15 Epichloë Endophytes: Clavicipitaceous Symbionts of Grasses CHRISTOPHER L. SCHARDL 1 , BARRY SCOTT 2 , SIMONA FLOREA 1 , DONGXIU ZHANG 1 CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275 II. Symbiosis and the Clavicipitaceae . . . . . . . . . . 276 A. Symbiota . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276 B. Life Cycles of Epichloë and Neotyphodium spp. . . . . . . . . . . . . . . . . . . . . 277 C. Evolution of the Epichloae . . . . . . . . . . . . . . 278 D. Host Compatibility . . . . . . . . . . . . . . . . . . . . 279 III. Ecological and Agronomic Roles of Endophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284 A. Host Fitness Effects . . . . . . . . . . . . . . . . . . . . 284 1. Resistance to Biotic Stresses . . . . . . . . . 284 2. Drought Tolerance . . . . . . . . . . . . . . . . . 285 B. Diversity and Plasticity of Endophyte Benefits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 286 C. Ecosystem Effects. . . . . . . . . . . . . . . . . . . . . . 286 IV. Endophyte Metabolites . . . . . . . . . . . . . . . . . . . . 287 A. Ergot Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . 287 1. Ergot Alkaloid Activities . . . . . . . . . . . . 287 2. Ergot Alkaloid Biosynthesis . . . . . . . . . 290 3. Genetics of Ergot Alkaloid Biosynthesis . . . . . . . . . . . . . . . . . . . . . . 291 B. Lolitrems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292 C. Loline Alkaloids . . . . . . . . . . . . . . . . . . . . . . . 294 D. Peramine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297 V. Genome and Transcriptome of Epichloë festucae . . . . . . . . . . . . . . . . . . . . . . . . . 298 VI. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . 299 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300 I. Introduction The modern approach to biology emphasizes the workings and system integration of individual organisms, with microbial infections usually con- sidered in a disease context, yet it is benign and mutualistic symbioses that actually dominate the biosphere. Even our own healthy bodies host complex microbial consortia (Gill et al. 2006). The ecological importance of lichens (fungi hosting green algae or cyanobacteria; DePriest 2004) and the reliance of corals on zooxanthellate algae (Baker 2003) are clear. Root nodules, representing sym- bioses of legumes with rhizobia (Rhizobium spp. and related bacteria; Doyle 1994), provide a large portion of fixed nitrogen on which much of the biosphere relies. Even more ubiquitous are the mycorrhizae, which serve a key nutritional role in the vast majority of land plants (Strack et al. 2003; Chaps. 13, 14). These symbioses are readily appar- ent to the unaided eye. For example, lichens coat rocks and tree trunks in much of earth’s wilder- ness, and algae bestow their bright colors upon vast coral reefs. More sophisticated microbio- logical techniques must be employed to visualize endophytic and epiphytic microbes, and often the structures observed need much further investiga- tion to determine if they represent benign symbi- onts or latent plant pathogens. Perhaps because of the difficulties inherent in studying benign epiphytes and endophytes, the particularly stable and well characterized symbi- oses of grasses with members of the fungal fam- ily Clavicipitaceae have become the favorite model for these lifestyles. Most species in a clade of the Clavicipitaceae (Spatafora et al. 2007) maintain systemic and long-term symbioses with plants that are largely or completely asymptomatic. What is intriguing is that most of these symbioses defy the usual categorization as mutualistic, commensal or antagonistic, because their effects on host fitness can vary with environment, ecological circum- stance, and the stage of host development (Clay 1990; Saikkonen et al. 1998). Many of these sym- bionts, such as Epichloë, Atkinsonella, Parepichloë, and several Balansia spp. (White 1997; White and Reddy 1998; White et al. 1995, 1997), fruit on host inflorescences or florets, which consequently fail to develop and set seed. Others, such as Myriog- enospora spp. and some Balansia spp., fruit on leaves or nodes, but still may more or less suppress host flowering and seed production (Clay 1990; Clay et al. 1989; White and Glenn 1994). Ironically, Plant Relationships, 2nd Edition The Mycota V H. Deising (Ed.) © Springer-Verlag Berlin Heidelberg 2009 1 Department of Plant Pathology, 201F Plant Science Building, 1405 Veterans Drive, Lexington, KY 40546-0312, USA; e-mail: schardl@ uky.edu 2 Institute of Molecular BioSciences, Massey University, Palmerston North 5321, New Zealand