Epichloë (formerly Neotyphodium) fungal endophytes increase adaptation of cool-season perennial grasses to environmental stresses

Abstract

Many cool-season grass species have evolved with asexual, nonsymptomatic fungal endophytes of the genus <em>Epichloë</em> (formerly <em>Neotyphodium</em>) of the family Clavicipitaceae. These associations range from parasitic to mutualistic and have dramatic effects on grass host chemistry, increasing resistance to abiotic (drought, soil mineral imbalance) and biotic (vertebrate and invertebrate herbivory, nematodes, plant pathogens, plant competition) stresses. Native endophyte strains produce a range of bioprotective alkaloid and other nonalkaloid secondary compounds, several of them known to have detrimental effects on grazing animals. In the past two decades, epichloid endophyte strains have been selected with marginal or no capacity of producing ergot and/or lolitrem alkaloids. These novel endophyte strains have been introduced to several grass cultivars with the idea to increase grass host resistance to abiotic stresses without hindering grazing livestock, and abiotic stresses to ensure high competitive ability of symbiotic grass cultivars. In this presentation, we discuss mechanisms underlying the competitiveness of epichloid endophyte/grass associations and consequences of endophyte infection for grassland ecosystem functions.

A Systematic Review on the Effects of Epichloë Fungal Endophytes on Drought Tolerance in Cool-Season Grasses

“…It is well-known today that fescue toxicosis and ryegrass staggers are animal diseases caused by alkaloids (ergovaline and lolitrem-B) produced by their common associated fungi Epichloë coenophiala and Epichloë festucae , respectively (Schardl et al, 2013 ; Leuchtmann et al, 2014 ). The importance of these two forage grass species in temperate regions of the world triggered an enormous research activity aimed at understanding the endophyte effects not only on animal health and growth but also on plant performance, stand persistence, and forage production (Bacon, 1993 ; Malinowski and Belesky, 2000 , 2019 ; Klotz, 2015 ). Removing fungal endophytes from grass cultivars was an alternative to avoid the antiquality traits (i.e., toxic alkaloids) in forage; however, this was also associated with a poor performance of grass plants in the field (Bouton et al, 2001 ).…”

“…Motivated by its conspicuous characteristics (namely, “the vertical transmission” and “the alkaloid-mediated defense of hosts against herbivores”), the grass–endophyte symbiosis became a model system of studies in ecology and evolution (Saikkonen et al, 2006 ; Rudgers et al, 2009 ; Gundel et al, 2011 ; Omacini et al, 2012 ; Hume et al, 2020 ). In fact, the studies of factors driving plant–endophyte specificity and environmental controls favoring or not the symbiosis incidence in populations have been among the major goals in research (Malinowski and Belesky, 2006 , 2019 ; Schardl et al, 2008 ; Rudgers et al, 2009 ; Karimi et al, 2012 ; Iannone et al, 2013 ; Semmartin et al, 2015 ; Schirrmann et al, 2018 ). However, it has been not straightforward to explain the driving environmental factors behind the distribution and abundance of symbiotic grasses in nature (Saikkonen et al, 2006 ; Rudgers et al, 2009 ; Gundel et al, 2011 , 2016 ; Semmartin et al, 2015 ; Wang et al, 2020 ).…”

“…Summary table showing adaptation mechanisms for the different strategies plant may use to withstand drought conditions (sensuMalinowski and Belesky, 2019) and that can be modulated by Epichloë fungal endophytes.…”

Non-Transgenic CRISPR-Mediated Knockout of Entire Ergot Alkaloid Gene Clusters in Slow-Growing Asexual Polyploid Fungi

“…Epichloë coenophiala is widespread as a seed-borne endophyte of the highly popular pasture, forage, and turf grass, Lolium arundinaceum (= Schedonorus arundinaceus = Festuca arundinacea ; tall fescue), although its existence was unsuspected in the first decades of widespread propagation of the grass during the mid-20th century. The fungus provides important benefits that translate to enhanced stand longevity and productivity and improved tolerance of drought and other stresses [ 9 , 10 ], and it is capable of producing up to four different classes of alkaloids that protect the grass hosts against invertebrates [ 2 , 11 ]. Unfortunately, the strains of E. coenophiala that have been unwittingly co-propagated with tall fescue, and which remain dominant in much of the cool-season pasturelands, produce ergovaline, which is an ergot alkaloid of the highly toxic ergopeptine type [ 12 , 13 , 14 ].…”

Maternal Exposure to Ozone Modulates the Endophyte-Conferred Resistance to Aphids in Lolium multiflorum Plants

“…In addition to the alkaloid-mediated herbivore resistance, endophytes can be source of other metabolites with functional roles such as phenolic compounds [ 35 , 36 , 37 ]), antioxidants [ 38 , 39 , 40 ] and phytohormones [ 41 ]. These are suggested to explain the usually documented higher performance of endophyte-symbiotic plants, relative to endophyte-free plants, under conditions of stress caused by biotic (competing plants, herbivores, pathogens) and abiotic factors (drought, heavy metal, herbicides) [ 38 , 39 , 40 , 42 , 43 , 44 , 45 ]. Nonetheless, the endophyte effects on host plant performance have been shown to depend on the ecological context and thus, symbiosis outcome can yield positive, neutral, or even negative [ 46 , 47 , 48 ].…”