Malinoswki (Drought Tolerance by Endophyte)

CROP SCIENCE
Volume 40 July–August 2000 Number 4
REVIEW & INTERPRETATION

Adaptations of Endophyte-Infected Cool-Season Grasses to Environmental Stresses:
Mechanisms of Drought and Mineral Stress Tolerance
Dariusz P. Malinowski* and David P. Belesky
ABSTRACT the host grass, forming nonpathogenic, systemic, and
Cool-season grasses infected with Neotyphodium spp. endophytes usually intercellular associations (Bacon and De Bat-
have an extraordinary impact on the ecology and economy of pasture tista, 1991). The best known grass endophytes are classi-
and turf. A range of adaptations of endophyte-infected grasses to fied in the tribe Balansieae of the family Clavicipitaceae
biotic and abiotic stresses has been identified but mechanisms of these (Ascomycetes) (Diehl, 1950). Currently, seven genera
adaptations are not clearly understood. In this review, we present have been identified including Atkinsonella, Balansia,
recent research progress on endophyte-related mechanisms affecting Balansiopsis, Echinodothis, Epichloë, Myriogenospora
abiotic (drought, mineral) and selected aspects of biotic stress toler- (White, 1994), and Parepichloë (White and Reddy,
ance in cool-season grasses. Endophytes induce mechanisms of
1998). Morgan-Jones and Gams (1982) erected the sec-
drought avoidance (morphological adaptations), drought tolerance
(physiological and biochemical adaptations), and drought recovery in
tion Albo-lanosa to accommodate the anamorphic (im-
infected grasses. Mineral nutrition (nitrogen, phosphorus, calcium)
perfect) stage of Epichloë spp. in the genus Acremonium
affects production of ergot alkaloids, thus understanding mechanisms that caused symptomless infections of grasses in the
involved in mineral economy of endophyte-infected grasses will help subfamily Pooideae (Siegel, 1993). Glenn et al. (1996)
in developing management practices to reduce forage toxicity to live- reclassified the genus Acremonium sect. Albo-lanosa in
stock. Previous research resolved the role of endophyte in nitrogen a new genus Neotyphodium to separate clavicipitaceous
(N) economy of tall fescue. We identified two endophyte-related Acremonium (e-endophytes) from Acremonium with
mechanisms in tall fescue operating in response to phosphorus (P) other affinities (usually saprotrophs). The most widely
deficiency. The mechanisms are altered root morphology (reduced known Neotyphodium endophytes are N. coenophialum
root diameters and longer root hairs) and chemical modification of (Morgan-Jones and Gams) Glenn, Bacon and Hanlin,
the rhizosphere resulting from exudation of phenolic-like compounds.
N. lolii (Latch, Christensen, and Samuels) Glenn, Bacon
These mechanisms were shown to benefit endophyte-infected plants
and Hanlin, and N. uncinatum (Gams, Petrini and
grown under P deficiency. We also report a mechanism of aluminum
(Al) sequestration on root surfaces in endophyte-infected tall fescue,
Schmidt) Glenn, Bacon and Hanlin that colonize tall
which appears to be related to exudation of phenolic-like compounds fescue (Festuca arundinacea Schreb.), perennial rye-
with Al-chelating activity. Understanding mechanisms of abiotic stress grass (Lolium perenne L.), and meadow fescue (F. pra-
tolerance in endophyte-infected grasses is essential for continued im- tensis Huds.), respectively. Studies with grasses led to
provement and persistence of grasses for a range of applications, e.g., the discovery of two other groups of symptomless fungal
forage for semi-arid areas or cover plants for soil renovation. endophytes. One group (p-endophytes) consists of
closely related Gliocladium-like endophytes (An et al.,
1993) in perennial ryegrass (Latch et al., 1984; Philipson,
I n their evolution, grasses have developed symbiotic

associations with fungi including mycorrhizal fungi
that grow in or on the roots (Smith and Read, 1997),
1991) and Phialophora-like endophytes in meadow fes-
cue, F. gigantea (L.) Vill., and Arizona fescue (F. arizon-
ica Vasey) (Schmidt, 1991; An et al., 1993). The p-endo-
and fungi that systemically infect grass shoots. Among phytes are ordered to Eurotiales (Ascomycetes) (Siegel
the latter are grass endophytes, defined as fungi that et al., 1995) and are not related to e-endophytes (Leucht-
live their entire life cycle within the aerial portion of mann, 1992). The p-endophytes differ from e-endo-
phytes in patterns of mycelium growth and leaf blade
D.P. Malinowski, Texas A&M Univ., Texas Agric. Exp. Stn., P.O.B. colonization, colonization of roots, ability to sporulate
1658, Vernon, TX 76385; D.P. Belesky, USDA-ARS, Appalachian on the host grass (thus being naturally infective), no
Farming Systems Research Center, 1224 Airport Rd., Beaver, WV
25813. Received 26 Oct. 1999. *Corresponding author (d-malinowski
@tamu.edu). Abbreviations: DM, dry matter; PWUE, instantaneous water use effi-
ciency; TW/DW, turgid weight:dry weight ratio; WUE, water use effi-
Published in Crop Sci. 40:923–940 (2000). ciency.
923
924 CROP SCIENCE, VOL. 40, JULY–AUGUST 2000
alkaloid production (Siegel et al., 1995), and negligible tive than noninfected grasses and thrive better than
effects on host tolerance to biotic and abiotic stresses noninfected grasses with limited resources (Marks et
(Schmidt, 1993; Malinowski et al., 1997a). Both groups al., 1991; Bacon and Hill, 1996; Hill et al., 1998). Recent
of endophytes may occur symbiotically in the same host approaches to endophyte–grass interactions focus on
plant (Latch et al., 1984; Schmidt, 1991). The third group isolated endophyte strains that, in association with
of grass endophytes (a-endophytes) has been proposed grasses, show minimal or no production of alkaloids
to accommodate endophytes found in annual ryegrass toxic to livestock yet retain the pest- and drought-resis-
(L. multiflorum Lam.) and F. paniculata L. (Naffaa et tance benefits of symbiotic plants (Fletcher and Easton,
al., 1998a). These endophytes belong to the section Sim- 1997; Funk and White, 1997; Bacon and Hinton, 1998).
plex of the genus Acremonium and are represented by These associations are crucial for improved livestock
parasitic species of Acremonium similar to A. chilense, performance on fescue and ryegrass. Once alkaloid pro-
an endophyte of orchardgrass (Dactylis glomerata L.) duction has been altered, it is essential to understand
(Morgan-Jones et al., 1990). Similar to p-endophytes, mechanisms involved in abiotic stress tolerance of endo-
effects of a-endophytes on physiological processes and phyte-infected grasses for their continued improvement
ecology of cool-season grasses are much less understood and persistence for a range of applications.
than effects of Neotyphodium spp. endophytes (Mor- We outline the principal research findings and conclu-
gan-Jones et al., 1990; Schmidt, 1993; Malinowski et al., sions on abiotic and biotic stress tolerance of Neotypho-
1997a; Naffaa et al., 1998a), and will not be discussed dium spp. endophyte–grass associations, emphasizing
in this review. recent research progress on endophyte-induced mecha-
Interactions between Neotyphodium spp. endophytes nisms of mineral stress tolerance in tall fescue.
and cool-season grasses have been referred to as defen-
sive mutualism (Clay, 1988). In these associations, endo- Mechanisms of Biotic Stress Tolerance
phytes produce a range of alkaloids (Porter, 1994) or
stimulate the host grass to synthesize alkaloids and other Persistence of individual plants and ultimately popu-
secondary metabolites (Bush et al., 1997; Ju et al., 1998) lations in grassland and pasture ecosystems is deter-
that protect the symbiotum from mammalian, insect, mined by biotic and abiotic factors (reviewed in Briske
and nematode herbivores. Mutualistic symbioses, how- and Heitschmidt, 1991; Briske, 1996) interacting with
ever, result in a net benefit to each participant. By com- population genetics. Biotic factors include herbivores
paring genetically identical endophyte-infected with (animals, insects), nematodes, and pathogens (fungi,
noninfected plants, such benefits to the grass host may bacteria, and viruses). Herbivory can influence the can-
be shown. In contrast, Neotyphodium spp. endophytes opy environment by altering light conditions, nutrient
cannot exist without their grass hosts (cultured mycelia cycling dynamics, and water use. Because endophyte-
excepted); therefore, they are completely dependent on infected and noninfected grasses respond differently to
the host grass for protection and supply for nutrients such changes in canopy environment, herbivory, there-
and water. Wilkinson and Schardl (1997) revised the fore, can interact with endophyte infection to determine
concept of mutualistic symbioses between Neotypho- productivity of grasses. There is a strong selective advan-
dium spp. endophytes and their grass hosts and defined tage for endophyte-infected grasses in populations that
them as asymptomatic symbioses. In such associations, include noninfected plants (Clay, 1988). This is because
the loss of sexuality is a fundamental cost in the long endophyte infection stimulates production of an array
term in contrast to associations which have both means of bioprotective alkaloids (Porter, 1994; Bush et al.,
of reproduction (called balanced symbioses). Thus, the 1997) and non-alkaloid secondary metabolites (Koshino
most important benefit to Neotyphodium spp. endo- et al., 1989; Ju et al., 1998) in the host grass. These
phytes appears to be dissemination through seeds of the metabolites can deter livestock and insect herbivores
host plant. This may, in part, explain an often reported (Breen, 1994; Ball, 1997). A relationship between health
increase in fitness of endophyte-infected grasses. Appar- disorders in cattle and a high level of endophyte infesta-
ently, maximizing host growth by endophyte is in the tion in tall fescue from toxic pastures in the USA was
ecological interest of both partners. Recently, virus-like first shown by Bacon et al. (1977). A similar relationship
particles have been identified in the endophyte Epichloë was later reported for perennial ryegrass in New
festucae Leuchtmann, Schardl and Siegel isolated from Zealand (Fletcher and Harvey, 1981) and other grass
asymptomatic F. rubra L. plants (Zabalgogeazcoa et al., species infected with Neotyphodium spp. endophytes
1998), suggesting a third component (a mycovirus) of (Petroski et al., 1992; Miles et al., 1998).
endophyte–grass associations. Although the presence of Researchers identified several alkaloids responsible
viral RNA did not induce any phenotypic effects in its for poor performance of animals grazed or fed on endo-
fungal host, possible phenotypic effects on the grass host phyte-infected grasses (Porter, 1994). Ergot alkaloids
deserve attention in future experiments. (clavines, lysergic acid and its amides, ergopeptines) are
Endophyte-infected grasses express a range of adap- responsible for fescue toxicosis in grazing livestock and
tations to biotic (reviewed in Latch, 1993) and abiotic are produced by endophytes of tall fescue and perennial
stresses, including drought (reviewed in Bacon, 1993; ryegrass, N. coenophialum and N. lolli, respectively.
West, 1994), mineral imbalance (Lyons et al., 1990; Mali- When artificially infected with N. coenophialum,
nowski et al., 1998a, 1999b), and soil acidity (Belesky meadow fescue can also synthesize ergot alkaloids in
and Fedders, 1995; Malinowski and Belesky, 1999a). As contrast to the natural N. uncinatum-meadow fescue
a result, endophyte-infected grasses are more competi- association, which does not (Christensen, 1997). Ergot
MALINOWSKI & BELESKY: MECHANISMS OF STRESS TOLERANCE IN ENDOPHYTE-INFECTED GRASSES 925
alkaloids were detected in many endophyte-infected is referred to Bacon et al. (1997) for a thorough review
grass species other than Lolium spp. and Festuca spp. of endophyte–grass association effects on biotic factors
(Bacon et al., 1986; Miles et al., 1996). Lolitrem (indole including bacteria, fungi, nematodes, insects, and non-
diterpene) alkaloids [paxilline, paxitriol(s), lolitriol, loli- domesticated mammals.
trems] were first identified in symbiotic ryegrass plants Endophyte-infected grasses, in general, compete suc-
and related to livestock neurotoxicities known as rye- cessfully with non-infected conspecifics as well as with
grass staggers. The ability to produce lolitrems and paxil- other plant species and, in time, can dominate a sward
line has also been shown in vitro for cultures of N. (Clay and Holah, 1999). In some cases, the competitive
coenophialum and N. uncinatum (Penn et al., 1993), and advantage may result from morphological responses
in vivo in endophyte-infected tall fescue (Garthwaite, such as more massive and more numerous tillers (Hill
1997). The pyrrolopyrazine alkaloid peramine is pro- et al., 1990), greater leaf elongation rate (Eerens et
duced by endophyte-infected ryegrass, tall fescue, and al., 1993; Malinowski et al., 1997b), and altered root
other grasses (Siegel et al., 1990). Peramine has insect- architecture (Malinowski et al., 1999b). In others, endo-
feeding deterrent properties (Breen, 1994), but no ap- phyte-infected grasses may have direct chemical effects
parent activity against mammalian herbivores (Bush et (allelopathy) on the competitor. For example, the num-
al., 1997). Loline alkaloids (N-acetylloline, N-formyllo- ber of white clover (Trifolium repens L.) plants declined
line) are synthesized by endophyte-infected grasses in pastures dominated by endophyte-infected, com-
(Siegel et al., 1990; Porter, 1994) and they are potent pared with non-infected, perennial ryegrass (Percival
insecticides (Dahlman et al., 1997). In endophyte- and Duder, 1983; Sutherland and Hoglund, 1989). Seed
infected meadow fescue and tall fescue, the fungal com- extracts of endophyte-infected tall fescue inhibited ger-
ponent of the association seems to play a key role in mination of Trifolium spp. (Springer, 1997). Strong sup-
synthesis of loline alkaloids (Wilkinson et al., 1997). pression of leguminous companion species by endo-
Huizing et al. (1991) documented involvement of high phyte-infected tall fescue in a mixed sward could have
temperatures in loline alkaloid production by endo- significant negative effects on productivity and N econ-
phyte-infected perennial ryegrass. Loline alkaloids have omy of a sward. Loline alkaloids may be one such group
negligible effects on livestock compared with ergot or of endophyte-related secondary metabolites with allelo-
lolitrem alkaloids (Strickland et al., 1996), although pathic properties. Despite their role as insect deterrants,
their concentrations in endophyte-infected grasses are loline alkaloids were the only group of endophyte-
100 to 1000 times higher than those of other alkaloids related alkaloids shown to reduce germination rate of
(Siegel et al., 1989). Indole alkaloids (indoleglycerol, monocot and dicot seeds (Petroski et al., 1990); there-
indoleacetic acid) are products of tryptophan metabo- fore, loline alkaloids may enhance the competitive abil-
lism of endophyte, plant, and the symbiotum. Their ef- ity of endophyte-infected grasses by retarding the
fects on animal performance are not known. Indole al- establishment of competitors in a sward. Recently, allel-
kaloids have the potential to interfere with host plant opathic effects of lolines in endophyte-infected tall fes-
physiology and synthesis of other secondary metabolites cue-competitor associations have been reported by
by the symbiotum. Other miscellaneous alkaloids (er- Bush et al. (1997) and Malinowski et al. (1999a). Mali-
gosterol, ergostatetraeneone, ergosterol-peroxide, har- nowski et al. (1999a) observed that loline alkaloid con-
man, norharman, halostachine) found in endophyte-in- centration in roots of endophyte-infected tall fescue ge-
fected grasses may be involved in animal toxicities and notype DN2 was twice that detected in genotype DN11
may act as phytoalexins (antibiotics) as well (Latch, (1083 ␮g g⫺1 and 536 ␮g g⫺1, respectively). When both
1993). tall fescue genotypes were grown in binary mixtures
Non-alkaloid secondary metabolites occurring in tim- with red clover (Trifolium pratense L.), the relative yield
othy (Phleum pratense L.) infected with E. typhina total (RYT) of the red clover/DN2 tall fescue mixture
(Pers. : Fr.) have been classified as sesquiterpenoids, was less than 1.0 in response to endophyte infection (Fig.
fatty acids, and phenolic compounds (Yoshihara et al., 1). This suggested an allelopathic interaction between
1985; Koshino et al., 1988, 1989), while flavonoids have these two components of the mixture (Trenbath, 1974).
been detected in bluegrass (Poa ampla Merr.) infected In contrast, the RYT values of red clover binary mix-
with N. typhinum (Morgan-Jones and Gams) Glenn, tures with endophyte-infected DN11 and noninfected
Bacon and Hanlin (Ju et al., 1998). The ecological signif- DN2 and DN11 tall fescue were not significantly differ-
icance of these compounds in terms of biotic stress toler- ent from 1.0, indicating full competition for the same
ance of endophyte-infected grasses is unknown. limiting resources (Snaydon and Sattore, 1989). De-
Endophytes can indirectly reduce insect-transmitted tailed research with additional tall fescue genotypes is
viral diseases in grasses (West et al., 1990). Endophyte- needed to resolve the role of loline alkaloids in allelo-
infected grasses are more resistant than noninfected pathic effects of endophyte-infected grasses on other
grasses to soil-borne nematodes (West et al., 1988; plant species.
Eerens et al., 1997), with resistance probably attribut- Current efforts focus on development of endophytes
able to alkaloids present in roots (Malinowski et al., which, in association with grass hosts, produce little or
1998b, 1999a). Increased secretion of phenolic-like com- no ergot alkaloids toxic to livestock, yet retain pest- and
pounds from roots of infected tall fescue (Malinowski drought-resistance attributes of symbiotic plants. The
et al., 1998a) could act as feeding deterrents in the rhizo- impact of endophyte-mediated surrogate transforma-
sphere, although this remains to be resolved. The reader tion (Bacon and Hinton, 1998) on mechanisms of adap-
phyte-infected grasses. Responses of grass root system

to infection with shoot-located endophytes are not easy
to quantify because of difficulties in measuring root
characteristics. Malinowski et al. (1999b) showed that
endophyte infection increased root hair length and de-
creased root diameter in tall fescue. These traits could
increase root surface area for water and mineral acquisi-
tion. Because roots are the first plant organs to sense
water depletion in the soil, further research on root
activity of endophyte-infected grasses should clarify the
hypothesis of a water stress signaling system existing in
endophyte-infected grasses (West et al., 1994).
Control of Transpiration. Water deficits in plants in-
duce stomatal closure, which may benefit plants in the
short term by reducing water loss via transpiration
(Turner, 1986). Endophyte presence in shoots was
shown to affect stomatal behavior in tall fescue (Elmi
Fig. 1. Relative yield total (RYT) of red clover and endophyte-in- and West, 1995; Buck et al., 1997) and meadow fescue
fected (E⫹) and noninfected (E⫺) tall fescue genotypes DN2 and (Malinowski et al., 1997a, b), but apparently not in pe-
DN11 grown in binary mixtures. When endophyte-infected, the
concentration of loline alkaloids in roots of DN2 was twice that
rennial ryegrass (Barker et al., 1997). Stomatal conduc-
of DN11, indicating a possible allelopathic effects on red clover. tance of water-stressed endophyte-infected fescues (Fes-
Adapted from Malinowski et al. (1999a). tuca spp.) declined earlier and faster than that of
noninfected plants, suggesting more rapid stomatal clos-
tation and host survival in competitive environment and ing (Elbersen et al., 1994; Elmi and West, 1995). The
marginal edaphic conditions is unknown and warrants direct mechanism of this phenomenon is not known. A
investigation. biochemical signal from the endophyte or an altered
hormonal status in the host may predispose leaf blades
to respond quickly to early stages of water deficit
Adaptations and Mechanisms of Drought (Belesky et al., 1987a; West et al., 1994). The hypothe-
Stress Tolerance sized biochemical signal induced in endophyte–grass as-
Drought stress tolerance is the most thoroughly docu- sociations in response to water deficit may be interpre-
mented attribute of abiotic stress tolerance in endo- ted as an endophyte-related perturbance in host grass
phyte-infected grasses. Drought stress in temperate en- homeostasis. Endophyte, as a xenobiotic component of
vironments is usually a result of water deficit in the soil a grass plant, may induce a permanent internal stress
and high temperature. Water deficit induces a range of in the host grass. This may precondition or sensitize the
adaptations in plants that favor their growth or survival plant to drought and other stresses, thereby permitting
(Arraudeau, 1989). These adaptations include mecha- the plant to exhibit adaptive responses (such as stomata
nisms of drought avoidance, tolerance, and recovery closure) sooner than noninfected conspecifics. Recent
from drought. In our discussion, we will show that infec- research results on symptomless fungal endophytes and
tion with Neotyphodium spp. endophytes may induce their host plants suggest mutual defense responses in-
some adaptations and mechanisms of drought stress tol- volving a range of secondary metabolites produced in
erance in cool-season grasses and ensure a better sur- much higher quantities than observed in plant-fungal
vival than noninfected conspecifics. pathogen interactions (Schulz et al., 1999). The authors
hypothesize that both the pathogen-host and the endo-
Drought Avoidance phyte-host interactions involve constant mutual antago-
Drought-avoiding plants possess a variety of morpho- nisms at least in part based on the secondary metabolites
logical and physiological adaptations to maintain favor- the partners produce. Whereas the pathogen-host inter-
able water status, either by maintaining an efficient wa- action is imbalanced and results in a disease, that of
ter supply to aboveground organs or conserving water the endophyte and its host is a balanced antagonism.
during periods of soil water deficit (Clarke and Durley, Responses suggest that host grasses recognize Neoty-
1981). The adaptations may be divided into three basic phodium spp. endophyte infection by inducing a range
groups: (i) improved water uptake from the soil by an of defense mechanisms similar to those against patho-
extensive root system, (ii) reduced transpiration losses, genic fungi. Circumstantial evidence for defense mecha-
and (iii) water storage in plant tissues. nisms of grasses to endophyte infection includes the
Extensive Root System. Improved water uptake from presence of chitinase (a pathogenesis-related protein)
the soil may be promoted by a deeper and denser root (Roberts et al., 1992), resveratrol (a phenolic compound
system (Arraudeau, 1989). In response to endophyte with antifungal activity correlated with disease resis-
infection, increased root dry matter (DM) has fre- tance) (Powell et al., 1994), and increased concentration
quently been reported in perennial ryegrass (Latch et of phenolic-like compounds in shoots and roots com-
al., 1985), tall fescue (De Battista et al., 1990), and pared with noninfected grasses (Malinowski et al.,
meadow fescue (Malinowski et al., 1997a, b). A direct 1998a). Novel endophyte–grass associations may be
relationship between the size of root system and drought highly incompatible (Koga et al., 1993; Christensen et
tolerance, however, has not been documented for endo- al., 1995). This incompatibility may be a result of fungal
problems with enzymatic degradation of the middle la- status. In contrast, Elbersen and West (1996) ob-
mella of host cell walls, which in turn would restrict the served lower proline concentrations in three
nutritional supply within the apoplast of host tissues drought-stressed endophyte-infected genotypes of
(Leuchtmann, 1994), also suggesting multifaceted de- tall fescue compared with their noninfected iso-
fense responses. lines in a field experiment, suggesting that endo-
Water Storage in Plant Tissues. Water content of tiller phyte-infected plants were less stressed than non-
bases of some endophyte–grass associations may be infected plants. Under field conditions, however,
maintained at higher levels than those in noninfected lower concentrations of proline in endophyte-in-
plants during drought (Elbersen and West, 1996; Buck fected tall fescue plants could be related not only
et al., 1997). This phenomenon may be explained by to water stress but to other factors (e.g., mineral
enhanced accumulation of solutes in tissues of endo- status) as well. In meadow fescue, proline accumu-
phyte-infected plants compared with noninfected plants, lation during imposed single water stress cycle was
or by reduced leaf conductance and a slow-down of the not affected by endophyte, but proline metabolism
transpiration stream, or thicker cuticle. (proline degradation rate) during recovery was
slower in endophyte-infected plants compared
Drought Tolerance with genetically identical, noninfected plants (Ma-
Drought tolerance refers to physiological and bio- linowski, 1995). This might suggest a residual effect
chemical adaptations that enable plant tissues to with- which predisposes endophyte-infected plants to
stand water deficits (Clarke and Durley, 1981). In most rapid adjustment when undergoing subsequent
grasses, a combination of drought avoidance and toler- drought stress events. Proline metabolism may be
ance mechanisms determines the survival potential dur- affected in endophyte-infected grasses because
ing drought. Mechanisms of drought tolerance have proline is a product of ergot alkaloid breakdown
been divided into three major groups: (i) accumulation (Stoll and Hofmann, 1965) and peramine synthesis
and translocation of assimilates, (ii) osmotic adjustment, (Siegel et al., 1990).
and (iii) maintenance of cell wall elasticity (Arraudeau, 4. Other amino acids. Belesky et al. (1984) showed
1989). All these mechanisms can be affected by endo- that water stress increased accumulation of amino
phyte infection in grasses. acids in endophyte-infected tall fescue but the re-
Accumulation and Translocation of Assimilates. Ac- sults were not compared to noninfected plants.
cumulation of carbohydrates during growth under non- Nitrogen fertilization increased amino acid con-
drought conditions and translocation during imposed centrations in endophyte-infected, compared to
drought stress may contribute to drought tolerance. In noninfected, tall fescue (Lyons et al., 1990), with
some endophyte–tall fescue associations, endophyte- greater accumulation in leaf sheaths (where the
infected plants had greater concentrations of total non- fungal hyphae are present in great number) than
structural carbohydrates in tillers than noninfected blades (less frequent hyphae).
plants when grown under non-limiting water supply 5. Loline alkaloids. Loline alkaloids are produced by
(Hill et al., 1990). Water-stressed endophyte-infected some endophyte-infected grass species (Bush et
plants of tall fescue genotype CB1 accumulated more al., 1993). Because loline alkaloids are water solu-
glucose and fructose in leaf blades and leaf sheaths than ble, they may act as osmoregulators (Bacon, 1993).
noninfected plants (Richardson et al., 1992). These car- The concentration of loline alkaloids in plant tis-
bohydrates are osmotically active and may play a role sues may exceed 8 g kg⫺1 DM, which could affect
in endophyte-related osmotic adjustment in tall fescue. osmotic potential (Kennedy and Bush, 1983; Bush
Osmotic Adjustment. Accumulation of solutes in tis- et al., 1993). The presence of loline alkaloids in
sues in response to drought helps maintain turgor and roots of endophyte-infected tall fescue (Bush et
facilitates physiological and biochemical processes. The al., 1993; Malinowski et al., 1999a) suggests that,
following groups of solutes have been particularly con- once metabolized by the shoot-located fungus,
sidered to contribute to osmotic adjustment in endo- they may be translocated within the plant to zones
phyte-infected grasse. lacking the fungus, such as roots and meristematic
1. Water-soluble sugars (Richardson et al., 1992). tissues (Justus et al., 1997). The evidence for
2. Fungal metabolites mannitol and arabitol (polyols) involvement of loline alkaloids in drought toler-
(Richardson et al., 1992). ance of endophyte-infected grasses is circumstan-
3. Amino acid proline. Accumulation of proline in tial at this time (Bacon and Hinton, 1998). Endo-
plant tissues in response to drought is common phyte-infected tall fescue and meadow fescue
and is correlated with drought resistance in many contain high levels of loline alkaloids, and both
crops (Hsiao, 1973). Proline may be an osmotically grasses express greater drought tolerance than do
active metabolite (Joyce et al., 1992). Increased noninfected plants (Bacon, 1993; Malinowski et al.,
proline concentration was not related to osmotic 1997a,b). In contrast, endophyte-related increase
adjustment in drought stressed Lolium spp. and in drought tolerance could not be confirmed for
Festuca spp. grasses (Thomas, 1991; Barker et al., perennial ryegrass (Barker et al., 1997), where lo-
1993; Abernethy and McManus, 1998; Abernethy line alkaloids occur in low concentrations. The con-
et al., 1998). Belesky et al. (1984) likewise did not centration of loline alkaloids in tall fescue in-
find a drought-stress related proline accumulation creased in response to soil water deficit (Belesky
in tall fescue of unspecified endophyte infection et al., 1989b) and high temperature during summer
(Robbins et al., 1973). In contrast, Kennedy and absorb water. Higher values of the TW/DW ratio indi-
Bush (1983) could not confirm high temperature cate less damaged cell walls. Similar to tall fescue, the
effects on loline alkaloid accumulation in tall fes- TW/DW ratio in meadow fescue leaves was also higher
cue in growth chamber experiments. The influence in response to endophyte infection during imposed wa-
of high temperature on loline alkaloid synthesis in ter stress (Malinowski, 1995). These results suggest that
perennial ryegrass was shown by Huizing et al. in response to water stress, endophyte may alter cell
(1991) and may explain the absence of loline alka- wall characteristics in a similar way in both grass species.
loids in perennial ryegrass in previous studies con- At this time, it is not known which metabolites are
ducted under optimal temperatures for cool-sea- directly involved in the process.
son perennial grasses (Gleason et al., 1990).
Production of loline alkaloids in field-grown tall Water Use Efficiency
fescue and meadow fescue varied seasonally
One adaptation to drought stress in plants is efficient
(Belesky et al., 1987b; Justus et al., 1997). In endo-
water use. Considerable research has been conducted
phyte-infected tall fescue, loline alkaloids are accu-
concerning limitations to efficient water use in grass
mulated in greater amounts in response to drought production and improving water use efficiency (WUE)
and during recovery from drought (Bush et al., in grasses (reviewed in Johnson and Asay, 1993). The
1993, 1997). WUE measures the ability to limit water loss while
Future research should resolve the role of loline alka- maintaining net carbon uptake in the leaves. Because
loids in drought tolerance of cool-season grasses. One endophyte-infected grasses can reduce water loss
approach may be a comparison of drought stress re- through stomatal closure during soil drying, they may
sponses between endophyte-infected plants producing be better able to prolong assimilation or resume growth
loline alkaloids and endophyte-infected plants with a after drought more rapidly than noninfected grasses
disturbed pattern of loline alkaloid synthesis. Loline (West, 1994). Experimental results are not consistent in
alkaloids are synthesized from two polyamines, putres- support of this hypothesis (Belesky et al., 1987a; Marks
cine and spermidine (Bush et al., 1993; Graser and Hart- and Clay, 1996). Under water non-limiting conditions
mann, 1997). Spermidine is supposed to be the precursor in a greenhouse, instantaneous water use efficiency
of the pyrrolizidine ring system of loline alkaloids (Bush (PWUE, ratio of photosynthesis:transpiration rates on
et al., 1993). At this time, it is not known if the loline unit leaf area basis) calculated from data reported by
alkaloid precursors putrescine and spermidine are of Richardson et al. (1990) tended to be higher in leaves
fungal or host origin. If loline alkaloids were produced of endophyte-infected tall fescue genotypes than in non-
from fungal-derived polyamines, a disturbed pattern of infected conspecifics. In contrast, PWUE values of
polyamine synthesis by endophyte might affect synthesis drought-stressed endophyte-infected tall fescue geno-
of loline alkaloids in the symbiotum. This could create types were lower than those of noninfected plants (Bates
a basis for a precise identification of physiological mech- and Joost, 1990). The latter results showed, however,
anisms of abiotic stress tolerance in endophyte-infected that noninfected tall fescue plants reduced PWUE more
grasses directly related to loline alkaloid action. Certain rapidly than endophyte-infected plants as soil water def-
chemicals have been shown to disturb polyamine syn- icit increased, suggesting less efficient adaptation to wa-
thesis in fungi with negligible effects on plant-synthe- ter stress.
sized polyamines and plant growth (Elghachtouli et al., In cool-season grasses and other plant species that
1996; Walters and Macintosh, 1997). For example, ␣- fix carbon by the C3 pathway, WUE is related to the
difluoromethylornitine (DFMO) is an inhibitor of orni- stable 13C isotope composition of tissues and can be
thine decarboxylase, and ␣-difluoromethylarginine indirectly estimated from the 13C to 12C ratio in the
(DFMA) inhibits arginine decarboxylase (Walters and biomass (Johnson and Bassett, 1991). Plants discrimi-
Macintosh, 1997). These inhibitors may suppress polya- nate against 13C during the process of photosynthesis
mine synthesis by endophyte and affect loline alkaloid and the 13C discrimination (⌬) is described as:
production in the host. If endophyte could synthesize ⌬ ⫽ (13CO2/12CO2 [sample]/13CO2/12CO2 [standard]
loline alkaloids from grass-originated polyamines, fun-
gal polyamine inhibitors might not affect loline alkaloid ⫺ 1) ⫻ 1000 (Tieszen and Grant, 1990).
synthesis in infected grasses. To date, there is no pub- Theoretically, the ⌬ gives an integrated estimate of the
lished information of endophyte effects on polyamine ratio of leaf intercellular CO2 concentration (Ci) to am-
accumulation and involvement of polyamines in drought bient CO2 concentration (Ca) at constant vapor pressure
stress-related accumulation of loline alkaloids in in- difference (Johnson and Bassett, 1991). Drought-
fected grasses. stressed endophyte-infected grasses have a reduced
Maintaining Cell Wall Elasticity. Cellular (tissue) transpiration rate because of a more rapid stomatal clo-
elasticity enables cell size to change in synchrony with sure than noninfected plants (Elbersen et al., 1994; Elmi
water availability (Arraudeau, 1989). White et al. (1992) and West, 1995). Therefore, one would also expect a
showed that endophyte infection lowered bulk modulus reduced carbon fixation rate in endophyte-infected
of tissue elasticity (suggesting less rigid cell walls) and grasses due to a lower Ci/Ca ratio and, in consequence,
increased turgid weight:dry weight (TW/DW) ratio in higher ⌬ values (Johnson, 1993). Because the ⌬ is nega-
water stressed tall fescue. The TW/DW determines wa- tively correlated with WUE (Farquhar et al., 1989; Read
ter uptake capacity and reflects the ability of cells to et al., 1991), endophyte-infected grasses are expected
to have lower WUE than noninfected plants under fertilization reduced concentration of this alkaloid
drought. A limited number of experiments on ⌬ and (Gentry et al., 1969). After the discovery of endophyte
WUE in endophyte-infected grasses do confirm this hy- and its role in alkaloid synthesis in the host grass, man-
pothesis. In a population of Kentucky-31 tall fescue, agement practices were developed to reduce alkaloid
Johnson and Tieszen (1993) observed lower mean ⌬ in production and toxicity of tall fescue. One of the first
noninfected plants compared with endophyte-infected management strategies was manipulating N nutrition.
plants in response to drought. Although the authors
considered this result as preliminary, it might suggest Nitrogen
that endophyte-infected plants had lower WUE than
noninfected plants. In other words, endophyte-infected High rates of N fertilizer increased the concentration
plants might be more conservative than noninfected of ergopeptine alkaloids in controlled-environment (Ly-
plants by reducing growth during drought and conserv- ons and Bacon, 1984) and field grown endophyte-
ing water in the soil–plant system. Detailed results on infected tall fescue (Belesky et al., 1988). Increasing N
WUE in perennial ryegrass confirmed that endophyte- fertilization from 134 kg ha⫺1 to 334 kg ha⫺1 increased
infected plants had lower WUE than noninfected plants the concentration of total ergopeptine alkaloids by 60%
in response to drought (Eerens et al., 1998). Interest- to 80%, depending on the year (Belesky et al., 1988).
ingly, endophyte-infected plants of perennial ryegrass Using a single clone of Kentucky-31 tall fescue, Arecha-
were less wilted (thus less stressed) than noninfected valeta et al. (1992) showed that accumulation of ergot
plants because of improved water status characteristics. alkaloids increased not only in response to N fertiliza-
Results suggest that endophytes do not directly affect tion but was also dependent on N source. In that experi-
water use efficiency in drought-stressed grasses. Endo- ment, ergot alkaloids were not detected at a very low
phytes appear to help maintain physiological and bio- N level in the soil (11 mg pot⫺1). In contrast, concentra-
chemical processes at the cost of reduced growth during tions of ergovaline and total ergopeptides were 0.41 and
drought and facilitate rapid regrowth of host grasses 0.57 ␮g mg⫺1 DM, respectively, at a high N level (220
soon after soil water becomes available. mg pot⫺1). The NH4⫹ form of applied N had a greater
Recovery mechanisms determine the ability of plants effect on accumulation of ergot alkaloids than the
to regrow when drought stress is relieved. In endophyte- NO3⫺ form. The concentration of loline alkaloids is also
infected grasses, these mechanisms include a rapid water affected by N fertilization. Belesky et al. (1987b) showed
uptake by roots and the ability of tissues to restore that greater loline alkaloid concentrations on a unit of
physiological functions. Endophyte effects on growth endophyte infection rate were associated with increased
and water relations in grasses were observed during the N availability in the soil.
weeks following water stress (West et al., 1994; Mali- It is well known that N fertilization increases herbage
nowski et al., 1997b). West et al. (1994) postulated that yield of grasses. Clay (1987) analyzed endophyte effects
endophyte effects on growth and drought tolerance may on DM production of tall fescue and perennial ryegrass
be more important for grass persistence during recovery seedlings grown under optimal nutrient supply (weekly
from drought than during the onset of drought. applied soluble fertilizer 20:20:20 NPK, 1 g L⫺1). For
Although responses of endophyte-infected grasses to both species, tiller number and above-ground biomass
drought have been well documented, the understanding of endophyte-infected plants were greater than those
of mechanisms by which endophytes enhance host grass of noninfected plants. Cheplick et al. (1989) found that
survival during drought is incomplete. Endophyte infec- DM production by seedlings of tall fescue and perennial
tion of grasses induces a range of responses to water ryegrass depended on nutrient availability and endo-
deficit that are a combination of drought avoidance, phyte infection. Seedling DM of endophyte-infected
tolerance and recovery mechanisms. These responses ryegrass was greater at intermediate (biweekly applied
may or may not be expressed by a particular endophyte– soluble fertilizer 20:20:20 NPK, 0.15 g L⫺1) and high (1.5
grass association, but the sum of responses of individual g L⫺1) nutrient levels compared with noninfected plants
endophyte–grass associations determines the ecological but no differences in plant biomass were observed when
success of a given grass population (West, 1994). As a no nutrients were added. In contrast, endophyte infec-
result, the range of adaptation of endophyte-infected tion reduced biomass of tall fescue seedlings at low
cool-season grasses can be extended into areas domi- nutrient level but increased plant biomass at high nutri-
nated by warm-season grasses which can help improve ent level. Endophyte-infected adult plants of tall fescue
pasture productivity (Bouton et al., 1993; Cunningham produced more biomass than did noninfected plants,
et al., 1994). whereas adult ryegrass plants did not respond to endo-
phyte infection, regardless of nutrient availability. On
the basis of these results, the authors concluded that
Adaptations and Mechanisms endophyte infection might induce an additional meta-
of Mineral Stress Tolerance bolic cost to the host plant grown under mineral stress
Alkaloids in tall fescue were reported long before conditions. Plants used by Cheplick et al. (1989) repre-
the discovery of its associated endophyte (Yates, 1962, sented a population. As such, they varied in the genetic
1963), and before close relationships between alkaloid make up, thus endophyte-related effects on growth were
concentrations in tall fescue herbage and mineral nutri- inconsistent. Belesky et al. (1991) showed that endo-
tion were identified. For example, greater N fertilization phyte did not affect carbohydrate accumulation in field-
increased concentrations of perloline while P and K grown tall fescue populations grown either at low (134
kg ha⫺1) or high (336 kg ha⫺1) N availability. The authors

concluded that endophyte was not detrimental to the
host grass grown at low soil N level. Working on geneti-
cally identical plants, Belesky et al. (1989a) found that
four of five tall fescue clones produced more biomass
(15% on the average) in response to endophyte infec-
tion when grown at optimal N level of 150 mg kg⫺1
soil and adequate water supply. A detailed study by
Arachevaleta et al. (1989) showed that N-use efficiency
was greater in endophyte-infected plants. In response
to endophyte infection, plants of a tall fescue clone
derived from cv. Kentucky-31 grown at low (11 mg
pot⫺1) N level produced a similar herbage DM to nonin-
fected plants grown at high (220 mg pot⫺1) N level. With
increased N supply, the difference between endophyte-
infected and noninfected plants became more dramatic
as shown by a 100% and a 50% increase in herbage
DM, respectively for plants grown at 73 and 220 mg
N pot⫺1.
Proline and amino acid concentrations in Kentucky-
31 tall fescue populations (the degree of endophyte in-
fection not determined) depended on soil N availability
(Belesky et al., 1982, 1984). Similarly, amino acid con-
centrations were greater in endophyte-infected than in
noninfected tall fescue as N fertilization increased
(Belesky et al., 1984). Lyons et al. (1990) observed a
greater accumulation of amino acids in leaf sheaths than
blades of tall fescue. An endophyte-related increase in
total amino acid concentration was significant only at
high N level (10 mM ) but no effects were observed at
low N level (0.5 mM). They found an endophyte-related
increase in sheath NH4⫹ concentrations and decrease in Fig. 2. Root and shoot DM of endophyte-infected (E⫹) and nonin-
sheath and blade NO3⫺ concentrations, which suggested fected (E⫺) tall fescue (averaged over four genotypes) as a function
of soil P availability. Adapted from Malinowski et al. (1998b).
an endophyte effect on nitrogen metabolism in tall fes-
cue. A detailed investigation showed that endophyte-
infected plants had greater activity of glutamine synthe- single clone of perennial ryegrass grown in nutrient solu-
tase, an enzyme responsible for NH4⫹ reassimilation, tions at low (3 ␮M NH4NO3) and high (30 ␮M NH4NO3)
regardless of N availability. This mechanism helped ex- N levels, endophyte infection did not affect either DM
plain a more efficient use of N by endophyte-infected production or N uptake (Lewis et al., 1996). In an experi-
tall fescue as previously shown by Arachevaleta et al. ment by Ravel et al. (1997) with three clones of peren-
(1989). Alteration of N metabolism by endophyte in tall nial ryegrass, endophyte-infected plants had more
fescue appears to involve both assimilatory and basic leaves and tended to have more tillers than noninfected
nitrogen metabolism (Lyons et al., 1990) and may be plants when grown at low (2.33 mM) N level in the
correlated with mechanisms of in vitro N utilization soil. Dry matter yield, however, was not affected by
by endophyte mycelium. Kulkarni and Nielsen (1986) endophyte, confirming results by Lewis et al. (1996).
showed that a N. coenophialum strain could assimilate They suggested that photosynthesis was similar for en-
NH4⫹ but not NO3⫺ as a source of N from the growth dophyte-infected and noninfected plants grown under
medium. In contrast, three out of four N. coenophialum N deficiency. Interestingly, endophyte-infected plants
isolates from Kentucky-31 tall fescue analyzed by Fergu- compensated for lower net photosynthesis with an in-
son et al. (1993) could utilize NO3⫺ and all of them could creased number of green leaves compared with nonin-
utilize NH4⫹ as N source. Naffaa et al. (1998b) examined fected plants. Malinowski (1995) observed no significant
growth of endophytes from 12 grass species of Poaceae effect of endophyte on N use efficiency (DM produced
and found that all of them (including N. lolii) could per unit of uptaken N) of meadow fescue grown under
assimilate NH4⫹ but only A. chilense-like endophytes (a- nonstressed (daily supply with 7.5 mM N nutrient solu-
endophytes) could assimilate NO3⫺. These results sug- tion) conditions, regardless of soil water content. Cloned
gest a considerable variability in N utilization among genotypes of Arizona fescue infected with a Neotypho-
endophyte isolates from different grass species. It re- dium spp. endophyte had a greater herbage DM at low
mains to be resolved if increased N use efficiency in soil N level but no responses were observed at high soil
grasses could be directly (fungal enzymes) or indirectly N level compared with noninfected plants (Louis and
(stimulation of the host enzymes) related to endo- Faeth, 1997). In a subsequent study with grazed popula-
phyte infection. tions of Arizona fescue, Schulthess and Faeth (1998)
Responses of endophyte-infected grasses, other than found more N. starri-infected plants at a location with
tall fescue, to N nutrition are less well studied. In a the lowest soil N concentration (about 0.6 mg kg⫺1) than
Fig. 3. Concentrations of P, Mg, and Ca in roots and shoots of endophyte-infected (E⫹) and noninfected (E⫺) tall fescue (averaged over four
genotypes) as a function of soil P availability. Adapted from Malinowski et al. (1998b).
at a location with the highest soil N concentration (about related to specific endophyte strain–tall fescue genotype
2.0 mg kg⫺1). These results suggest that endophyte bene- association (Azevedo et al., 1993). In a subsequent study
fits in cool-season grasses depend on specific endo- (Azevedo and Welty, 1995), endophyte hyphae accumu-
phyte–host associations and site nutrient availability lated inorganic P, similar to that found in mycorrhizal
conditions. fungi (White and Brown, 1979; Lapeyrie et al., 1984).
Such P reserves in endophyte hyphae might benefit grass
Phosphorus host under low soil P conditions.
Phosphorus is involved in ergot alkaloid biosynthesis Our research group conducted a series of experiments
in Claviceps spp., a fungus related to clavicipitaceous to clarify the role of endophyte in tall fescue tolerance to
grass endophytes (Robbers, 1984; Flieger et al., 1991). P deficiency. We grew four tall fescue cloned genotypes
A high P concentration restricted the activity of the first (DN2, DN4, DN7, and DN11) infected with endemic
enzyme in the biosynthesis pathway of ergot alkaloids, endophytes and their noninfected clones in an acidic,
dimethylallyl tryptophan synthase (DMATase), in in high Al content soil at three P levels of 17, 50, and
vitro grown Claviceps spp. A similar pathway of ergot 96 mg kg⫺1 (Malinowski et al., 1998b). The P levels
alkaloid biosynthesis is proposed for grass endophytes represented low, medium, and high P fertilization rates
within the Clavicipitaceae (Garner et al., 1993; Glenn appropriate for acidic soils (Wright et al., 1987). Endo-
and Bacon, 1997). Phosphorus nutrition, therefore, has phyte-infected plants had less root and shoot DM com-
been postulated to affect ergot alkaloid production and pared with noninfected plants as P availability increased
growth of Neotyphodium spp. infected grasses (Por- (Fig. 2). At low and medium P levels, specific root length
ter, 1994). of endophyte-infected tall fescue was considerably
Detailed studies on P involvement in growth and er- greater than that of noninfected plants suggesting a finer
got alkaloid production in endophyte-infected tall fes- root system. Concentrations of P, magnesium (Mg), and
cue were initiated by Azevedo (1992) and Azevedo et calcium (Ca) in roots and shoots were greater in re-
al. (1993). The authors investigated two cloned geno- sponse to endophyte infection only when plants were
types of Kentucky-31 tall fescue, DN7 and DN11, grown grown at low soil P level (Fig. 3). Concentrations of
at contrasting soil P levels determined as deficient (0.02 ergot alkaloids were increased in low ergot alkaloid
mg kg⫺1 P) to sufficient (2.0 mg kg⫺1 P). These tall fescue genotypes DN2 and DN4 as P fertilization increased.
clones produce low (DN7) and high (DN11) amounts of In contrast, ergot alkaloid production in high ergot alka-
ergot alkaloids when endophyte-infected, and have been loid genotypes DN7 and DN11 reached a peak at me-
used extensively to study endophyte effects on tall fes- dium soil P level and declined with a further increase
cue growth and physiology (Belesky et al., 1989a,b; Hill in soil P availability. Interestingly, Al concentration in
et al., 1990, 1996). Growth and photosynthesis rates roots was greater than in shoots of endophyte-infected
of both endophyte-infected tall fescue genotypes were plants compared with noninfected plants, suggesting an
reduced compared to noninfected plants as P availability Al sequestration mechanism located in/on the roots of
in the soil increased. Endophyte appeared to be a sink endophyte-infected tall fescue. The results show that
for P (Azevedo, 1992). The production of ergovaline endophyte infection does not benefit tall fescue growth
was a function of increased P availability and was not as P availability in the soil increases, and that manipulat-
Fig. 4. Root DM of tall fescue genotypes DN2 and DN4 grown in a Fig. 5. Root diameter and root hair length of tall fescue (averaged
P-deficient soil supplied with phosphate rock (PR) and in vitro P over genotypes DN2 and DN4) grown in P-deficient and P-suffi-
solubility (from PR) by tall fescue root exudates in response to cient nutrient solution as a function of endophyte infection (E⫺,
infection with the leaf fungal endophyte, N. coenophialum (E⫺, noninfected; E⫹, infected). Adapted from Malinowski et al.
noninfected; E⫹, infected). Adapted from Malinowski and (1999b).
Belesky (1999a).
ing P nutrition may reduce or increase production of of root exudates. Both of those mechanisms might be
ergot alkaloids, depending on particular endophyte–tall differently expressed in a particular endophyte–tall fes-
fescue associations. cue association.
Negligible responses of root and shoot DM to endo- We cultivated the same endophyte–tall fescue associ-
phyte infection in tall fescue grown at low soil P level ations in P-deficient (0.31 mg P L⫺1) and P-sufficient
and increased concentrations of P, Mg, and Ca in plant (31 mg P L⫺1) nutrient solutions (Malinowski et al.,
tissues suggested an endophyte-related mechanism of 1999b). In response to P deficiency, endophyte-infected
mineral uptake. In a subsequent study (Malinowski and plants produced roots with smaller diameters and longer
Belesky, 1999a), we investigated growth of two tall fes- root hairs (Fig. 5), which may increase the root surface
cue genotypes (DN2 and DN4) at low (about 10 mg area that functions in mineral acquisition (Foehse and
kg⫺1) soil P level where P was supplied in a readily Jungk, 1983). These endophyte-related adaptations in
available form of commercial fertilizer or less available root morphology of hydroponically grown tall fescue to
form of phosphate rock. Endophyte-related increase in P deficiency agreed with our previous observations of
root DM (10%), relative growth rate (16%), and P up- a modified specific root length in soil-grown tall fescue
take rate (24%) were observed in plants grown with (Malinowski et al., 1998b). Therefore, we proposed
phosphate rock but no significant effects of endophyte longer root hairs and smaller root diameters of endo-
were observed in plants grown with commercial P fertil- phyte-infected plants as one mechanism of P deficiency
izer. Interestingly, endophyte infection increased root tolerance induced in tall fescue by its endophyte.
growth in tall fescue genotype DN4 but no significant We were interested in the nature of exudates released
effect was observed in genotype DN2 grown with phos- by tall fescue roots in response to endophyte infection
phate rock (Fig. 4). In contrast, the activity of root under P-deficient conditions (Malinowski and Belesky,
exudates in dissolving P from phosphate rock was in- 1999a). On the basis of our preliminary observations on
creased by 100% in response to endophyte infection in genotypes DN2, DN4, DN7, and DN11, we applied a
DN2 but no endophyte effects were observed in DN4 technique to visualize chemical changes in the rhizo-
(Fig. 4). We concluded that endophyte might induce at sphere of tall fescue in response to endophyte infection
least two mechanisms of mineral uptake in response to and P deficiency (Malinowski et al., 1998a). Roots of
P deficiency: alteration in root morphology and activity endophyte-infected plants released exudates (identified
Fig. 6. Fe3⫹ reducing activity of exudates from intact roots of tall

fescue (averaged over genotypes DN2, DN4, DN7, and DN11) in
response to endophyte infection (E⫺, noninfected; E⫹, infected)
and P availability in the growth medium during a 24-h measurement
cycle. Adapted from Malinowski et al. (1998a).
as phenolic-like compounds) with a higher iron (Fe3⫹)

reducing activity than those of noninfected plants (Fig.
6). The Fe3⫹ reducing activity was located on the root
surface and limited to the zones of active nutrient up-
take. Concentrations of phenolic-like compounds in
roots and shoots of endophyte-infected tall fescue were
greater than those in noninfected plants only under P-
deficient conditions (Fig. 7). A release of phenolic-like
compounds by tall fescue roots was previously reported
by Creek and Wade (1982) in plants with undetermined
endophyte status. Phenolics can increase P availability
in the soil by binding soluble Al, Fe, and manganese
(Mn), which can otherwise render P unavailable (Kaf- Fig. 7. Concentrations of water soluble (W) and ethanol:water (50:50
kafi et al., 1988; Appel, 1993). The mechanism responsi- v/v) soluble phenolic compounds (EW) in roots and shoots of
endophyte-infected (E⫹) and noninfected (E⫺) tall fescue (aver-
ble for production of phenolic-like compounds by endo- aged over genotypes DN2, DN4, DN7, and DN11) as a function
phyte-infected tall fescue in response to P deficiency of P availability in the growth medium. Adapted from Malinowski
is not known. We suggest that endophyte, despite the et al. (1998a).
mutualistic relationship, may induce an internal stress
in tall fescue and, under certain stress conditions, trigger (1996) observed greater Al tolerance in endophyte-in-
a range of defense mechanisms in the host plant similar fected fine fescues (Festuca spp.) compared with nonin-
to those induced by infection with pathogenic fungi. fected plants in terms of DM accumulation. On the basis
Circumstantial evidence supports our hypothesis. Pow- of our previous findings (Malinowski et al., 1998a), we
ell et al. (1994) reported an endophyte-related increase suggested that phenolic-like compounds released in
in the concentration of resveratrol, a phenolic com- greater amounts by roots of tall fescue in response to
pound, in a range of cool season grasses. Resveratrol endophyte infection and mineral stress might contribute
has antifungal activity and has been correlated with to Al stress tolerance. Phenolics can chelate Al
disease resistance in plants (Siemann and Creasy, 1992). (Marschner, 1986) and may facilitate transport of Al
Chitinase, a pathogenesis related protein, was found in within a plant in nontoxic forms (Taylor, 1988). We
greater concentrations in roots and shoots of endophyte- evaluated two (DN2 and DN4) of the endophyte–tall
infected tall fescue compared with noninfected, geneti- fescue associations investigated by Malinowski et al.
cally identical conspecifics (Roberts et al., 1992). Occur- (1998a) for exudation of phenolic-like compounds by
rence of resveratrol and chitinase suggests that endo- roots under high Al (640 ␮M Al) conditions (Malinow-
phyte may influence the host to induce a range of ski and Belesky, 1999b). Endophyte infection did not
defense responses. affect DM production of Al-stressed tall fescue but the
relative (to no Al) reduction in root and shoot DM was
Aluminum greater in endophyte-infected than noninfected plants.
Foy and Murray (1998) showed that tall fescue accu- This suggested a negative effect of endophyte infection
mulated considerably less Al in shoot than root tissues, in terms of DM production under Al stress. Concentra-
suggesting an efficient mechanism for Al sequestration tions of Al in shoots were not affected by endophyte
in or on the roots. The endophyte status in experimental and were about 10 fold less when compared with Al
plants was not determined by the authors. Liu et al. concentrations in roots, suggesting an Al sequestration
cue genotype (DN2) but the responses were not consis-

tent in another genotype (DN4) (1998, unpublished
data). This confirms a frequently reported specificity of
endophyte–grass associations in responses to environ-
mental stresses. Copper (Cu) concentration was lower in
herbage of endophyte-infected Kentucky 31 tall fescue
grown in greenhouse (Dennis et al., 1998). Allen et al.
(1997) observed the same response in field experiments
in Virginia, but an opposite one in Mississippi. Steers
fed endophyte-infected tall fescue forage with low Cu
had reduced Cu concentrations in serum compared with
steers fed noninfected forage (Saker et al., 1998). Ap-
parently, uptake of mineral elements by symbiotic plants
may be controlled by a range of factors including tall
fescue genotype, endophyte strain, and environmental
conditions.
An endophyte-enhanced release of phenolic-like
Fig. 8. Relationship between root DM and amount of Al desorbed
compounds with Fe3⫹- reducing activity into the rhizo-
from root surfaces of tall fescue (averaged over genotypes DN2 sphere (Malinowski et al., 1998a) may affect Fe uptake
and DN4) as a function of endophyte infection (E⫺, noninfected; by tall fescue. The mechanism of Fe uptake in grasses
E⫹, infected). Adapted from Malinowski and Belesky (1999b). involves nonproteinogenic amino acid carriers (phytosi-
derophores) (Tagaki, 1976; Marschner, 1986). Recently,
mechanism as proposed by Foy and Murray (1998) and an alternative mechanism has been reported for mycor-
Malinowski et al. (1998b). Roots of endophyte-infected rhiza-infected sorghum [Sorghum bicolor (L.) Moench]
plants accumulated 35% more Al than did roots of non- (Caris et al., 1998). The authors reported a direct
infected plants (excluded Al removed from root surfaces involvement of mycorrhizal fungi in Fe mobilization or
by citric acid). Most of the total Al (94%) could be uptake and transfer into the host plant. Phytosidero-
removed from root surfaces and cortical free spaces phores exuded by grass roots form highly stable com-
by citric acid, which confirms an efficient sequestration plexes with Fe3⫹ (Mino et al., 1983) but not with Fe2⫹
mechanism. The concentration of Al desorbed from (Beneš et al., 1983). The Fe3⫹ chelates are transported
root surfaces was 46% greater in response to endophyte into root cells where Fe3⫹ is reduced to Fe2⫹ and used
infection. Calculated on a basis of root DM, more Al in biochemical processes. Because endophyte-infected
was sequestered on root surfaces of endophyte-infected tall fescue had greater Fe3⫹ reducing activity on root
plants compared with noninfected plants (Fig. 8). We surfaces (Malinowski et al., 1998a) compared with non-
did not analyze phenolic-like compound concentrations infected plants, Fe uptake may be indirectly affected by
in this experiment. On a basis of our previous results
endophyte. More detailed research is required to resolve
(Malinowski et al., 1998a), however, we suggest that
the relationship between rhizosphere chemistry and Fe
phenolic-like compounds may contribute to increased
uptake by endophyte-infected tall fescue.
Al sequestration on tall fescue roots in response to endo-
phyte infection. Increased production of root exudates
in response to mineral stresses requires a high energy Soil Acidity
cost to the plant (Smucker, 1984). Therefore, a reduc- The major factors limiting plant growth on acid soils
tion in DM of endophyte-infected plants in response to are increased concentrations of exchangable H⫹, ex-
Al stress may be related to the increase in exudation changable Al3⫹, and soluble Mn, decreased concentra-
of phenolic-like compounds to alleviate toxic effects
tions of exchangable Ca2⫹, Mg2⫹, K⫹, and reduced solu-
of Al in the rhizosphere. This mechanism should be
bility of P and molybdenum (Mo) (Marschner, 1991).
considered in future research on endophyte-related tol-
Low soil pH and high exchangable Al concentration
erance to Al stress in tall fescue.
restrict root growth, N uptake, and N transport within
grass plants (Thornton, 1998). Research on endophyte
Other Mineral Elements effects on tolerance to acid soils is very limited. Under
Responses of endophyte-infected grasses to mineral simulated acid rain, Cheplick (1993) observed a reduced
stress other than N, P, and Al have received minimal productivity of tall fescue in response to endophyte in-
attention. Calcium is another mineral which may be fection. In contrast, some endophyte-infected tall fescue
affected by endophyte. Calcium, along with N and P, is genotypes (DN2 and DN7) grown in acidic, high ex-
involved in ergot alkaloid biosynthesis as a coenzyme changable Al content soil produced greater root systems
for DMATase (Lee et al., 1976; Cress et al., 1981). than did noninfected plants while other genotypes
Preliminary studies showed that Ca fertilization in- (DN4, DN5, and DN11) did not respond to endophyte
creased ergot alkaloid concentration in tall fescue re- infection (Belesky and Fedders, 1995). Malinowski and
gardless of the soil pH (Hill, 1995). We observed in- Belesky (1999a) observed that the pH of a limed, acidic
creased specific absorption rates for Ca, P, Mg, K, and soil increased faster as a result of root activity of endo-
some microelements in one endophyte-infected tall fes- phyte-infected tall fescue compared with noninfected
plants under P deficient conditions. We observed an rect changes in root morphology and function. These
increase in the pH of a P-deficient (0.31␮g mL⫺1 P) adaptations may arise from a chemical signaling system
nutrient solution from 6.0 to 7.5 within 3 d, regardless of in the symbiotum. Apparently, drought or mineral stress
endophyte status of tall fescue plants (1998, unpublished signals registered by roots can be received by endophyte
data). In contrast, changes in the pH of a P-sufficient and induce a range of responses in the host plants which
(31␮g mL⫺1 P) nutrient solution were dependent on may affect the uptake and transport of water and nutri-
specific endophyte–tall fescue associations. This sug- ents. Less is known about the chemistry of these signals
gests that rhizosphere chemistry may be affected in dif- at this time. Benefits arising from symbioses between
ferent ways depending on endophyte and tall fescue leaf fungal endophytes and grasses, in terms of drought
genome interactions. and mineral stress tolerance, are similar to well-known
benefits of symbioses between mycorrhizal fungi and
Manipulating of the Neotyphodium–Grass grasses. Mycorrhizal fungi can alter water relations of
Association for Beneficial Uses the host grass and enhance drought tolerance (for re-
The responses of Neotyphodium endophyte–grass as- view see Miller, 1987; Smith and Read, 1997) by in-
sociations are often inconsistent and are a function of creased root surface area via mycorrhizal hyphae, and
a particular association, as well as extrinsic factors. This increased water uptake by hyphae (Ruiz-Lozano and
creates a high degree of plasticity in populations of Azcón, 1995). Endophyte-infected grasses increase root
endophyte-infected tall fescue, which enables the popu- surface area by reducing root diameter and producing
lation to persist under a range of growing conditions longer root hairs compared to noninfected grasses (Ma-
and management practices. Variable responses suggest linowski et al., 1999b). The presence of mycorrhizal
that expression of characteristics may be regulated by hyphae in roots increased leaf gas exchange as the result
interactions or products of multiple genes of the endo- of improved water transfer (Hardie, 1985; Ruiz-Lozano
phyte as well as the grass host genomes. This complicates and Azcón, 1995). Endophyte effects on gas exchange
the approach required to obtain the beneficial aspects in grasses are opposite to that of mycorrhizal plants
of the association. Should the endophyte, the grass host (Elbersen and West, 1996). Mycorrhizal grasses can bet-
or the association be manipulated? Hill et al. (1991) ter acquire water compared with non-mycorrhizal
identified a strong contribution of the plant genome grasses as soil water deficit increases; therefore, grass
in controlling the expression of ergopeptine alkaloid growth is less diminished during brief periods of drought
production by the endophyte. This suggests that ergo- (Ebel et al., 1994). In contrast, endophyte-infected
alkaloid production patterns of isolated endophyte grasses survive drought by reducing transpiration losses
strains may be unpredictable once they are introduced compared with noninfected plants. This adaptation may
into tall fescue hosts. Similar results were reported for ensure drought survival but not necessarily better
short- and long-term drought acclimation in tall fescue, growth of endophyte-infected grasses compared to non-
indicating that plant chemistry as well as physiology infected conspecifics. These two strategies differ from
were highly dependent on a particular endophyte–plant each other; however, they both enhance survival of sym-
genome interaction (Hill et al., 1996). The highly plastic biotic plants. Altered hormonal status in grasses, as an
endophyte–host grass association suggests that further effect of fungal infection, may also affect water status
research be conducted at the population level rather regulation (Dannenberg et al., 1992; Joost et al., 1993).
than with specific associations to understand plant popu- Increased nutrient uptake, particularly that of P, by
lation responses (West, 1994). Before this can be symbiotic grasses in response to mineral stress occurs
achieved, it is important to identify mechanisms op- because of chemical modification of the rhizosphere
erating in endophyte–grass associations that might be directly by the mycorrhizal hyphae (for review see Smith
sensitive indicators of change. Investigations should be and Gianinazzi-Pearson, 1988) or indirectly by alter-
conducted with highly responsive endophyte–host grass ation of root chemical activity in endophyte-infected
associations to isolate genes involved in the expression grasses (Malinowski et al., 1998a). Although there are
of beneficial traits. The long-term impact of genetically substantial differences between mycorrhizal grasses and
modified Neotyphodium–tall fescue associations on endophyte-infected grasses, both types of the symbiosis
plant diversity (Clay and Holah, 1999) must be consid- benefit plants grown in mineral deficient soils and under
ered and balanced with the relatively short-term eco- drought, contributing to their survival and reproductive
nomic returns from improved pasture productivity. success compared with nonsymbiotic plants. These two
different symbiotic associations of grasses with fungi
Symbiosis of Cool-Season Grasses with might be antagonistic in tall fescue (Barker, 1987; Chu-
Neotyphodium spp. Fungal Leaf Endophytes Chou et al., 1992; Guo et al., 1992) suggesting alternative
and Environmental Stress Tolerance—An strategies to ensure plant survival under suboptimal en-
Alternative Strategy to VA Mycorrhiza? vironmental conditions.
Endophyte-infected grasses are better adapted than
noninfected grasses to abiotic stresses, i.e., drought and
marginal soil conditions. Results presented in this re-
CONCLUSIONS
view show that Neotyphodium spp. endophytes induce Mutualistic symbiosis of grasses with shoot-localized
direct changes affecting water status in shoots and indi- Neotyphodium spp. endophytes contributes to adapt-
ability and subsequent widespread persistence of the REFERENCES

associations in challenging edaphic and environmental Abernethy, G.A., D.W. Fountain, and M.T. McManus. 1998. Observa-
conditions. Infection with Neotyphodium spp. endo- tions on the leaf anatomy of Festuca novae-zelandiae and biochemi-
phytes induces changes in host grass physiology, espe- cal responses to a water deficit. N.Z. J. Bot. 36:113–123.
cially in root morphology and root function. These Abernethy, G.A., and M.T. McManus. 1998. Biochemical responses
to an imposed water deficit in mature leaf tissue of Festuca arundi-
changes may be a result of intricate signaling and bio- nacea. Environ. Exp. Bot. 40:17-28.
feedback systems involving the symbionts. Compounds Allen, V.G., J.P. Fontenot, C.P. Bagley, R.L. Ivy, and R.R. Evans.
produced as a function of endophyte infection, such as 1997. Effects of seaweed treatment of tall fescue on grazing steers.
pyrrolozidine alkaloids in tall fescue, may function in p. 168–172. In M.J. Williams (ed.) Proc. 1997 Am. Forage Grassl.
both biotic (anti-herbivory, allelopathy) and abiotic Council Conf., Fort Worth, TX. 13-15 Apr. 1997. AFCG, George-
town, TX.
(osmoregulation) stress resistance mechanisms. Endo- An, Z.Q., M.R. Siegel, W. Hollin, H.F. Tsai, D. Schmidt, G. Bunge,
phyte-infection induced root exudates appear to have and C.L. Schardl. 1993. Relationships among non-Acremonium sp.
the same dual stress resistance function in tall fescue. fungal endophytes in five grass species. Appl. Environ. Micro-
These root exudates may contribute to nematode resis- biol. 59:1540–1548.
tance and apparent allelopathic effects on competitors Appel, H. M. 1993. Phenolics in ecological interactions: The impor-
tance of oxidation. J. Chem. Ecol. 19:1521–1552.
in mixed swards (biotic stress) and metal ion chelation Arachevaleta, M., C.W. Bacon, C.S. Hoveland, and D.E. Radcliffe.
affecting sequestration and availability (abiotic stress). 1989. Effect of the tall fescue endophyte on plant responses to
This facet of symbiont response requires further investi- environmental stress. Agron. J. 81:83–90.
gation to realize the full benefit of endophyte–tall fescue Arechavaleta, M., C.W. Bacon, R.D. Plattner, C.S. Hoveland, and
associations surrogately transformed to modify ergo- D.E. Radcliffe. 1992. Accumulation of ergopeptide alkaloids in
symbiotic tall fescue grown under deficits of soil water and nitrogen
alkaloid production. The nature of communication be- fertilizer. Appl. Environ. Microbiol. 58:857–861.
tween endophyte and host grass remains to be de- Arraudeau, M.A. 1989. Breeding strategies for drought resistance. p.
termined. 107–116. In F.W.C. Baker (ed.) Drought resistance in cereals. CAB
Defining the responses of endophyte–grass associa- International, Wallingford, UK.
Azevedo, M.D. 1992. Studies on the fungal endophyte Acremonium
tions to various extrinsic factors is fundamental to un- coenophialum in tall fescue. MS Thesis. Oregon State Univer-
derstanding pasture community structure and ulti- sity, Corvalli.
mately, success of the population. Further careful Azevedo, M.D., and R.E. Welty. 1995. A study of the fungal endophyte
investigation of surrogately transformed endophyte– Acremonium coenophialum in the roots of tall fescue seedlings.
grass associations is necessary if the valuable attributes Mycologia 87:289–297.
Azevedo, M.D., R.E. Welty, A.M. Creaig, and J. Bartlett. 1993. Ergo-
of such associations should be considered for improve- valine distribution, total nitrogen and phosphorus content of two
ment in tolerance of cool-season grasses to environmen- endophyte-infected tall fescue clones. p. 59–62. In D.E. Hume
tal stresses. Close linkage between shoot-root function et al. (ed.) Proc. Second Intl. Symposium on Acremonium/Grass
and evolving knowledge of how endophytes mediate the Interactions, Palmerston North, New Zealand. 4–6 Feb. 1993.
AgResearch, Grassland Research Centre, Palmerston North.
relationship, complicates our extrapolation of individual Bacon, C.W. 1993. Abiotic stress tolerances (moisture, nutrients) and
behavior to community level responses. Modifying en- photosynthesis in endophyte infected tall fescue. Agric. Ecosys.
dophyte–host relationships for a specific factor may Environ. 44:123–141.
have unknown consequences for association persis- Bacon, C.W., and J. De Battista. 1991. Endophytic fungi of grasses.
tence, once multi-faceted extrinsic factors and trophic p. 231–256. In D.K.Arora et al. (ed.) Handbook of applied mycol-
ogy. Vol. 1. Soil and plants. Marcel Dekker, New York.
levels are considered. Bacon, C.W., and N.S. Hill. 1996. Symptomless grass endophytes:
Products of coevolutionary symbioses and their role in the ecologi-
ACKNOWLEDGMENTS cal adaptation of infected grasses. p. 155–178. In S.C. Redlin and
L.M. Carris (ed.) Systematics, ecology end evolution of endophytic
We thank G.A. Alloush (Deptartment of Soil Science fungi of grasses and woody plants. Am. Phytopathol. Soc., St.
and Plant Nutrition, Tishreen University, Lattakia, Paul, MN.
Bacon, C.W., and D.M. Hinton. 1998. Tall fescue: Symbiosis, and
Syria), D.K. Brauer (USDA-ARS, Dale Bumpers Small surrogate transformations for increased drought tolerance. p. 17–
Farms Research Center, Booneville, AR), J. Fedders, 33. In G.E. Brink (ed.) Proc. Southern Pasture and Forage Crop
J. Ruckle, and G. Lambert (USDA-ARS, Appalachian Improvement Conf., 54th, Lafayette, LA. 27–29 April 1998.
Soil and Water Conservation Research Laboratory, Bacon, C.W., P.C. Lyons, J.K. Porter, and J.D. Robbins. 1986. Ergot
toxicity from endophyte- infected grasses: A review. Agron. J. 78:
Beaver, WV) for help with conducting our research 106–116.
program on endophyte involvement in phosphorus Bacon, C.W., J.K. Porter, J.D. Robbins, and E.S. Luttrell. 1977.
economy in tall fescue. We also thank G.C. Lewis Epichloë typhina from toxic tall fescue grasses. Appl. Environ.
(IGER, North Wyke Research Station, Okehampton, Microbiol. 35:576–581.
UK), A. Leuchtmann (Institute of Geobotany, Swiss Bacon, C.W., M.D. Richardson, and J.F. White. 1997. Modification
and uses of endophyte-enhanced turfgrasses—A role for molecular
Federal Institute of Technology, Zurich, CH) , and C.P. technology. Crop Sci. 37:1415–1425.
West (Department of Crop, Soil, and Environmental Ball, D.M. 1997. Significance of endophyte toxicosis and current prac-
Sciences, University of Arkansas, Fayetteville, AR) for tices in dealing with the problem in the United States. p. 395–410.
suggestions and comments on the earlier version of the In C.W. Bacon and N.S. Hill (ed.) Neotyphodium/grass interactions.
manuscript. We appreciate the comments and sugges- Plenum Press, New York.
Barker, D.J., D.E. Hume, and P.E. Quigley. 1997. Negligible physio-
tions made by anonymous reviewers who have contrib- logical responses to water deficit in endophyte-infected and unin-
uted to this and our other publications cited in this fected perennial ryegrass. p. 137–139. In C.W. Bacon and N.S. Hill
review. (ed.) Neotyphodium/grass interactions. Plenum Press, New York.
Barker, D.J., C.Y. Sullivan, and L.E. Moser. 1993. Water deficit effects infection by endophytic fungi and nutrient limitation in the grasses
on osmotic potential, cell wall elasticity and proline in five forage Lolium perenne and Festuca arundinacea. New Phytol. 111:89–97.
grasses. Agron. J. 85:270–275. Christensen, M.J. 1995. Variation in the ability of Acremonium endo-
Barker, G.M. 1987. Mycorrhizal infections influences Acremonium- phytes of perennial rye-grass (Lolium perenne ), tall fescue (Festuca
induced resistance to Argentine stem weevil in ryegrass. p. 199–203. arundinacea ) and meadow fescue (F. pratensis ) to form compatible
In A.J. Popay (ed.) Proc. New Zealand Weed and Pest Contr. associationsin the three grasses. Mycol. Res. 99:466–470.
Conf., 40th, Nelson, N.Z. 11–13 Aug. 1987. Christensen, M.J. 1997. Endophyte compatibility in perennial rye-
Bates, G.E., and R.E. Joost. 1990. The effect of Acremonium coenophi- grass, meadow fescue, and tall fescue: A short review. p. 45–48.
alum on the physiological responses of tall fescue to drought stress. In C.W. Bacon and N.S. Hill (ed.) Neotyphodium/grass interactions.
p. 121–124. In S.S. Quisenberry and R.E. Joost (ed.) Proc. Intl. Plenum Press, New York.
Symp. on Acremonium/Grass Interactions, Baton Rouge, LA. 3 Chu-Chou, M., G. Guo, Z.Q. An, J.W. Henrix, R.S. Ferris, M.R.
Nov. 1990. Louisiana Agric. Exp. Stn., Baton Rouge. Siegel, C.T. Dougherty, and P.B. Burrus. 1992. Suppression of
Belesky, D.P., O.J. Devine, J.E. Pallas, Jr., and W.C. Stringer. 1987a. mycorrhizal fungi in fescue by the Acremonium coenophialum en-
Photosynthetic activity of tall fescue as influenced by a fungal dophyte. Soil Biol. Biochem. 24:633–637.
endophyte. Photosynthetica 21:82–87. Clarke, J.M., and R.C. Durley. 1981. The responses of plants to
Belesky, D.P., and J.M. Fedders. 1995. Tall fescue development in drought stress. p. 89–139. In G.M. Simpson (ed.) Water stress on
response to Acremonium coenophialum and soil acidity. Crop plants. Praeger Publishers, New York.
Sci. 35:529–553. Clay, K. 1987. Effects of fungal endophytes on the seed and seedling
Belesky, D.P., J.D. Robbins, J.A. Stuedemann, S.R. Wilkinson, and biology of Lolium perenne and Festuca arundinacea. Oecologia
O.J. Devine. 1987b. Fungal endophyte infection-loline derivate 73:358–362.
alkaloid concentration of grazed tall fescue. Agron. J. 79:217–220. Clay, K. 1988. Fungal endophytes of grasses: a defensive mutualism
Belesky, D.P., W.C. Stringer, and N.S. Hill. 1989a. Influence of endo- between plants and fungi. Ecology 69:10–16.
phyte and water regime upon tall fescue accessions. I. Growth Clay, K., and J. Holah. 1999. Fungal endophyte symbiosis and plant
characteristics. Ann. Bot. (London) 63:495–503. diversity in successional fields. Science 285:1742–1744.
Belesky, D.P., W.C. Stringer, and R.D. Plattner. 1989b. Influence Creek, R., and G.L. Wade. 1982. Excretion of phenolic compounds
of endophyte and water regime upon tall fescue accessions. II. from the roots of Festuca arundinacea, Eragrostis curvula, and
Pyrrolizidine and ergopeptine alkaloids. Ann. Bot. (London) 64: Lespedeza striata. Trans. Kentucky Acad. Sci. 46:51–55.
343–349. Cress, W.A., L.T. Chayet, and H.C. Rilling. 1981. Crystallization and
Belesky, D.P., J.A. Stuedemann, R.D. Plattner, and S.R. Wilkinson. partial characterization of dimethylallyl pyrophosphate: l-trypto-
1988. Ergopeptine alkaloids in grazed tall fescue. Agron. J. 80: phan dimethylallyl transferase from Claviceps sp. SD58. J.
209–212. Chem. 256:10917–10923.
Belesky, D.P., S.R. Wilkinson, and J.J. Evans. 1984. Amino acid com- Cunningham, P.J., M.J. Blumenthal., M.W. Anderson, K.S. Prakash,
position of fractions of ‘Kentucky-31’ tall fescue as affected by N and A. Leonforte. 1994. Peerennial ryegrass improvement in Aus-
fertilization and mild water stress. Plant Soil 81:257–267. tralia. N.Z. J. Agric. Res. 37:298–310.
Belesky, D.P., S.R. Wilkinson, and J.E. Pallas, Jr. 1982. Response of Dahlman, D.L., M.R. Siegel, and L.P. Bush. 1997. Insecticidal activity
four tall fescue cultivars grown at two nitrogen levels to low soil of N-formylloline. Session 13, p. 5–6. In Proc. XVIII Int. Grasslands
water availability. Crop Sci. 22:93–97. Congr. Winnipeg, Canada. 8–19 June 1997.
Belesky, D.P., S.R. Wilkinson, and J.A. Stuedeman. 1991. The influ- Dannenberg, G., C. Latus, W. Zimmer, B. Hundeshagen, H.J. Schnei-
ence of nitrogen fertilizer and Acremonium coenophialum on the der-Poetsch, and H. Bothe. 1992. Influence of vesicular-arbuscular
soluble carbohydrate content of grazed and nongrazed Festuca mycorrhiza on phytohormone balances in maize (Zea mays L.). J.
arundinacea. Grass Forage Sci. 46:159–166. Plant Physiol. 141:33–39.
Beneš, I., K. Schreiber, H. Ripperger, and A. Kircheiss. 1983. Metal De Battista, J.P., J.H. Bouton, C.W. Bacon, and M.R. Siegel. 1990.
complex formation by nicotianamine, a possible phytosiderophore. Rhizome and herbage production of endophyte removed tall fescue
Experimentia 39:261–262. clones and populations. Agron. J. 82:651–654.
Bouton, J.H., R.N. Gates, D.P. Belesky, and M. Owsley. 1993. Yield Dennis, S.B., V.G. Allen, K.E. Saker, J.P. Fontenot, J.Y.M. Ayad,
and persistence of tall fescue in the Southeastern Coastal plain and C.P. Brown. 1998. Influence of Neotyphodium coenophialum
after removal of its endophyte. Agron. J. 81:220–223. on copper concentration in tall fescue. J. Anim. Sci. 76:2687–2693.
Breen, J.P. 1994. Acremonium endophyte interactions with enhanced Diehl, W.W. 1950. Balansia and the Balansiae in America. U.S.D.A.
plant resistance to insects. Annu. Rev. Entomol. 39:401–423. Monograph 4:1–82.
Briske, D.D. 1996. Strategies of plant survival in grazed systems: A Ebel, R.C., A.J.W. Stodola, X. Duan, and R.M. Augé. 1994. Non-
functional interpretation. p. 37–67. In J. Hodgson and A.W. Illius hydraulic root-to-shoot signalling in mycorrhizal and non-mycor-
(ed.) The ecology and management of grazing systems. CAB Inter- rhizal sorgum exposed to partial soil drying or root severing. New
national, Wallingford, UK. Phytol. 127:495–505.
Briske, D.D., and R.K. Heitschmidt. 1991. An ecological perspective. Eerens, J.P.J., R.J. Lucas, H.S. Easton, and J.G.H. White. 1998. Influ-
p. 11–26. In R.K. Heitschmidt and J.W. Stuth (ed.) Grazing manage- ence of the endophyte (Neotyphodium lolii ) on morphology, physi-
ment. An ecological perspective. Timber Press, Portland, OR. ology, and alkaloid synthesis of perennial ryegrass during high
Buck, G.W., C.P. West, and H.W. Elbersen. 1997. Endophyte effect temperature and water stress. N.Z. J. Agric. Res. 41:219–226.
on drought tolerance in diverse Festuca species. p. 141–143. In Eerens, J.P.J., M.H.P.W. Visker, R.J. Lucas, H.S. Easton, and J.G.H.
C.W. Bacon and N.S. Hill (ed.) Neotyphodium/grass interactions. White. 1997. Influence of the ryegrass endophyte on phyto-nema-
Plenum Press, New York. todes. p. 153–156. In C.W. Bacon and N.S. Hill (ed.) Neotyphodium/
Bush, L.P., F.F. Fannin, M.R. Siegel, D.L. Dahlman, and H.R. Burton. grass interactions. Plenum Press, New York.
1993. Chemistry, occurrence and biological effects of pyrrolizidine Eerens, J.P.J., J.G.H. White, and R.J. Lucas. 1993. The influence of
alkaloids associated with endophyte-grass associations. Agric. Eco- Acremonium endophyte on the leaf extension rate of moisture
sys. Environ. 44:81–102. stressed ryegrass plants. p. 200–204. In D.E. Hume et al. (ed.)
Bush, L.P., H.H. Wilkinson, and C.L. Schardl. 1997. Bioprotective Proc. Second Intl. Symposium on Acremonium/Grass Interactions,
alkaloids of grass-fungal endophyte symbioses. Plant Physiol. Palmerston North, New Zealand. 4–6 Feb. 1993. AgResearch,
114:1–7. Grassland Research Centre, Palmerston North.
Caris, C., W. Hördt, H.-J. Hawkins, V. Römheld, and E. George. Elbersen, H.W., G.W. Buck, C.P. West, and R.E. Joost. 1994. Water
1998. Studies on iron transport by arbuscular mycorrhizal hyphae loss from tall fescue leaves is decreased by endophyte. Arkansas
from soil to peanut and sorghum plants. Mycorrhiza 8:35–39. Farm Res. 43:8–9.
Cheplick, G.P. 1993. Effect of simulated acid rain on the mutualism Elbersen, H.W., and West C.P. 1996. Growth and water relations of
between tall fescue (Festuca arundinacea ) and an endophyte fungus field-grown tall fescue as influenced by drought and endophyte.
(Acremonium coenophialum ). Intl. J. Plant Sci. 154:134–143. Grass Forage Sci. 51:333–342.
Cheplick, G.P., K. Clay, and S. Marks. 1989. Interactions between Elghachtouli, N., M. Paynot, J. Martinatanguy, D. Morandi, and S.
Gianinazzi. 1996. Effect of polyamines and polyamine biosynthesis Hill, N.S., W.C. Stringer, G.E. Rottinghaus, D.P. Belesky, W.A. Par-
inhibitors on spore germination and hyphal growth of Glomus rot, and D.D. Pope. 1990. Growth, morphological and chemical
mossae. Mycol. Res. 100:597–600. component responses of tall fescue to Acremonium coenophialum.
Elmi, A.A., and C.P. West. 1995. Endophyte infection effects on Crop Sci. 30:156–161.
stomatal conductance, osmotic adjustment and drought recovery Hsiao, T.C. 1973. Plant responses to water stress. Annu. Rev. Plant
of tall fescue. New Phytol. 131:61–67. Physiol. 24:519–570.
Farquhar, G.D., J.R. Ehleringer, and K.T. Hubick. 1989. Carbon iso- Huizing, H.J., W. van der Molen, W. Kloek, A.P.M. Den Nijs. 1991.
tope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Detection of loline in endophyte-containing meadow fescue in the
Plant Mol. Biol. 40:503–537. Netherlands and the effect of elevated temperature on induction
Ferguson, N.H., J.S. Rice, and N.G. Allgood. 1993. Variation in nitro- of lolines in endophyte-infected perennial ryegrass. Grass Forage
gen utilization in Acremonium coenophialum isolates. Appl. Envi- Sci. 46:441–445.
ron. Microbiol. 59:3602–3604. Johnson, D.A., and K.H. Asay. 1993. Viewpoint: selection for im-
Fletcher, L.R., and H.S. Easton. 1997. The evaluation of use of endo- proved drought response in cool- season grasses. J. Range Man-
phytes for pasture improvement. p. 209–228. In C.W. Bacon and age. 46:194–202.
N.S. Hill (ed.) Neotyphodium/grass interactions. Plenum Press, Johnson, R.C. 1993. Carbon isotope discrimination, water relations,
New York. and photosynthesis in tall fescue. Crop Sci. 33:169–174.
Fletcher, L.R., and I.C. Harvey. 1981. An association of a Lolium Johnson, R.C., and L.M. Bassett. 1991. Carbon isotope discrimination
endophyte with ryegrass staggers. N.Z. Vet. J. 32:185–186. and water use efficiency in four cool-season grasses. Crop Sci.
Flieger, M., P. Sedmera, J. Novak., L. Cvak, J. Zapletal, and J. Stuchlik. 31:157–162.
1991. Degradation products of ergot alkaloids. J. Nat. Prod. 54: Johnson, R.C., and L.L. Tieszen. 1993. Carbon isotope discrimination,
390–395. water relations, and gas exchange in temperate grass species and
Foehse, D., and A. Jungk. 1983. Influence of phosphate and nitrate accessions. p. 281–296. In J.R. Ehleringer et al. (ed.) Stable isotopes
supply on root hair formation of rape, spinach and tomato plants and plant carbon-water relations. Academic Press, Inc., San
(Brassica oleracea, Spinacia oleracea, Lycopersicon esculentum ). Diego, CA.
Plant Soil 74:359-368. Joost, R.E., R.E. Sharp, and T.L. Holder. 1993. Involvement of the
Foy, C.D., and J.J. Murray. 1998. Developing aluminum-tolerant Acremonium-endophyte in ABA-mediated gas exchange responses
strains of tall fescue for acid soils. J. Plant Nutr. 21:1301–1325. in tall fescue. Tall Fescue Toxicosis Workshop, Atlanta, GA. South-
Funk, C.R., and J.F White, Jr. 1997. Use of natural and transformed ern Extension and Research Activity Information Exchange
endophytes for turf improvement. p. 229–239. In C.W. Bacon and Group 8:41–42.
N.S. Hill (ed.) Neotyphodium/grass interactions. Plenum Press, Joyce, P.A., D. Aspinall, and L.G. Paleg. 1992. Photosynthesis and
New York. the accumulation of proline in response to water deficit. Aust. J.
Garner, G.B., G.E. Rottinghaus, C.N. Cornell, and H. Testereci. 1993. Plant Physiol. 19:249–261.
Chemistry of compounds associated with endophyte/grass interac- Ju, Y., J.N. Sacalis, and C.C. Still. 1998. Bioactive flavonoids from
tion: ergovaline- and ergopeptine-related alkaloids. Agric. Ecosyst. endophyte-infected blue grass (Poa ampla ). J. Agric. Food
Environ. 44:65–80. Chem. 46:3785–3788.
Garthwaite, I. 1997. Cellular and molecular techniques for characteriz- Justus, M., L. Witte, and T. Hartmann. 1997. Levels and tissue distribu-
ing Neotyphodium/grass interactions. p. 361–376. In C.W. Bacon tion of loline alkaloids in endophyte-infected Festuca pratensis.
and N.S. Hill (ed.) Neotyphodium/grass interactions. Plenum Press, Phytochemistry 44:51–57.
New York. Kafkafi, U., B. Bar-Yosef, R. Rosenberg, and G. Sposito. 1988. Phos-
Gentry, C.E., R.A. Chapman, L. Henson, and R.C. Buckner. 1969. phorus adsorption by kaoloinite and montmorillonite: II. Organic
Factors affecting the alkaloid content of tall fescue. Agron. J. anion competition. J. Am. Soc. Soil Sci. 52:1585–1589.
61:313–316. Kennedy, C.W., and L.P. Bush. 1983. Effect of environmental and
Gleason, M.L., N.E. Christians, and M. Agnew. 1990. Effect of endo- management factors on the accumulation of N-acetyl and N-formyl
phyte infection of perennial ryegrass on growth under drought loline alkaloids in tall fescue. Crop Sci. 23:547–552.
stress. Phytopathology 80:1031. Koga, H., M.J. Christensen, and R.J. Bennett. 1993. Incompatibility
Glenn, A.E., and C.W. Bacon. 1997. Distribution of ergot alkaloids of some grass/Acremonium endophyte associations. Mycol. Res.
within the family Clavicipitaceae. p. 53–56. In C.W. Bacon and 97:1237–1244.
N.S. Hill (ed.) Neotyphodium/grass interactions. Plenum Press, Koshino, H., S. Terada, T. Yoshihara, S. Sakamura, T. Shimanuki, T.
New York. Sato, and A. Tajimi. 1988. Three phenolic acid derivates from
Glenn, A.E., C.W. Bacon, R. Price, and R.T. Hanlin. 1996. Molecular stromata of Epichloë typhina on Phleum pratense. Phytochemis-
phylogeny of Acremonium and its taxonomic implications. Myco- try 27:1333–1338.
logia 88:369–383. Koshino, H., T. Yoshihara, S. Sakamura, T. Shimanuki, T. Sato, and
Graser, G., and T. Hartmann. 1997. Biosynthetic incorporation of A. Tajimi. 1989. A ring B aromatic sterol from stromata of Epichloë
the aminobuthyl group of spermidine into pyrrolizidine alkaloids. typhina. Phytochemistry 28:771–772.
Phytochemisry 45:1591–1595. Kulkarni, R.K., and D. Nielsen. 1986. Nutritional requirements for
Guo, B.Z., J.W. Hendrix, Z.-Q. An, and R.S. Ferris. 1992. Role of growth of a fungus endophyte of tall fescue grass. Mycologia 78:
Acremonium endophyte of fescue on inhibition of colonization and 781–786.
reproduction of mycorrhizal fungi. Mycologia 84:882–885. Lapeyrie, F.F., G.A. Chilvers, and P.A. Douglass. 1984. Formation
Hardie, K. 1985. The effect of removal of extraradical hyphae on of metachromatic granules following phosphate uptake by mycelial
water uptake by vesicular-arbuscular mycorrhizal plants. New Phy- hyphae of an ectomycorrhizal fungus. New Phytol. 98:345–360.
tol. 101:677–684. Latch, G.C.M. 1993. Physiological interactions of endophytic fungi
Hill, N.S. 1995. Progress report - The University of Georgia. p. 14–16. and their hosts. Biotic stress tolerance imparted to grasses by endo-
In F.T. Withers (ed.) Proc. Tall Fescue Workshop. The Southern phytes. Agric. Ecosyst. Environ. 44:143–156.
Extension and Research Activity Information Exchange Group 8, Latch, G.C.M, M.J. Christensen, and G.J. Samuels. 1984. Five endo-
Mississippi Agric. Forestry Exp. Stn., Mississippi State. phytes of Lolium and Festuca in New Zealand. Mycotaxon, 20:
Hill, N.S., D.P. Belesky, and W.C. Stringer. 1998. Encroachment of 535–550.
endophyte-infected on endophyte-free tall fescue. Ann. Bot. (Lon- Latch, G.C.M., W.F. Hunt, and D.R. Musgrave. 1985. Endophytic
don) 81:483–488. fungi affect growth of perennial ryegrass. N.Z. J. Agric. Res.
Hill, N.S., J.G. Pachon, and C.W. Bacon. 1996. Acremonium coenophi- 28:165–168.
alum-mediated short- and long-term drought acclimation in tall Lee, S.L., H.G. Floss, and P. Heinstein. 1976. Purification and proper-
fescue. Crop Sci. 36:665–672. ties of dimethylallyl-pyrophosphate: Tryptophan dimethylallyl
Hill, N.S., W.A. Parrott, and D.D. Pope. 1991. Ergopeptine alkaloid tryptophan transferase, the first enzyme of ergot alkaloid biosyn-
production by endophytes in a common tall fescue genotype. Crop thesis in Claviceps sp. SD 58. Arch. Biochem. Biophysiol. 177:
Sci. 31:1545–1547. 84–94.
Leuchtmann, A. 1992. Systematics, distribution, and host specificity infection by an Acremonium-like endophytic fungus. J. Agric. Food
of grass endophytes. Natural Toxins 1:150–162. Chem. 44:1285–1290.
Leuchtmann, A. 1994. Isozyme characterization, persistence, and com- Miller, R.M. 1987. The ecology of vesicular-arbuscular mycorrhizae
patibility of fungi and grass mutualists. p. 21–29. In C.W. Bacon in grass- and shrublands. p. 135–170. In G.R. Safir (ed.) Ecophysiol-
and J.F. White, Jr. (ed.) Biotechnology of endophytic fungi of ogy of VA mycorrhizal plants. CRC Press, Boca Raton, FL.
grasses. CRC Press, Boca Raton, FL. Mino, Y., T. Ishida, N. Ota, M. Inoue, K. Nomoto, T. Takemoto, H.
Lewis, G.C., A.K. Bakken, J.H. Macduff, and N. Raistrick. 1996. Tanaka, and Y. Sugiura. 1983. Migineic acid-iron (III) complex
Effect of infection by the endophytic fungus Acremonium lolii on and its structurally analogous cobalt (III) complexes: Characteriza-
growth and nitrogen uptake by perennial ryegrass (Lolium per- tion and implication for absorption and transport of iron in gramin-
enne ) in flowing solution culture. Ann. Appl. Biol. 129:451–460. eous plants. J. Am. Chem. Soc. 105:4671–4676.
Liu, H., J.R. Heckman, and J.A. Murphy. 1996. Screening fine fescues Morgan-Jones, G., and W. Gams. 1982. Notes on Hyphomycetes.
for aluminum tolerance. J. Plant Nutr. 19:677–688. XLI. An endophyte of Festuca arundinacea and the anamorph of
Louis, M. St., and S.H. Faeth. 1997. The effect of endophytic fungi Epichloë typhina, new taxa in one of two new sections of Acremo-
on the fitness of Arizona fescue (Festuca arizonica ) under varying nium. Mycotaxon 15:311–318.
nitrogen levels. The Fourth Annual Undergraduate Research Morgan-Jones, G., J.F. White, and E.L. Piontelli. 1990. Endophyte-
Poster Symposium, Arizona State University, Abstract 18. host associations in forage grasses. XIII. Acremonium chilense, an
Lyons, P.C., and C.W. Bacon. 1984. Ergot alkaloids in tall fescue undescribed endophyte occurring in Dactylis glomerata in Chile.
infected with Sphacelia typhina. Phytopathology 75:501. Mycotaxon 39:441–454.
Lyons, P.C., J.J. Evans, and C.W. Bacon. 1990. Effects of the fungal Naffaa, W., C. Ravel, and J.J. Guillaumin. 1998a. A new group of
endophyte Acremonium coenophialum on nitrogen accumulation endophytes in European grasses. Ann. appl. Biol. 132:211–226.
and metabolism in tall fescue. Plant Physiol. 92:726–732. Naffaa, W., C. Ravel, and J.J. Guillaumin. 1998b. Nutritional require-
Malinowski, D. 1995. Rhizomatous ecotypes and symbiosis with endo- ments for growth of fungal endophytes of grasses. Can. J. Micro-
phytes as new possibilities of improvement in competitive ability biol. 44:231–237.
of meadow fescue (Festuca pratensis Huds.). Ph.D. Thesis. Diss Penn, J., I. Garthwaite, M.J. Christensen, C.M. Johnson, and N.R.
ETH No. 11397. Swiss Fed. Inst. Technology, Zurich. Towers. 1993. The importance of screening for potentially trem-
Malinowski, D., A. Leuchtmann, D. Schmidt, and J. Nösberger. 1997a. orgenic Acremonium isolates. p. 88–92. In D.E. Hume et al. (ed.)
Growth and water status in meadow fescue is affected by Neotypho- Proc. Second Intl. Symposium on Acremonium/Grass Interactions,
dium and Phialophora species endophytes. Agron. J. 89:673–678. Palmerston North, New Zealand. 4–6 Feb. 1993. AgResearch,
Malinowski, D., A. Leuchtmann, D. Schmidt, and J. Nösberger. 1997b. Grassland Research Centre, Palmerston North.
Symbiosis with Neotyphodium uncinatum endophyte may increase Percival, N.S., and F.R. Duder. 1983. A comparison of perennial
the competitive ability of meadow fescue. Agron. J. 89:833–839. grasses under sheep grazing on the Central Plateau. Proc. N.Z.
Malinowski, D.P., G.A. Alloush, and D.P. Belesky. 1998a. Evidence Grassl. Assoc. 44:81–90.
for chemical changes on the root surface of tall fescue in response to Petroski, R.J., D.L. Dornbos, Jr., and R.G. Powell. 1990. Germination
infection with the fungal endophyte Neotyphodium coenophialum. and growth inhibition of annual ryegrass (Lolium multiflorum )
Plant Soil 205:1–12. and alfalfa (Medicago sativa ) by loline alkaloids and synthetic N-
Malinowski, D.P., and D.P. Belesky. 1999a. Endophyte infection en- acetylloline derivates. J. Agric. Food Chem. 38:1716–1718.
hances the ability of tall fescue to utilize sparingly available phos- Petroski, R.J., R.G. Powell, and K. Clay. 1992. Alkaloids of Stipa
phorus. J. Plant Nutr. 22:835–853. robusta (Sleepygrass) infected with an Acremonium endophyte.
Malinowski, D.P., and D.P. Belesky. 1999b. Infection with leaf fungal Natural Toxins 1:84–88.
endophyte Neotyphodium coenophialum increases aluminum se- Philipson, M.N. 1991. Ultrastructure of the Gliocladium-like endo-
questration on root surfaces of tall fescue. J. Plant Nutr. 22: phyte of perennial ryegrass (Lolium perenne L.). New Phytol.
1335–1349. 117:271–280.
Malinowski, D.P., D.P. Belesky, and J.M. Fedders. 1999a. Endophyte Porter, J.K. 1994. Chemical constituents of grass endophytes. p. 103–
infection may affect the competitive ability of tall fescue grown 23. In C.W. Bacon and J.F. White, Jr. (ed.) Biotechnology of endo-
with red clover. J. Agron. Crop Sci. 183:91–102. phytic fungi of grasses. CRC Press, Boca Raton, FL.
Malinowski, D.P., D.K. Brauer, and D.P. Belesky. 1999b. Neotypho- Powell, R.G., M.R. Te Paske, R.D. Plattner, J.F. White, and S.L.
dium coenophialum-endophyte affects root morphology of tall fes- Clement S.L. 1994. Isolation of resveratrol from Festuca versuta
cue grown under phosphorus deficiency. J Agron. Crop Sci. 183: and evidence for the widespread occurence of this stilbene in the
53–60. Poaceae. Phytochemistry 35:335–338.
Malinowski, D.P., D.P. Belesky, N.S. Hill, V.C Baligar, and J.M. Ravel, C., C. Courty, A. Coudret, and G. Charmet. 1997. Beneficial
Fedders. 1998b. Influence of phosphorus on the growth and ergot effects of Neotyphodium lolii on the growth and the water status in
alkaloid content of Neotyphodium coenophialum-infected tall fes- perennial ryegrass cultivated under nitrogen deficiency or drought
cue (Festuca arundinacea Schreb.). Plant Soil 198:53–61. stress. Agronomie 17:173–181.
Marks, S., and K. Clay. 1996. Physiological responses of Festuca arun- Read, J.J., D.A. Johnson, K.H. Asay, and L.L. Tieszen. 1991. Carbon
dinacea to fungal endophyte infection. New Phytol. 133:727–733. isotope discrimination, gas exchange, and water use efficiency in
Marks, S., K. Clay, and G.P. Cheplick. 1991. Effects of fungal endo- creasted wheatgrass clones. Crop Sci. 31:1203–1208.
phytes on interspecific and intraspecific competition in the grasses Richardson, M.D., C.W. Bacon, and C.S. Hoveland. 1990. The effect
Festuca arundinacea and Lolium perenne. J. Appl. Ecol. 28:194–204. of endophyte removal on gas exchange in tall fescue. p. 189–193.
Marschner, H. 1986. Mineral nutrition in higher plants. Academic In S.S. Quisenberry and R.E. Joost (ed.) Proc. Intl. Symp. on
Press Inc., Orlando, FL Acremonium/Grass Interactions. Baton Rouge, LA. 3 Nov. 1990.
Marschner, H. 1991. Mechanisms of adaptation of plants to acid soils. Louisiana Agric. Exp. Stn., Baton Rouge.
p. 683–702. In R.J. Wright et al. (ed.) Plant-Soil Interactions at Richardson, M.D., G.W. Chapman, Jr., C.S. Hoveland, and C.W.
Low pH: Proc. Second Intl. Symp. on Plant-Soil Interactions at Low Bacon. 1992. Sugar alkohols in endophyte-infected tall fescue. Crop
pH, Beckley, WV. 24–29 June 1991. Kluwer Academic Publisher. Sci. 32:1060–1061.
Dordrecht, the Netherlands. Robbers, J.E. 1984. The fermentative production of ergot alkaloids.
Miles, C.O., M.E. Dimenna, S.W.L. Jacobs, I. Garthwaite, G.A. Lane, p. 197. In A. Mizrahi and A.L. van Wezel (ed.) Advances in biotech-
R.A. Prestidge, S.L. Marschall, H.H. Wilkinson, C.L. Schardl, nological processes, Vol. 3. A.R. Liss, New York.
O.J.P. Ball, and G.C.M. Latch. 1998. Endophytic fungi in indige- Robbins, J.D., S.R. Wilkinson, and D. Burdick. 1973. Loline alkaloids
nous Australasian grasses associated with toxicity to livestock. of tall fescue seed and forage. p. 98–107. In Proc. Fescue Toxicity
Appl. Environ. Microbiol. 64:601–606. Conf., Lexington, KY. 31 May – 1 June 1973. University of Ken-
Miles, C.O., G.A. Lane, M.E. di Menna, I. Garthwaite, E.L. Piper, tucky, Lexington.
O. J-P. Ball, G.C.M. Latch, J.M. Allen, M.B. Hunt, L.P. Bush, F.K. Roberts, C.A., S.M. Marek, T.L. Niblack, and A.L. Karr. 1992. Para-
Min, I. Fletcher, and P.S. Harris. 1996. High levels of ergonovine sitic Meloidogyne and mutualistic Acremonium increase chitinase
and lysergic acid amide in toxic Achnatherum inebrians accompany in tall fescue. J. Chem. Ecol. 18:1107–1116.
Ruiz-Lozano, J.M., and R. Azcón. 1995. Hyphal contribution to water Taylor, G.J. 1988. The physiology of aluminum tolerance in higher
uptake in mycorrhizal plants as affected by the fungal species and plants. Commun. Soil Sci. Plant Anal. 19:1179–1194.
water status. Physiologia Plantarum 95:472–478. Thomas, H. 1991. Accumulation and consumption of solutes in swards
Saker, K.E., V.G. Allen, J. Kalnitsky, C.D. Thatcher, W.S. Swecker, of Lolium perenne during drought and after rewatering. New Phy-
Jr., and J.P. Fontenot. 1998. Monocyte immune cell response and tol. 118:35–48.
copper status in beef steers that grazed endophyte- infected tall Thornton, B. 1998. Influence of pH and aluminum on nitrogen parti-
fescue. J. Anim. Sci. 76:2694–2700. tioning in defoliated grasses. Grass Forage Sci. 53:170–178.
Schmidt, D. 1991. Les endophytes de la fétuque des prés. Rev. Suisse Tieszen, L., and D. Grant. 1990. Carbon isotope discrimination among
Agric. 23:369–375. selected Pioneer Hi-Bred and public inbreds and hybrids. Maize
Schmidt, D. 1993. Effects of Acremonium uncinatum and a Phialo- Genet. Coop. Newsl. 64:70.
phora-like endophyte on vigour, insect and disease resistance of Trenbath, B.R. 1974. Biomass productivity of mixtures. Adv.
meadow fescue. p. 185–187. In D.E. Hume et al. (ed.) Proc. Second Agron. 26:177–210.
Intl. Symposium on Acremonium/Grass Interactions, Palmerston Turner, N.C. 1986. Adaptation to water deficits: a changing perspec-
North, New Zealand. 4–6 Feb. 1993. AgResearch, Grassland Re- tive. Aust. J. Plant Physiol. 13:175–190.
search Centre, Palmerston North. Walters, D.R., and C.A. Mackintosh. 1997. Control of plant disease
Schulthess, F.M., and S.H. Faeth. 1998. Distribution, abundances, and by perturbation of fungal polyamine metabolism. Physiologia Plan-
associations of the endophytic fungal community of Arizona fescue tarum 100:689–695.
(Festuca arizonica ). Mycologia 90:569–578. West, C.P. 1994. Physiology and drought tolerance of endophyte-
Schulz, B., A.K. Rommert, U. Dammann, H.J. Aust, and D. Strack. infected grasses. p. 87–99. In C.W. Bacon and J.F. White, Jr. (ed.)
1999. The endophyte-host interaction: A balanced antagonism? Biotechnology of endophytic fungi of grasses. CRC Press, Boca
Mycol. Res. 103:1275–1283. Raton, FL.
Siegel, M.R. 1993. Acremonium endophytes: our current state of West, C.P., H.W. Elbersen, A.A. Elmi, and G.W. Buck. 1994. Acremo-
knowledge and future directions for research. Agric. Ecosyst. Envi- nium effects on tall fescue growth: parasite or stimulant? p. 102–111.
ron. 44:301–321. In G.E. Brink (ed.) Proc. Southern Pasture Forage Crop Improve-
Siegel, M.R., D.L. Dahlman, and L.P. Bush. 1989. The role of endo- ment Conf. Knoxville, TN., 50th. 23–25 May 1994.
phytic fungi in grasses: New approaches to biological control of West, C.P., E. Izekor, D.M. Oosterhuis, and R.T. Robbins. 1988. The
pests. p. 169–186. In A.L. Leslie and R.L. Metcalf (ed.) Pesticide effect of Acremonium coenophialum on the growth and nematode
problems and IPM solutions for urban turfgrass and ornamentals. infestation of tall fescue. Plant Soil 112:3–6.
Environm. Protection Agency, Washington, DC. West, C.P., E. Izekor, R.T. Robbins, R. Gergerich, and T. Mahmood.
Siegel, M.R., G.C.M. Latch, L.P. Bush, F.F. Fannin, D.D. Rowan, B.A. 1990. Acremonium coenophialum effects on infestations of Barley
Tapper, C.W. Bacon, and M.C. Johnson. 1990. Fungal endophyte- Yellow Dwarf Virus and soil-borne nematodes and insects in tall
infected grasses: Alkaloid accumulation and aphid response. J. fescue. p. 196–198. In S.S. Quisenberry and R.E. Joost (ed.) Proc.
Chem. Ecol. 16:3301–3315. Intl. Symp. on Acremonium/Grass Interactions. Baton Rouge, LA.
Siegel, M.R., C.L. Schardl, and T.D. Phillips. 1995. Incidence and 3 Nov. 1990. Louisiana Agric. Exp. Stn., Baton Rouge.
compatibility of nonclavicipitaceous fungal endophytes in Festuca White, J.A., and M.R. Brown. 1979. Ultrastructure and x-ray analysis
and Lolium grass species. Mycologia 87:196–202. of phosphorus granules in a vesicular-arbuscular mycorrhizal fun-
Siemann, E.H., and L.L. Creasy. 1992. Concentration of the phyto- gus. Can. J. Bot. 57:2812–2818.
alexin resveratrol in wine. Am. J. Enol. Vitic. 43:49–52. White, J.F., Jr. 1994. Taxonomic relationships among the members
Smith, S.E., and V. Gianinazzi-Pearson. 1988. Physiological interac- of the Balansiae (Clavicipitales). p. 3–20. In C.W. Bacon and J.F.
tions between symbionts in vesicular-arbuscular mycorrhizal plants. White, Jr. (ed.) Biotechnology of endophytic fungi of grasses. CRC
Ann. Rev. Plant Physiol. Plant Mol. Biol. 39:221–244. Press, Boca Raton, FL.
Smith, S.E., and D.J. Read. 1997. Mycorrhizal symbiosis. Second edi- White, J.F., Jr., and P.V. Reddy. 1998. Examination of structure and
molecular phylogenetic relationships of some graminicolous symbi-
tion. Academic Press, San Diego, CA.
onts in genera Epichloë and Parepichloë. Mycologia 90:226–234.
Smucker, A.J.M. 1984. Carbon utilization and losses by plant root
White, R.H., M.C. Engelke, S.J. Morton, J.M. Johnson-Cicalese, and
systems. p. 27–63. In S.A. Barber and D.R Bouldin (ed.) Roots,
B.A. Ruemmele. 1992. Acremonium endophyte effects on tall fes-
nutrients and water influx, and plant growth. SSSA, Madison, WI.
cue drought tolerance. Crop Sci. 32:1392–1396.
Snaydon, R.W., and E.H. Sattore. 1989. Bivariate diagrams for plant Wilkinson, H.H., L.P. Bush, H.R. Burton, M.R. Siegel, and C. Schardl.
competition data: Modification and interpretation. J. Appl. Ecol. 1997. Lolines are fungal metabolites. Poster Abstract 27. In Poster
26:1043–1057. Abstracts of the Int. Neotyphodium/Grass Interactions Symp. Ath-
Springer, W.C. 1997. Allelopathic effects of tall fescue. p. 25–33. In ens, GA. 8-31 May 1997.
G.E. Brink (ed.) Proc. Southern Forage Crop Improvement Conf., Wilkinson, H.H., and C.L. Schardl. 1997. The evolution of mutualism
53rd, Fort Worth, TX. 12–13 Apr. 1997. in grass-endophyte associations. p. 13–25. In C.W. Bacon and N.S.
Stoll, A., and A. Hoffmann. 1965. The ergot alkaloids. In R.H.F. Hill (ed.) Neotyphodium/grass interactions. Plenum Press, New
Manske (ed.) The alkaloids: Chemistry and physiology. Academic York.
Press, New York. Wright, R.J., V.C. Baligar, and S.F. Wright. 1987. The influence of
Strickland, J.R., E.M. Bailey, L.K. Abney, and J.W. Oliver. 1996. acid soil factors on the growth of snapbeans in major Appalachian
Assessment of the mitogenic potential of the alkaloids produced soils. Commun. Soil Sci. Plant Anal. 18:1235–1252.
by endophyte (Acremonium coenophialum )-infected tall fescue Yates, S.G. 1962. Toxicity of tall fescue forages. A review. Econ.
(Festuca arundinacea ) on bovine vascular smooth muscle in vitro. Bot. 16:295–303.
J. Anim. Sci. 74:1664–1671. Yates, S.G. 1963. Paper chromatography of alkaloids of tall fescue
Sutherland, B.L., and J.H. Hoglund. 1989. Effect of ryegrass con- hay. J. Chromatography 12:423–426.
taining the endophyte (Acremonium lolii ) on the performance of Yoshihara, T., S. Togiya, H. Koshino, S. Sakamura, T. Shimanuki, T.
associated white clover and subsequent crops. Proc. N.Z. Grassl. Sato, and A. Tajimi. 1985. Three fungitoxic sesquiterpenes from
Assoc. 50:265–269. stromata of Epichloë typhina. Tetra. Lett. 26:5551–5554.
Takagi, S. 1976. Naturally occurring iron-chelating compounds in oat Zabalgogeazcoa, I., E.P. Benito, A.G. Ciudad, B.G. Criado, and A.P.
and rice-root washings. 1. Activity, measurement and preliminary Eslava. 1998. Double-stranded RNA and virus-like particles in the
characterization. Soil Sci. Plant Nutr. 22:423–433. grass endophyte Epichloë festucae. Mycol. Res. 102:914–918.

Malinoswki (Drought Tolerance by Endophyte)

Uploaded by

Copyright:

Available Formats

Malinoswki (Drought Tolerance by Endophyte)

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Malinoswki (Drought Tolerance by Endophyte)

Uploaded by

Copyright:

Available Formats

CROP SCIENCE

Volume 40 July–August 2000 Number 4

REVIEW & INTERPRETATION

I n their evolution, grasses have developed symbiotic

phyte-infected grasses. Responses of grass root system

kg ha⫺1) or high (336 kg ha⫺1) N availability. The authors

Fig. 6. Fe3⫹ reducing activity of exudates from intact roots of tall

as phenolic-like compounds) with a higher iron (Fe3⫹)

cue genotype (DN2) but the responses were not consis-

ability and subsequent widespread persistence of the REFERENCES

You might also like

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.