Plant Science 180 (2011) 190–195 Contents lists available at ScienceDirect Plant Science journal homepage: www.elsevier.com/locate/plantsci Review What triggers grass endophytes to switch from mutualism to pathogenism? Carla J. Eaton a,d , Murray P. Cox a,b,c , Barry Scott a,b,∗ a Institute of Molecular BioSciences, Massey University, Palmerston North, New Zealand b The Bio-Protection Research Centre, New Zealand c The Allan Wilson Centre for Molecular Ecology and Evolution, New Zealand d Department of Plant Pathology and Microbiology, University of California, Riverside, USA article info Article history: Received 28 July 2010 Received in revised form 4 October 2010 Accepted 4 October 2010 Available online 16 October 2010 Keywords: Symbiosis Next generation sequencing Reactive oxygen Nox Intercalary extension abstract Symbioses between cool season grasses and fungi of the family Clavicipitaceae are an integral component of both natural and agricultural ecosystems. An excellent experimental model is the association between the biotrophic fungus Epichloë festucae and Lolium perenne (perennial ryegrass). The fungal partner pro- duces a suite of secondary metabolites that protect the host from various biotic and abiotic stresses. The plant host provides a source of nutrients and a mechanism of dissemination via seed transmission. Crucial mechanisms that maintain a stable mutualistic association include signaling through the stress activated MAP kinase pathway and production of reactive oxygen species by the fungal NADPH oxidase (Nox) com- plex. Disruption of components of the Nox complex (NoxA, NoxR and RacA), or the stress-activated MAP kinase (SakA), leads to a breakdown in this finely balanced association, resulting in pathogenic infection instead of mutualism. Hosts infected with fungi lacking a functional Nox complex, or the stress-activated MAP kinase, display a stunted phenotype and undergo premature senescence, while the fungus switches from restricted to proliferative growth. To gain insight into the mechanisms that underlie these physio- logical changes, high throughput mRNA sequencing has been used to analyze the transcriptomes of both host and symbiont in wild-type and a mutant association. In the sakA mutant association, a dramatic up- regulation of fungal hydrolases and transporters was observed, changes consistent with a switch from restricted symbiotic to proliferative pathogenic growth. Analysis of the plant transcriptome revealed dramatic changes in expression of host genes involved in pathogen defense, transposon activation and hormone biosynthesis and response. This review highlights how finely tuned grass-endophyte associa- tions are, and how interfering with the signaling pathways involved in maintenance of these associations can trigger a change from mutualistic to pathogenic interaction. © 2010 Elsevier Ireland Ltd. All rights reserved. Contents 1. The biology of grass–endophyte interactions ....................................................................................................... 191 2. Breakdown of mutualism in mutant associations .................................................................................................. 191 3. Insights into symbiosis from next generation sequencing ......................................................................................... 193 4. Plant gene expression ............................................................................................................................... 193 5. Conclusions .......................................................................................................................................... 195 Acknowledgements ................................................................................................................................. 195 References ........................................................................................................................................... 195 ∗ Corresponding author at: Institute of Molecular BioSciences, Massey University, Private Bag 11222, Palmerston North 4442, New Zealand. Tel.: +64 6 350 5543; fax: +64 6 350 2267. E-mail address: d.b.scott@massey.ac.nz (B. Scott). 0168-9452/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2010.10.002