHt, AND NICHOLAS P. MONEY§ *Central Research and Development, and tFibers, The DuPont Company, Wilmington, DE 19880-0402; and §Department of Biochemistry, Colorado State University, Fort Collins, CO 80523 Communicated by Arthur Kelman, September 20, 1991 (receivedfor review June 27, 1991) ABSTRACT Many fungal pathogens penetrate plant MATERIALS AND METHODS an The rice leaves from a specialized cell called appressorium. Organism and Growth Conditions. These studies were blast pathogen Magnaporthegnsea can also penetrate synthetic conducted with strain 042 (see ref. 8) of M. grisea (Hebert) surfaces such as poly(vinyl chloride). Previous experiments time requires an elevated appres- Barr, telomorph of Pyricularia grisea Sacc. (10). The have suggested that penetration course of infection-structure development in vitro has been sorial turgor pressure. In the present report we have used well documented and closely resembles development on the nonbiodegradable Mylar membranes, exhibiting a range of in that penetration is host (11, 12). When harvested and placed on a surface surface hardness, to test the proposition distilled water, conidia germinate in 1-3 hr to form germ driven by turgor. Reducing appressorial turgor by osmotic to form and are firmly stress inhibited penetration ofthese membranes. The size ofthe tubes. By 4 hr appressoria begin was a function of attached to the substratum. By 6-8 hr their structure appears turgor deficit required to inhibit penetration complete. Much later, from 20 to 240 hr depending upon the the surface hardness. Penetration of the hardest membranes substrate, a penetration peg emerges from the appressorium was inhibited by small decreases in appressorial turgor, while and penetrates the underlying surface. penetration ofthe softer membranes was sensitive only to large Substrates. We attempted to grow M. grisea on a number decreases in turgor. Similarly, penetration of the host surface of surfaces of different composition by adding droplets of was inhibited in a manner comparable to penetration of the aqueous conidial suspensions, as described previously (8). hardest Mylar membranes. Indirect measurements of turgor, Based on an earlier report (1) two different gold substrates obtained through osmotically induced collapse of appressoria, were tested: 10-gm-thick gold foil (Engelhard Industries, indicated that the infection apparatus can generate turgor Carteret, NJ), and cellophane membrane (8) sputter-coated pressures in excess of 8.0 MPa (80 bars). We conclude that to 100 nm of gold. Films of the following materials were also penetration of synthetic membranes, and host epidermal cells, tested: poly(methyl methacrylate) (Lucite), poly(tetrafluoro- is accomplished by application of the physical force derived ethylene) (Teflon; see ref. 11), a neutralized copolymer of from appressorial turgor. poly(ethylenemethacrylic acid) (Surlyn), a proprietary film made from the Kevlar polymerp-phenyleneterephthalamide, The mechanism of host surface penetration by plant patho- glass, and polyethylene (cut from PolyGloves, VWR Scien- genic fungi has been debated for nearly a century (1-6). The tific). All but the latter two were obtained from Robert R. potential role of extracellular enzymes, to facilitate perfora- Matheson, DuPont Central Research and Development. tion of the host cuticle or cell wall during fungal invasion, is The following six different Mylar films composed of poly- poorly understood (with one exception) due to the complex (ethylene terephthalate) fiber were also tested (Table 1). and ill-defined chemical nature of plant surfaces (7). On the Amorphous, as-cast, unoriented Mylar (designated sample other hand, an essential role for mechanical force during host 1), obtained from John R. Barkley, DuPont Electronics surface penetration has been proposed for the rice blast Department, Circleville Research Laboratory, Circleville, fungus Magnaporthe grisea (Hebert) Barr (8). This pathogen OH, was thermally crystallized to generate samples desig- produces unicellular infection structures, called appressoria, nated 2, 3, 5, and 6. Crystallizations were achieved by which adhere tightly to the host surface and produce slender annealing at temperatures between the glass transition (67°C) infection pegs that pierce the underlying cell wall. The cell and melting (280°C) temperatures of the polymer. The degree walls of appressoria contain a dense layer of pentaketide- of crystallinity and the density were controlled by the an- derived melanin whose presence is correlated with a build-up nealing temperature and the duration of heating (13-15). of appressorial turgor pressure (8) and is essential for pene- These modified Mylar samples were generated by John C. tration (8, 9). In this study, we have inhibited penetration by Coburn, DuPont Electronics, Wilmington, DE. An additional exposing appressoria to solutions of high osmotic pressure. Mylar substrate, obtained from Robert R. Matheson and This approach was used to reduce the hydrostatic pressure designated sample 4, was not treated thermally. The densities (or turgor) within the infection apparatus and to estimate the of all six Mylar substrates were determined by the density- magnitude of the turgor involved in penetration. Our results gradient technique (16). Crystallinities were calculated by offer unequivocal evidence for an extraordinary mechanical assuming amorphous and crystalline densities of 1.335 and component of the mechanism by which appressoria pene- 1.495 g/cm3, respectively (17, 18). Surface hardness was trate hard surfaces, but do not exclude a role in host pene- determined by Vicker's indentation techniques (19) at loads tration for some other factor such as extracellular en- ranging from 2 to 20 g. The resulting impressions were imaged zymes. with differential interference-contrast optics and a low-light video camera and were measured from a video screen. Hardness, expressed in MPa, was calculated as H = P/2a2, The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 11281 Downloaded by guest on September 30, 2021 11282 Microbiology: Howard et al. Proc. Natl. Acad. Sci. USA 88 (1991) Table 1. Mylar [poly(ethylene terephthalate)] films, numbered appressoria forming pegs during incubation was determined 1-6, used as substrates for appressorium formation either by examining intact appressoria by light microscopy or and penetration by sonicating the specimens for 5 min, sputter coating them Tmnew, tanneal Density, xtl, Hardness, with gold, and then examining the appressorial remnants with Sample 0C hr g/cm3 % MPa scanning EM (8). This experiment was repeated twice, with 4 samples of 100 appressoria counted by each technique for 1 1.345 6.1 140 each experiment (1600 appressoria total). No significant 2 90 50 1.374 24.1 173 difference was found between data obtained by the two 3 130 70 1.379 27.6 180 methods. 4 - ND ND 200 Inhibition of Penetration. Appressoria were allowed to 5 180 50 1.393 36.3 240 form in water droplets for 12-18 hr on the surface of Mylar 6 240 50 1.405 43.6 250 membranes or of detached newly expanded third foliar Sample 1 was heated at various temperatures (T0nw) and for leaves of rice cultivar M201. The water droplets were then various times Qna) to yield samples 2, 3, 5, and 6. Sample 4 was replaced with PEG solutions of varying osmotic pressure. obtained separately. Density, crystallinity (Xtl), and hardness were Penetration of the Mylars and rice leaves was assessed after determined as described in the text. ND, not determined. 13 days and 48 hr, respectively. Solutions of PEG-8000 (Sigma, lot 49F-0383) were pre- where P is the load and 2a is the hardness impression pared by dissolving 2.0-13.0 g in 10.0 ml ofdistilled deionized diagonal. water. An average molecular weight of 8410 was determined Ceil Wail Pore Measurement. Pore size of the appressorial in tetrahydrofuran at 350C by R. E. Davis (DuPont Polymer wall was estimated with a solute exclusion technique (20, 21). Products) and used to calculate molarity (M). The osmotic Briefly, appressoria were incubated for 15 min in concen- pressure H of each solution was calculated with the formula trated solutions of poly(ethylene glycols) (PEGs) of different H = a(M) + ,3(M2), where a and j3 were derived by average molecular weights and were screened for plasmolysis interpolation from the values given by Money (24). and cytorrhysis (collapse). Plasmolysis occurs only when the solute molecule can diffuse through the pores in the cell wall, RESULTS whereas cytorrhysis is evidence of exclusion. Therefore, the Selection ofSubstrates. M. grisea formed appressoria on all diameter of the pores in the wall is estimated by the size of surfaces tested except gold foil, gold-coated cellophane, and the smallest excluded molecules. These measurements were glass. Teflon was the only surface never penetrated. The conducted on melanized appressoria and on unmelanized Mylar films, however, offered a series of chemically homo- appressoria formed in the presence of tricyclazole (8). geneous surfaces
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