ABSTRACT
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA
Adrian Leuchtmann
Geobotanisches Institut ETH, Zurich, Switzerland
24.1 INTRODUCTION
One of the world’s most intensely studied symbiotic systems is that of the grass
Lolium arundinaceum
(Schreb.) Darbysh. (=
Festuca arundinacea
Schreb.; tall fescue), with its common endophyte
Neotyphodium coenophialum
(G. Morgan-Jones et W. Gams) A.E. Glenn et al. The practical applications of this symbiosis, together with livestock toxicoses attributable to the endophyte, have fueled intense interest from mycologists, plant biologists, plant breeders, ecologists, chemists, and molecular biologists. This interest was further fueled by several remarkable facts that emerged shortly after the discovery of the endophyte (Bacon
et al., 1977; reviewed in Bush
et al., 1997; Malinowski and Belesky, 2000; Clay and Schardl, 2002; Panaccione and Schardl, 2003; Schardl, 2004; Schardl
et al., 2004a). First, the tall fescue-
N. coenophialum
symbiotum is a systemic and long-term association in which the endophyte colonizes all aerial parts of the plant and is vertically transmitted at very high efficiency (Siegel
et al., 1985). Second, the endophyte has the capability to protect the host from abiotic and biotic stresses by various means, including synthesis of anti-insect and antivertebrate alkaloids, and changes in host metabolism and architecture. Third, numerous other endophytes in cool-season grasses (subfamily Poöideae) are closely related to the tall fescue endophyte and share characteristics of systemic symbiosis, vertical transmission, bioprotection, and antiherbivore alkaloids (Figure 24.1). Fourth, although
N. coenophialum
and related endophytes are asexual, non-
pathogenic fungi, they are evolutionary derived from sexual plant pathogens, namely,
Epichloë
spp. Seed-transmitted grass endophytes have been known for well over a century (Free-
man, 1904), but only since 1982 have the characteristics and relationships of these endophytes been sufficient to begin describing new
Neotyphodium
spp. (Morgan-Jones and Gams, 1982). Also, development of the means to culture most endophytes and to introduce them into endophyte-cured plants of their native hosts (Latch and Christensen, 1985) or other grasses (Koga et al., 1993; Christensen et al., 2000; Johnson-Cicalese et al., 2000) has led to a better understanding of niche specialization of the endophytes. Furthermore, prior to 1993, all
Epichloë
spp. known from poöid grasses were classified as
Epichloë typhina
, but since phylogenetic analysis began to be applied to the problem, the characterization of new
Epichloë
spp. has gone hand in hand with descriptions of numerous new
Neotyphodium
spp. An understanding of the ecological and evolutionary implications of the epichloë
endophytes requires recognition of how the diversity of symbiotic types relates to taxonomic diversity of the partners involved. All of these symbioses involve fungal endophytes systemically inhabiting host grasses. In many the symbioses are maintained through host generations (inherited), and in many the symbiont is capable of horizontal transmission (Figure 24.2
)
. But the latter process is promoted by the sexual cycle, which entails symbiosis with fly species of the genus
Botanophila
(class Diptera, order Anthomyiidae) (Figure 24.1C). Molecular data such as isozymes (Leuchtmann and Clay, 1990), microsatellites (Moon
et al., 1999), and DNA sequences have indicated unexpected complexities underlying evolutionary relationships between
Epichloë
species (Craven
et al., 2001b)
Figure 24.1
(a) Infected
Brachypodium sylvaticum
with stromata. (b) Stromata of
Epichloë sylvatica
in different stages of maturation. (c) Larval brood chambers (arrows) from which larvae emerge to feed on developing perithecia of
Epichloë typhina
. (d) Infected leaf sheath of
Lolium perenne
stained for hyphae. (e) Fungal growth (arrows) in stem and leaf meristems of
Bromus ramosus
. (f)
Neotyphodium
anamorph of
Epichloë bromicola
in culture. (g) Endophytic hyphae among aleurone cells of
Lolium perenne
seed. Magnifications: (d)
×
700; (e)
×
150; (f and g)
×
and the evolution of
Neotyphodium
species from
Epichloë
species (Moon et al., 2004) (Figure 24.3).
