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Impact of the Exodermis on Infection of Roots by Fusarium Culmorum

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Impact of the Exodermis on Infection of Roots by Fusarium Culmorum Plant and Soil 167: 121-126, 1994. @ 1994 KluwerAcademicPublishers. Printedin the Netherlands. Impact of the exodermis on infection of roots by Fusarium culmorum Susan A. Kamula, Carol A. Peterson and Colin I. Mayfield Department of Biology, University of Waterloo, Waterloo, ON, Canada N2L 3G1 Key words: Casparian bands, exodermis, Fusarium culmorum, hypodermis, passage cells, short cells, suberin lamellae Abstract Patterns of infection with Fusarium culmorum (W G Smith) Saccardo were observed in seedling roots of barley (Hordeum vulgare L.), wheat (Triticum aestivum L.), maize (Zea mays L.) and asparagus (Asparagus officinalis L). Apical regions of the main roots were not infected. Since penetration into the root occurred several days after inoculation and the roots were growing during the experiment, these regions had apparently not been in existence long enough to be infected. In older regions of barley, wheat and asparagus, hyphae entered through the tips of lateral roots. In barley and wheat, which had not developed any suberin lamellae in their subepidermal layer, infection occurred randomly over the remainder of the root. In maize, the fungus penetrated the epidermis at many sites but did not breach the exodermis in which all cells possessed both Casparian bands and suberin lamellae. Maize roots, therefore, sustained only minimal infections. In asparagus, the fungus grew through the short (passage) cells but never the long cells of the exodermis. In doing so, it penetrated cells possessing Casparian bands but lacking suberin lamellae. The results support the hypothesis that suberin lamellae provide effective barriers to the growth of F. culmorum hyphae. Introduction guson and Clarkson, 1975; Peterson, et al., 1982). The exodermis of young roots of asparagus, on the oth- Deposition of suberin in plant cell walls is known to er hand, is dimorphic and consists of long and short deter fungal infection (Kolattukudy, 1984). Thus, the cells (Kroemer, 1903). At maturity, the long cells and suberin in the Casparian bands and suberin lamellae of possibly some of the short cells have both Casparian the exodermis, a specialized layer in the roots of many bands and suberin lamellae but the remainder of the angiosperm species (Perumalla et al., 1990; Peterson short cells have only Casparian bands (Hussey, 1982; and Perumalla, 1990), may play a role in preventing Kamula, 1991). Inclusion of a species with a dimorphic or delaying fungal invasion. Since the exodermis is exodermis made it possible to test the effects of Cas- the outermost layer of the cortex, it is well positioned parian bands and suberin lamellae on fungal growth to protect a large area of the organ. To determine the separately. potential importance of the exodermis as an antifun- gal layer, we compared the pattern of infection of four species by pathogen Fusarium culmorum (W G Smith) Materials and methods Saccardo. According to Perumalla et al. (1990), barley (Hordeum vulgare L.) and wheat (Triticum aestivum Caryopses of barley (Hordeum vulgare L.) and wheat L.) have nonexodermal roots. Maize (Zea mays L.) (Triticum aestivum L.) were purchased from Carolina and asparagus (Asparagus officinalis L.) have exoder- Biological Supply, Burlington, NC, USA ; caryopses mal roots (Peterson et al., 1982; Peterson and Peru- of maize (Zea mays L. cv. Seneca Chief) and seeds of malla, 1990). The exodermis of maize is similar, com- asparagus (Asparagus officinalis L. var. Mary Wash- prised of cells of uniform length and structure (Kroe- ington) were obtained from Ontario Seed Company, mer, 1903). At maturity, all cells of the exodermis Ltd., Waterloo, ON, Canada. All propagules were sur- have both Casparian bands and suberin lamellae (Fer- face sterilized in 5.2% sodium hypochiorite (commer- 122 cial Javex bleach) for five min and soaked overnight in mounted on microscope slides with props at the ends cold, running tap water. Plants were grown in vermi- of the coverslips to prevent squashing the specimens. culite, initially watered to saturation and subsequently To determine the location of suberin lamella develop- every 2-4 d with tap water, in a Conviron PGW-36 ment, cross sections were taken near the apices of exo- growth chamber (Controlled Environment, Winnipeg, dermal species and stained with Sudan red 7B which MN, Canada) at 25 °C during 16 h light (intensity 215 partitions into lipids, imparting a red colour to them /rE s -1 m -2) and 23 °C during 8 h darkness, relative (Brundrett et al., 1991). The experiment was repeated humidity 75-85%. Maize, barley and wheat grown for three times. 5 d and asparagus grown for 21 d were used in the All experimental specimens were observed with a experiments. Zeiss Axiophot microscope. Colour photographs were A culture of Fusarium culmorum (W.G. Smith) taken on Kodak Ektachrome 200 ISO, 35 mm slide Saccardo was provided by Dr Robert Hall, Department film, black and white on Ilford Pan F 50 ISO, 35 mm of Environmental Biology, University of Guelph, ON, negative film. Black and white prints were made from Canada, who had isolated it from the crown of a winter black and white negative film or from internegatives wheat plant in Elora, ON, Canada. The fungus was made from colour slides using Ilford Pan F 50 ISO, 35 grown on potato-dextrose agar (Difco Laboratories, mm negative film. Detroit, MI, USA) at room temperature in a dimly lit area for two months. A spore suspension was prepared by flooding the mycelium with sterile, distilled water Results and adjusting the volume to give 2 x 10s spores mL- 1. To begin an experiment, seedlings were gently No signs of contamination or infection were appar- uprooted and their root systems washed and laid hor- ent on control roots. The distinctive macroconidia of izontally in large, moist, sterile chambers. The pri- Fusarium culmorum were clinging to the surfaces of mary roots of each species were inoculated with E all treated roots and the majority of the conidia had ger- culmorum by pipetting 2 mL of the spore suspen- minated within 3 d. By 7 days, copious hyphae were sion over them. This resulted in an inoculum ranging present on the surfaces of the roots and were beginning between 14 and 38 spores mm -I root length. Roots to invade them. Penetration sites were at midlength and which served as controls were placed in similar sur- more proximal regions of the roots, never in the api- roundings and treated with water. The chambers were cal regions. Several distinct patterns of infection were covered with aluminum foil so that the roots were in discerned. darkness and the shoots emerged from the side. The In barley and wheat, infection occurred randomly containers were incubated at room temperature and in the midlength to basal regions of the roots (average the contents were wetted with sterile distilled water total root length about 170 mm). Hyphae grew through as necessary to maintain a moist environment around epidermal cells ( Fig. 1) and subsequently many runner, the roots. To determine the time course of infection, branched and coiled hyphae proliferated throughout three seedlings of each species were inoculated as the cortex (Fig. 2). Infection also occurred in some described above and individual roots were harvest- young lateral roots, often through their root caps (Fig. ed 0.5, 3, 7, 9, 14 and 21 d later. This experiment 3). Occasionally, black staining of the host tissue near was repeated three times. A further comparison of the an infection site was observed (Fig. 1) indicating that infection patterns in the four plant species was made suberin and/or lignin had been deposited as a wound by inoculating three seedlings of each and harvesting response. them after 21 d. Entire roots were analyzed from both In maize roots, the infection process was arrested at experiments. They were cut into segments 10-30 mm the exodermis. This layer became mature 40 mm from long which were cleared and stained with chlorazol the main root tip and very close to the tips of the later- black E (CBE) according to the method of Brundrett et als. Hyphae frequently penetrated the epidermis in mid al. (1984) with the following modifications. An auto- and basal regions of the main roots, as well as in the clave was used (20 rain at 121" C) for both cleating and young laterals. However, growth did not proceed into staining steps, the concentration of CBE was 0.03%, the cortex (Fig. 4). From 9 to 21 days after inocula- and the roots were mounted in 70% glycerin. With tion, masses of hyphae had formed in some epidermal this procedure, fungal walls, lignified plant walls and cells but the fungus had still not penetrated further into Casparian bands stained black. Root segments were the root (Fig. 5). Furthermore, hyphae did not grow 123 through the tips of the lateral roots. The pathogen, invasion in zones with an immature exodermis would therefore, produced only a minimal infection of the be anticipated. root, i.e. in the epidermis. A comparison of the infection patterns of various The exodermis of asparagus roots also influ- species indicates that the exodermis plays a role in enced the infection process. In these roots, Caspar- the invasion process and that the type of exodermis ian bands and suberin lamellae had formed 10 mm is critical for the outcome. Specifically, the failure of from the main root apex. The dimorphic nature of the fungus to penetrate the uniform exodermal cells the exodermis was apparent in clearings of control of maize and the long cells of asparagus indicates roots (Fig. 6). Fungal invasion of the root proceed- that suberin lamellae were the structures responsible ed through the epidermis overlying the short cells for prevention of its ingress. The Casparian band had and then through the short cells themselves, form- no such effect, since it was present in the short cells ing hyphal coils (Fig.
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