Abstract

Summary Beneficial associations between plants and microbes play an important role in both natural and agricultural ecosystems. For example, associations between fungi of the genus Epichloë, and cool‐season grasses are known for their ability to increase resistance to insect pests, fungal pathogens and drought. However, little is known about the molecular changes induced by endophyte infection.To study the impact of endophyte infection, we compared the expression profiles, based on RNA sequencing, of perennial ryegrass infected with Epichloë festucae with noninfected plants.We show that infection causes dramatic changes in the expression of over one third of host genes. This is in stark contrast to mycorrhizal associations, where substantially fewer changes in host gene expression are observed, and is more similar to pathogenic interactions. We reveal that endophyte infection triggers reprogramming of host metabolism, favouring secondary metabolism at a cost to primary metabolism. Infection also induces changes in host development, particularly trichome formation and cell wall biogenesis.Importantly, this work sheds light on the mechanisms underlying enhanced resistance to drought and super‐infection by fungal pathogens provided by fungal endophyte infection. Finally, our study reveals that not all beneficial plant–microbe associations behave the same in terms of their effects on the host.

Highlights

  • Interactions between plants and beneficial microbes are crucial to the establishment and maintenance of stable ecosystems, in the face of environmental stresses

  • In order to identify perennial ryegrass genes whose expression is altered in response to infection by E. festucae, high-throughput mRNA sequencing was performed on two biological replicates each for wild-type E. festucae-infected plants and uninfected control plants

  • Given that E. festucae infection is generally asymptomatic in the absence of biotic or abiotic stresses, and as mycorrhizal associations have limited impact on their host transcriptome (Gu€imil et al, 2005; Gomez et al, 2009; Guether et al, 2009; Zouari et al, 2014), few effects of endophyte infection were expected in the host grass transcriptome (Table 1)

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Summary

Introduction

Interactions between plants and beneficial microbes are crucial to the establishment and maintenance of stable ecosystems, in the face of environmental stresses. Endophyte infection of grasses can increase host resistance to insect pests through protection from herbivory (Gallagher et al, 1984; Rowan et al, 1986, 1990), enhance drought tolerance (Arachevaleta et al, 1989; West et al, 1993) and give protection from super-infection by fungal pathogens (Tian et al, 2008; Panka et al, 2013b). These associations have been widely exploited by the agricultural industry (Johnson et al, 2013; Young et al, 2013), and have been touted as a ‘perfect partnership’ (Christensen & Voisey, 2007). The effects of pathogen infection tend to be more dramatic, with significantly more host genes differentially expressed (c. 20%) (Doehlemann et al, 2008; Kawahara et al, 2012; De Cremer et al, 2013)

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