Evolutionary Origins and Ecological Consequences of Endophyte Symbiosis with Grasses

Abstract

Over the past 20 yr much has been learned about a unique symbiotic interaction between fungal endophytes and grasses. The fungi (Clavicipitaceae, Ascomycota) grow intercellularly and systemically in aboveground plant parts. Vertically transmitted asexual endophytes forming asymptomatic infections of cool-season grasses have been repeatedly derived from sexual species that abort host inflorescences. The phylogenetic distribution of seed-transmitted endophytes is strongly suggestive of cocladogenesis with their hosts. Molecular evidence indicates that many seed-transmitted endophytes are interspecific hybrids. Superinfection may result in hyphal fusion and parasexual recombination. Most endophytes produce one or more alkaloid classes that likely play some role in defending the host plant against pests. Hybridization may have led to the proliferation of alkaloid-production genes among asexual endophytes, favoring hybrids. The ergot alkaloid ergovaline, lolitrems, and lolines are produced by only a single sexual species, Epichloë festucae, but they are common in seed-transmitted endophytes, suggesting that E. festucae contributed genes for their synthesis. Asexual hybrids may also be favored by the counteracting of the accumulation of deleterious mutations (Muller's rachet). Endophyte infection can provide other benefits, such as enhanced drought tolerance, photosynthetic rate, and growth. Estimates of infection frequency have revealed variable levels of infection with especially high prevalence in the subfamily Pooideae. Longitudinal studies suggest that the prevalence of seed-transmitted endophytes can increase rapidly over time. In field experiments, infected tall fescue suppressed other grasses and forbs relative to uninfected fescue and supported lower consumer populations. Unlike other widespread plant/microbial symbioses based on the acquisition of mineral resources, grass/endophyte associations are based primarily on protection of the host from biotic and abiotic stresses.

Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize

“…Fungal mutualists confer a wide range of benefits to their hosts (Porras-Alfaro & Bayman, 2011), including enhanced host disease resistance (Djonović et al, 2007;Pozo & Azcó nAguilar, 2007;Viterbo et al, 2007), drought tolerance (Hause & Fester, 2005), improved nutrient uptake and Trichoderma NRPSs growth (Balestrini & Lanfranco, 2006;Martin et al, 2007;Chacó n et al, 2007), and protection against invertebrate and vertebrate herbivory (Clay & Schardl, 2002). The expression of induced defences is mediated by complex signalling networks in which the plant hormones JA and SA play key roles (Smith et al, 2009).…”

Fungal Assemblages Associated with Roots of Halophytic and Non-halophytic Plant Species Vary Differentially Along a Salinity Gradient

“…Several works point out that mutualistic interactions between plants and their associated fungal consortia are of paramount relevance for the distribution of plant communities worldwide, through increasing host fitness and assisting in adaptation to environmental and biological stresses [1][2][3][4]. Endophytic colonization of aboveground plant tissues may lead to beneficial effects to the host (e.g., [5]), for instance, in some grasses where Clavicipitaceous endophytes (classified as class 1 endophytes in [6]) are responsible for herbivory resistance [7]. However, it is generally assumed that most plant-fungus mutualistic interactions take place in roots, due to a more systemic colonization [6,8].…”

Epichloë glyceriae infection affects carbon translocation in the clonal grass Glyceria striata

“…While pathogens are generally associated with only negative effects on their host plants (Burdon, 1987;Agrios, 1997), this is clearly not the case for these fungal endophytes (Schardl et al ., 2004). Epichloë species typically have both pathogenic and mutualistic effects on their host grasses (Clay & Schardl, 2002). In previous studies, we found that E. glyceriae had a positive effect on G. striata clonal growth, increasing both number of stolons and clonal growth biomass, although total biomass did not differ between infected and uninfected plants (Pan & Clay, 2002, 2003.…”

“…In previous studies, we found that E. glyceriae had a positive effect on G. striata clonal growth, increasing both number of stolons and clonal growth biomass, although total biomass did not differ between infected and uninfected plants (Pan & Clay, 2002, 2003. Despite more vigorous vegetative growth, host plants infected by Epichloë endophytes are often completely sterilized by infection (Clay & Schardl, 2002), leading Bradshaw (1959) to refer to these interactions as 'a curious form of symbiosis'. Although the outcome is different, these fungal endophytes may have similar effects and use similar mechanisms to manipulate host physiology and resource movement as pathogens because of their similar dependence on host resources.…”