Symbiosis between grasses and asexual fungal endophytes

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The symbiosis between vertically transmitted asexual endophytic fungi and grasses is common and generally considered to be mutualistic. Recent studies have accumulated evidence of negative effects of endophytes on plant fitness, prompting a debate on the true nature of the symbiosis. Genetic factors in each of the two partners show high variability and have a range of effects (from positive to negative) on plant fitness. In addition, interacting environmental factors might modify the nature of the symbiosis. Finally, competition and multitrophic interactions among grass consumers are influenced by endophytes, and the effects of plant neighbours or consumers could feedback to affect plant fitness. We propose a mutualism–parasitism continuum for the symbiosis between asexual endophytes and grasses, which is similar to the associations between plants and mycorrhizal fungi.

Introduction

Endophytes are ubiquitous microbial associates found in most species of plants [1] and show an astonishing diversity [2, 3••, 4]. Given this diversity, there must be a role for these hidden microbes in structuring natural communities and affecting ecosystem functions [5]. The effects of some microbes on plant fitness are well understood, but endophytic fungi in grasses have received less attention than mycorrhizae, nitrogen-fixing bacteria and microbial pathogens, presumably because their function is not always clear. The first records of endophytic fungi in grasses date back to the late 19th century, but the symbiosis attained more recognition from the 1970s onwards, following the discovery of the toxicity to livestock of endophyte-produced alkaloids [6]. The grass endophytes that cause such effects belong to the family Clavicipitaceae (Ascomycota) and have a sexual and an asexual life cycle [6]. The sexual form, Epichloë, has a parasitic nature. This form causes choke disease (Figure 1a), which suppresses flower and seed production in grasses, and is transmitted horizontally to new host plants. The asexual form, Neotyphodium (previously Acremonium), is seen as a mutualist of grasses, causing no visible symptoms and being transmitted vertically through the seeds of the host plant [6, 7]. Neotyphodium can be observed as hyphal accumulations in infected grass seeds (Figure 1b) or as single, long and often convoluted hyphae that grow between the cells of the host's leaf tissue (Figure 1c). Neotyphodium is not normally found in roots, but might colonize the vascular bundles of the host plant [8]. Only the asexual life cycle is known for some host-specific endophytes on Lolium perenne.

In this review, we focus on associations between grasses, Neotyphodium and invertebrate consumers. Neotyphodium profits from host plants by receiving nutrients, shelter and guaranteed transmission to the next host generation. All of these benefits are a direct consequence of the fungus’ strictly symbiotic dependence, with the fungus living within the host's body. By contrast, the benefits for the host plant are indirect and more complex. Infection by Neotyphodium has been shown to induce increased above-ground biomass, tiller number, seed production, root growth and stress tolerance in the grass host [6]. The plant can benefit from increased resistance to herbivores, nematodes and pathogens thanks to the production of alkaloids by the fungus [7]. The toxic effects of endophytes on livestock mainly depend on the production of ergot alkaloids and indolediterpene alkaloids (including Lolitrem B), whereas loline alkaloids and peramine are especially toxic to invertebrate herbivores [6, 7]. Therefore, the symbiosis between grasses and Neotyphodium is assumed to be mutualistic because it provides benefits to both partners. However, this dogma of mutualistic symbioses has been challenged by recent work [9, 10, 11•, 12•, 13]. This is perhaps not surprising, because the fitness of the host depends not only on the presence of the endophyte but also on various abiotic factors and a whole network of species that interact with the host plant directly or indirectly (Figure 2). The difficulty is to incorporate all of these factors in experiments that investigate endophyte-derived benefits for the plant. Recently, research on the grass-endophyte symbiosis has started to integrate various elements, such as genetic background, nutrient levels, drought stress and herbivore consumers and their enemies, into experiments that assess the nature of the symbiosis. Integrative ecological studies of endophytes and their effects on complex trophic interactions, ecosystem functions and feedback systems within food webs are likely to advance quickly and should provide a more complete picture of these interesting symbiotic interactions between grasses and Neotyphodium [14, 15, 16, 17•]. Much basic knowledge of the grass-Neotyphodium interaction has accumulated over the past 40 years and has been exquisitely reviewed by several authors [6, 7, 10, 13]. Here, we concentrate on recent research, published between 2002 and 2004, into the grass-Neotyphodium symbiosis and its incorporation into a community framework.

Section snippets

Contrasting responses of grasses to endophyte infection

Most of our understanding of the grass–Neotyphodium interaction comes from studies of two economically important pasture grasses, Festuca arundinacea (Fa) and Lolium perenne (Lp). For these species, infected grass individuals and populations have been found to have numerous advantages over uninfected grass individuals and populations [6]. Such unambiguous results do not exist for other grass species that associate with Neotyphodium [9, 18]. For example, infection of Festuca arizonica with

Species, grass cultivars, genotypes, and endophyte strains

The number of grass species that are infected by Neotyphodium is unknown, but 14 asexual Neotyphodium species and several hybrids have been described to date [22], some of which are very species-specific [23]. Many interspecific hybrids that have independent origins have been found across a broad taxonomic and geographical sample of asexual isolates [24]. This suggests a mechanism by which even asexual endophytes can adapt to and evolve with new hosts. Despite this advantage, gene-flow among

Environmental factors

Infected grasses are normally claimed to have superior nutrient status and enhanced drought tolerance when compared with uninfected grasses [6], presumably because of deeper root growth [33] or physiological alterations [7]. For Lp, however, the plant's genotype or place of origin (ecotype) might be more important for drought resistance than is the presence or absence of endophyte infection [12]. Uninfected F. arizonica plants consistently have greater biomass than infected plants,

Community interactions based on endophytic fungi

Multitrophic interactions (Figure 3), herbivory and intra- and interspecific competition can influence the performance of plants either directly or indirectly.

In one four-year study, E+ grasses out-competed E− grasses, resulting in an overall decrease in plant-species richness [38]. Another study found that endophytes and mowing have positive effects on plant-species richness [39]. Intraspecific competition between E+ and E− individuals of F. arizonica has shown that E− grasses have advantages

Microbes, soil feedbacks and ecosystem function

Biotic interactions can occur between Neotyphodium and other microbes, and interactions among plants can be mediated by soil characters that can be altered through allelopathy by endophytes [46, 47] or by the decreased speed at which infected plants decompose [48]. Although direct effects of endophyte-infected grass communities on the growth of other plants through soil alterations are not prevalent, there could be interesting indirect effects that cause plants to grow better on soils that

Conclusions

The continuum between mutualism and parasitism in Neotyphodium–grass symbioses has been studied across all levels of biological organization. Many advances have been made at the molecular and genetic scale, but the effects of endophytes on the structure and organization of communities and ecosystems remain largely unexplored. Intrinsic factors (e.g. study species, cultivars, genotypes and strains), the environment (e.g. nutrient and water availability) and biotic interactions with other species

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Adrian Leuchtmann, Giorgina Bernasconi, Stan Faeth, Ted Farmer, Dennis Hansen and Simone Härri for helpful suggestions on the manuscript. This study is funded by a grant from the Swiss National Science Foundation to Christine Müller (Grant number 631-065950).

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