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Distribution of Acremonium Coenophialum in Developingseedlings

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Distribution of Acremonium Coenophialum in Developingseedlings AN ABSTRACT OF THE THESIS OF Kathy L. Cook for the degree of Master of Science in Botany and Plant Pathology presented onDecember 16, 1987 . Title: Distribution of Acremonium coenophialumin Developing Seedlings and Inflorescences ofFestuca arundinacea Redacted for privacy Abstract approved: Rona Welty Acremonium coenophialum isan endophytic fungus which infects the reproductive andvegetative tissue of tall fescue. Interest in this fungus was sparked byresearch which linked itspresence in tall fescue with reduced weightgains and alkaloid-like poisoning in cattle. Incomplete informationwas available on the endophyte's life or disease cycle withinthe host grass. This current investigation traces the progressionof A. coenophialum during plant development. Inflorescences of mature plants, in additionto seedlings, were histologicallyexamined for the presence of the endophyte. The fungus grows from shoot apicesinto immature inflorescences and, eventually,into mature seed. From infected seeds, A. coenophialumgrows into seedlings and occupies the shoot meristems of the plant. In contrast to previous information,the fungus invades the shootprimordia before seed germination, is capable of growing in roots,and is found inter/intracellularly. Distribution of Acremonium coenophialum inDeveloping Seedlings and Inflorescences of Festuca arundinacea by Kathy L. Cook A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Master of Science Completed December 16, 1987 Commencement June 1988 APPROVED: Redacted for privacy Professor of Botany Plant Pathology in charge of major Redacted for privacy Head of Department of Botany and Plant Pathology Redacted for privacy Dean of Graduat School Date thesis is presented December 16, 1987 Typed by Dianne Simpson for Kathy L. Cook ACKNOWLEDGMENT Many individuals contributed towards the completion of this degree. First, I must thank the department office personnel (Leona Nicholson, Itsue Pfund, Tina Butler, and Dianne Simpson), who guided me through the maize of requirements and madesure the paychecks were deliveredon time. Claudia Annis always "came through", even with unreasonable last minuterequests and Dianne Simpson was persuaded to type this thesis too easily. Special thanks are also given to my sister, Marilyn Rooper, for the calligraphy on the life cycle drawing. An assortment of professors werevery supportive. I wish to thank Ron Welty for being my major professor and Fred Ricksonfor giving critical evaluations of the research and thesis. Don Armstrong also offered sage advice and occasional witticisms. Fellow lab workers also deserve recognition. With a little begging and the promise of an alcoholic beverage rewardPeter Ryan, Shannon Houston, Blaine Baker, Tama Fox, and GayleNelms helped process a multitude of samples. Finally, my love and gratitude is offered to Janice Kimpel and, my husband, Mark Azevedo for theirencouragement, guidance, sincerity, and laughter. Hopefully, I didn't forget to acknowledge someone. To everyone, thank you for your support, and, more importantly, for your friendship. TABLE OF CONTENTS Page INTRODUCTION 1 MATERIALS AND METHODS 9 INFLORESCENCES 9 SEEDS/SEEDLINGS 11 RESULTS 13 STAINING REACTIONS 13 PERCENT ENDOPHYTE IN SEED 13 RE-ISOLATION OF ENDOPHYTE 13 INFLORESCENCE 16 Inflorescence Differentiation 16 Seed Development 24 SEEDLINGS 31 Germination 31 Seedling Development 36 DISCUSSION 42 BIBLIOGRAPHY 56 LIST OF FIGURES Figure Page 1 Colony of A. coenophialum isolated from leaf 14 sheath and blade. 2 Colony of A. coenophialum isolated from 17 immature inflorescence. 3 Hyphae between the rachilla andovary of the 20 inflorescence. 4 Endophyte in nucellus of ovule duringmega- 22 gametophyte development. 5 Hyphae in degrading nucellus. 25 6 Developing endosperm pushes hyphae to seed edge. 25 7 Endophyte in nucellar tissue between developing 27 aleurone cells and pericarp. 8 Hyphae above aleurone cells. 27 9 Endophyte in shoot apex of mature seed. 29 10 Hyphae invading scutellum of expanding embryo. 32 11 A. coenophialum infecting the embryo ofan 34 imbibed seed. 12 Hyphae in root primordium of seed. 34 13 Hyphae surrounding root of seedling. 38 14 Inter- and intra-cellular hyphae in root. 38 15 Distribution of the endophyte in tall fescue. 40 16 Hyphal ball surrounding the lateral root. 50 17 Hyphae above root primordium. 50 18 Root hair packed with hyphae. 52 Distribution of Acremonium coenophialum in DevelopingSeedlings and Inflorescences of Festuca arundinacea INTRODUCTION Since its introduction into the United States fromEurope, tall fescue (Festuca arundinacea Schreb.)has developed into one of the most important forage and turfgrasses grown in the United States. Its commercial successcan be attributed to its ease of establishment into a wide variety of soils andclimates, and to its tolerance of poor grazingmanagement. Although tall fescue has these favorable qualities, it has oftenbeen criticized as a forage grass because of associated livestock health problems andpoor animal performance. Animals grazing tall fescue have shown symptoms of "fescue toxicoses" (Garner, 1983). Fescue toxicoses in cows manifests itselfin three ways: fescue foot (Cornell and Garner, 1980),summer syndrome or poor animal performance (Jacobson et al., 1970),and fat necrosis (Stuedemann et al., 1973). Bacon et al. (1977) associated symptoms of fescue toxicities with thepresence of an endophytic fungus in the plant. Because no sexual stage was observed, thefungus was initially identified as Sphaceliatyphina Sacc., the anamorph of Epichloe typhina (Fr.) Tulasne, the chokedisease of grasses (Bacon et al., 1977; Saccardo, 1881; Sampson, 1933). However, the name was recently changed to Acremonium coenophialum (Morgan-Jonesand Gams, 1982). 2 Grass infected by A. coenophialum is symptomless. The fungus is entirely endophytic in habit and only with microscopic examination can plant infection be determined. It has been conservatively estimated that 75% of all U.S. tall fescueacreage is endophyte infected (Bacon et al., 1986). Several European ecotypes have also been verified as infected (Siegel et al., 1984). A tall fescue endophyte was first described in 1941 (Neill, 1941) and it has been hypothesized thatthis endophyte was A. coenophialum (Morgan-Jones and Gams, 1982; Latchet al., 1984). To date, fifteen species of fescue in additionto tall fescue have been observed to contain Acremonium endophytes (Haliskyet al., 1985; White and Cole, 1985a). Acremonium-type endophytes have also been identified in Lolium (White and Cole, 1985a). In 1983, Missouri, which produces 70% of the tall fescueseed in the U.S., had 100% of its seed lots infected (Rycykand Sharpe, 1984). Of the examined seed, 91% of the lots had 50%or more infection by A. coenophialum. In Kentucky, 97% of the fields surveyed in 1981 were endophyte-infected (Siegelet al., 1983). Many animal toxicity studies have been conductedsince Bacon's initial observations. In tall fescue, poor animal performance and endophyte infection are positively linked (Hovelandet al., 1980; Schmidt et al., 1982). Weight gains for steers grazing endophyte- free tall fescue are twiceas high versus gains for steers grazing endophyte-infected tall fescue (Hovelandet al., 1983). An inverse linear relationship has also been correlatedbetween average daily gains for cattle and the level of endophyteinfection (Williams 3 et al., 1984). Endophyte-infected tall fescue grassesare also suspected of causing reduced conception in grazingcattle, sheep and horses (Siegel et al., 1985). Before it was established that tall fescuewas infected with A. coenophialum, studies had linked thesymptoms of fescue toxicoses to alkaloids present in thegrass. Williams et al. (1975) demonstrated that fescue footsyndrome in cattle could be induced by an extract derived froma known toxic tall fescue (KY-31 variety) pasture. Summer syndrome was said to be caused by the accumulation of the alkaloid perloline (Bushet al., 1973). Poor average daily gain common in steers grazingKY-31, was attributed to this toxin. It is hypothesized that this type of toxin is responsible for decreasedenergy and nutrient availability to the animal. Studies correlating animal toxicities with perloline led to the development ofa new tall fescue variety, G1-307, which contains low levels ofperloline (Hemken, 1983). Subsequent research by Bush et al. (1982) demonstratesa positive relationship between thepresence of tall fescue endophyte and accumulation of loline alkaloidsin the grass. Cattle maintained on a diet of G1-307, whichwas discovered to be highly infected and high in loline alkaloids, showsevere symptoms indicative of summer syndrome (Hemkenet al., 1981). Loline alkaloids have also been isolated from seedof endophyte-infected panicles of tall fescue, butwere not extracted from seed of endophyte-free panicles (Jones et al., 1985). Definitive studies 4 linking loline production by A. coenophialum with fescuetoxicity in cattle have not occurred. Another group of alkaloids from tall fescue, unrelatedto perloline and loline, were reported recently. Ergot alkaloids are produced in vitro by A. coenophialum isolated from tallfescue (Porter et al., 1979). This is the first report of a fungus, outside the genera Balansia and Claviceps, havingthe capability of producing alkaloids that are N-peptide substitutedamides of lysergic acid. The 3 major ergot alkaloids produced by the tall fescue fungal isolate are ergovaline, ergovalinine,and chanoclavine I (Porter et al., 1981).
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