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Enhancement of Sporulation in Species of Bipolaris, Curvularia, Drechslera, and Exserohilum by Growth on Cellulose-Containing Substrates

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Enhancement of Sporulation in Species of Bipolaris, Curvularia, Drechslera, and Exserohilum by Growth on Cellulose-Containing Substrates Mycopathologia (2006) 162: 133–140 Ó Springer 2006 DOI 10.1007/s11046-006-0043-8 Enhancement of sporulation in species of Bipolaris, Curvularia, Drechslera, and Exserohilum by growth on cellulose-containing substrates Robert G. Pratt U.S. Department of Agriculture, Agricultural Research Service, Waste Management and Forage Research Unit, 5367Mississippi State, MS, 39762, USA Received 23 December 2005; accepted 24 May 2006 Abstract Nine species of Bipolaris, Curvularia, Drechslera, and Exserohilum were compared for sporulation on agar media and for enhancement of sporulation by growth on four cellulose-containing substrates (index card, filter paper, cheesecloth, cotton fabric). On two natural and one synthetic agar media, sporulation varied from profuse to nonexistent among three isolates of each species. Growth of all species on cellulose substrates resulted in large and significant increases in sporulation. Growth on index card pieces often provided the greatest increases, but no single substrate was superior for all species, and significant sub- strate  isolate interactions were observed within species. Overlay of filter paper onto whole colonies in agar plates resulted in 2 to 18-fold increases in sporulation for eight of nine species and production of spores in sufficient quantity for most experimental purposes. Overlay of soil dilution plates with filter paper to promote sporulation of colonies enabled detection of B. spicifera, B. hawaiiensis, C. lunata, and E. rostratum at relatively low population levels ( £ 1.3  103 colony-forming units per gram of soil) in samples of a naturally infested soil. Results indicate that enhancement of sporulation by growth of species of Bipolaris, Curvularia, Drechslera, and Exserohilum on cellulose substrates may facilitate (i) their identifi- cation in culture, (ii) production of spores at relatively high concentrations, and (iii) detection and enu- meration of these fungi in soil. Key words: Bipolaris, cellulose substrates, Curvularia, Drechslera, Exserohilum, sporulation Introduction species occur together and infect host tissues simultaneously [4–7]. On most susceptible grasses, Species of Bipolaris, Drechslera, Exserohilum, and these pathogens primarily cause foliar lesions and Curvularia constitute a group of taxonomically blights [5, 8, 9], but infection also may extend into related and ecologically similar deuteromycetes crowns, roots, stolons, and rhizomes to cause root (mitosporic fungi) that are important plant rot, dieback, and melting out of stands [5, 8–10]. pathogens or common saprophytes throughout the With B. sorokiniana (Sacc.) Shoemaker on small world. The first three of these genera were segre- grains, initial infection and subsequent pathogen- gated from Helminthosporium in several revisions esis may occur entirely below ground [11, 14]. from 1930 to 1974, and some species of Bipolaris B. sorokiniana, B. spicifera (Banier) Subramanian, and Curvularia share the same teleomorph [1, 2]. C. geniculata (Tracy & Earle) Boedijn, and C. lu- As pathogens, species of the four genera are most nata (Wakk.) Boedijn also have been isolated from important on a wide range of grasses, but many agricultural and natural soils under diverse plant dicots also are infected [1–3]. Often multiple communities throughout the world [1], but 134 estimates of soil population levels have been pre- (Reade) Honey, but strong differences in isolate sented only for B. sorokiniana [1, 13, 14]. responses were observed [19]. Booth [20] recom- Genera and species of dematiaceous hypho- mended media containing carboxymethycellulose mycetes are identified largely on the basis of and pure cellulose lens paper for stimulating conidial morphology and hosts of origin [2, 9]. conidium formation by Fusarium spp. Similarly, Conidial features used in taxonomy include size, growth of a nonsporulating fungus in a medium shape, color, wall thickness, septation, and the with cellulose as the sole carbon source induced presence of protruded hila in detached conidia. sporulation and enabled its re-identification as a Specific morphological features for the practical Fusarium sp. [21]. Although numerous cellulose- identification of most species included in this study containing substrates have been used to obtain were recently summarized [7]. Molecular methods sporulation by species of Bipolaris, Curvularia, have been used to study relationships between Drechslera, and Exserohilum [1, 2, 5, 13], we are isolates and races of some species within these four not aware of previous studies that have specifically genera [e.g., 15], but such methods have not been evaluated enhancement of sporulation by growth used to identify species or evaluate taxonomic on cellulose substrates for species of these genera. relationships. In preliminary experiments, it was observed Induction of sporulation by species of Bipo- that for several species of Bipolaris and Curvularia, laris, Curvularia, Drechslera, and Exserohilum is sporulation on pieces of paper index card placed essential for their identification [2, 9]. In addition, on growing colonies was greatly increased over large numbers of spores often are required for that present in the surrounding agar. It was not experimental purposes. As noted by Sivanesan [2], known whether such enhanced sporulation also sporulation by species of these genera is usually occurs in other species of the four genera or when abundant on naturally infected plant material, but they are grown on other cellulose substrates. some species may cease to sporulate after they are Therefore, this study was undertaken to fulfill four isolated and grown in pure culture. He recom- objectives: (i) to compare sporulation of nine mended growing cultures on Sach’s agar with species of Bipolaris, Curvularia, Drechslera, and sterilized plant material (commonly rice and barley Exserohilum on agar media, (ii) to evaluate grains, or leaves of maize and other plants) applied enhancement of sporulation by these fungi fol- to the agar. Domsch et al. [1] and Couch [8] also lowing growth on four cellulose substrates, (iii) to listed agar media that have been used to obtain evaluate growth on cellulose substrates for pro- sporulation by individual species. Miles and Wil- duction of large quantities of spores for experi- coxson [16] obtained abundant sporulation by two mental purposes; and (iv) to determine whether species of Bipolaris and Drechslera on a mixture of enhanced sporulation on a cellulose substrate can agar and natural substrates, and Pratt [5] obtained help to isolate and identify these fungi from soil. A satisfactory sporulation by species of Bipolaris, preliminary report has been presented [22]. Curvularia, and Exserohilum on infested wheat and oat grain. With these few exceptions, however, the effectiveness of media, substrates, or techniques Materials and methods for inducing or enhancing sporulation have not been demonstrated across a range of species in Sources, storage, and growth of isolates these four genera. Growth on cellulose substrates has been Three isolates each of Bipolaris cynodontis reported to enhance asexual sporulation by diverse (Marig.) Shoemaker, B. hawaiiensis (Ellis) Uchida imperfect fungi. Application of filter paper to the & Aragaki, B. sorokiniana (Sacc. Ex Sorok.) surfaces of agar media increased formation of Shoemaker, B. spicifera (Banier) Subr., B. stenos- pycnidia and conidia by Pyrenochaeta (Phoma) pila (Drechs.) Shoemaker, Curvularia geniculata terrestris (E.M. Hans.) Gorenz, J.C. Walker, and (Tracy & Earle) Boedijn, C. lunata (Wakk.) Bo- R.H. Larson [17] and Macrophomina phaseolina edijn and Exserohilum rostratum (Drechs.) Leon- (Tassi) Goid. [18]. Application of cellulose acetate ard & Suggs were obtained by the author in recent membranes to agar surfaces increased conidium years by direct transfer of individual spores from production by Monilinia vaccinii-corymbosi naturally infected leaves of bermudagrass 135 (Cynodon dactylon [L.] Pers.) in Mississippi as experiment, three randomized complete blocks of described [5, 6, 23]. Three isolates of Drechslera fifteen plates (5 substrates  3 isolates) were sealed dictyoides (Drechs.) Shoemaker were obtained by in plastic bags and incubated under growth lights the author in a similar manner from foliar lesions for 10 days. Each substrate piece then was on annual ryegrass (Lolium multiflorum Lam.) in removed to a 10 ml vial containing 0.25, 0.5, 1, 2, Mississippi in 2002. All isolates were stored in or 8 ml of 0.1% water agar (amount constant for infested, dried wheat and oat grain at 10 °C [5], each species) and agitated for 15 s with a micro- and kernels were plated on Difco cornmeal agar spatula to disperse spores. Substrate pieces were (CMA) to generate colonies. Growing colonies removed with a forceps from small quantities of were maintained by serial transfers on CMA. suspension, or larger quantities were poured through double-layer cheesecloth, and 0.05 ml of Sporulation on agar media spore suspension was deposited in a droplet on the surface of water agar. The total number of spores Isolates were transferred to edges of Difco potato in one droplet from each suspension was counted dextrose agar (PDA), CMA, and Bilay’s synthetic at 100 after liquid was absorbed into agar. medium [20] in small (3.5 cm) plastic plates and For each fungal species, data were compared grown for 10–14 days at 24–26 °C under plant by ANOVA of a 3 (isolates)  5 (substrates) fac- growth lights [5] on a 12-h photoperiod. A single torial experiment, and sources of variation
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