© 2002 by The Society for Integrative and Comparative Biology
Fungal Endophytes: Common Host Plant Symbionts but Uncommon Mutualists1
1 Department of Biology, P.O. Box 871501, Arizona State University, Tempe, Arizona 85287-1501
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Fungal endophytes are extremely common and highly diverse microorganisms that live within plant tissues, but usually remain asymptomatic. Endophytes traditionally have been considered plant mutualists, mainly by reducing herbivory via production of mycotoxins, such as alkaloids. However, the vast majority of endophytes, especially horizontally-transmitted ones commonly found in woody plants, apparently have little or no effect on herbivores. For the systemic, vertically-transmitted endophytes of grasses, mutualistic interactions via increased resistance to herbivores and pathogens are more common, as predicted by evolutionary theory. However, even in these obligate symbioses, endophytes are often neutral or even pathogenic to the host grass, depending on endophyte and plant genotype and environmental conditions.
We present a graphical model based upon variation in nitrogen flux in the host plant. Nitrogen is a common currency in endophyte/host and plant/herbivore interactions in terms of limitations to host plant growth, enhanced uptake by endophytes, demand for synthesis of nitrogen-rich alkaloids, and herbivore preference and performance. Our graphical model predicts that low alkaloid-producing endophytes should persist in populations when soil nutrients and herbivory are low. Alternatively, high alkaloid endophytes are favored under increasing herbivory and increasing soil nitrogen, at least to some point. At very high soil nitrogen levels, uninfected plants may be favored over either type of infected plants. These predictions are supported by patterns of infection and alkaloid production in nature, as well by a manipulative field experiment. However, plant genotype and other environmental factors, such as available water, interact with the presence of the endophyte to influence host plant performance.
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INTRODUCTION |
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".... steer clear of permanent alliance with any portion of the foreign world"—George Washington—Farewell Address to the People of the United States, 17 September 1796.
Endophytic fungi are an important, yet relatively unstudied group of microbial plant symbionts. Endophytic fungi live asymptomatically, and sometimes systemically, within plant tissues (Carroll, 1988
, 1991). Endophytes usually inhabit above-ground plant tissues (leaves, stems, bark, petioles and reproductive structures), which distinguishes them from better known mycorrhizal symbionts. The distinction is not firm, because endophytes may also inhabit root tissues. Overall, endophytic fungi are ubiquitous and extremely diverse in host plants. Every plant examined to date harbors at least one species of endophytic fungus and many plants, especially woody plants, may contain literally hundreds or thousands of species (Petrini, 1986; Petrini et al., 1992; Gaylord et al., 1996; Faeth and Hammon, 1997; Saikkonen et al., 1998; Arnold et al., 2000).
Like mycorrhizae, endophytic fungi are thought to interact mutualistically with their host plants mainly by increasing host resistance to herbivores (Carroll, 1988, 1991; Clay, 1988, 1990) and have been termed "acquired plant defenses" (Cheplick and Clay, 1988). Indeed, some agronomic grass species infected with systemic endophytes show striking toxic and noxious effects on vertebrate and invertebrate herbivores (Clay, 1988, 1990, 1992; Siegel and Latch, 1987; Breen, 1994) and pathogens (e.g., Gwinn and Gavin, 1992) by virtue of alkaloids such as pyrrolizidine alkaloids, ergot alkaloids and peramine produced by the fungi (Powell and Petroski, 1992; Siegel and Bush, 1996; Leuchtmann et al., 2000). Endophytes, at least systemic ones in agronomic grasses, may also increase host grass competitive abilities, by increasing germination success, resistance to drought and water stress and resistance to seed predators (Clay, 1988; Wolock-Madej and Clay, 1991; Knoch et al., 1993). In return, plants provide spatial structure and protection from desiccation, nutrients and photosynthate and, in the case of vertical-transmission, dissemination to the next generation of hosts.
However, more recent arguments and evidence suggest that interactions between host plants and endophytes are not fixed in either ecological or evolutionary time, or geographically (e.g., Saikkonen et al., 1998; Faeth and Bultman, 2002) and range from mutualistic to antagonistic. This view is in keeping with more recent and general concepts of species interactions, and mutualisms in particular (Law, 1985; Lewis, 1985; Carroll, 1992; Connor, 1995; Thompson, 1982, 1994, 1999; Thompson and Pellmyr, 1992; Pellmyr et al., 1996; Saikkonen et al., 1998; Morris, 1996; Stanton et al., 1999; Hochberg et al., 2000). For example, many plant-mycorrhizal interactions, the below-ground counterparts of endophytes, are now recognized as ranging from mutualistic to antagonistic, depending on phylogeny, genetic strains, other interacting species, geography and abiotic conditions (Parker, 1995, 1999; Johnson, 1993; Johnson et al., 1997; Gehring and Whitham, 1994; Gehring et al., 1997).
While systemic endophytes in agronomic grasses have been well-studied, the interactions between host plants and endophytes in natural populations and communities are poorly understood. The emerging picture from the limited studies of horizontally (spore) transmitted endophytes in plants suggests they: 1) are very abundant and common as localized infections in all types of plants, ranging from algae to angiosperms, 2) are extremely diverse, particularly in the more structurally complex and longer-lived woody plants, 3) have the same attributes of other macro-communities, including seasonality, successional changes, dominant and rare species, and generalist and specialist species (e.g., Hammon and Faeth, 1992; Faeth and Hammon, 1997; Schulthess and Faeth, 1998), and 4) do not appear to generally increase host plant resistance to herbivores (Faeth and Wilson, 1996; Saikkonen et al., 1998), as originally hypothesized (e.g., Carroll, 1988). Instead, many of these horizontally transmitted endophytes do not affect, or may even decrease, resistance to host plant herbivores (Faeth and Bultman, 2002). Herbivore damage to host plants may facilitate colonization of the spores and hyphae by breaching leaf surfaces (e.g., Faeth and Hammon, 1997) and spores and hyphae may be dispersed via passage through the gut of herbivores (Craven, Wilson and Faeth, unpublished data). One thus does not expect that these endophytes should deter or decrease survival of herbivores.
Alternatively, systemic grass endophytes, at least in some introduced agronomic grasses, as well as a few native grasses (e.g., Faeth and Bultman, 2002) may have profound effects on herbivores. Epichloë; and Neotyphodium endophytes in these introduced grasses cause toxicosis to grazing livestock (e.g., Clay, 1990, 1991, 1992; Hoveland, 1993), and increase resistance to invertebrate herbivores and pathogenic microorganisms (Carroll, 1988; Clay, 1988, 1990; Clay et al., 1993; Dahlman et al., 1991; Kimmons et al., 1990; West et al., 1993; Breen, 1994) and their natural enemies (e.g., Bultman et al., 1997; Ormacini et al., 2000) and may inhibit germination and growth of other grasses via allelopathy by endophyte alkaloids (e.g., Peters and Zam, 1981; Petroski et al., 1990). Neotyphodium-linked alkaloids (ergot and indole diterpene-type alkaloids) produce "staggers" (a neurological disorder) in sheep and cattle, while in tall fescue, pyrrolizidine and ergot-type alkaloids cause gangrene of extremities, reduced conception, and generally poor health in livestock (see Siegel and Bush, 1996; Schardl and Phillips, 1997). Resistance to insect pests in infected tall fescue and perennial ryegrass is mainly the result of peramine and pyrrolizidine alkaloids in tall fescue and ryegrass (Breen, 1994; Siegel and Bush, 1996). While endophytes may confer other benefits to their hosts, such as increased drought resistance (e.g., Richardson et al., 1992, 1993; West et al., 1993; Archavaleta et al., 1992; Bacon, 1993), alkaloids produced by symbiotic endophytes mediated many known benefits (Siegel and Bush, 1996).
However, the beneficial effects of endophytes, especially those related to herbivory, are much less clear in native grasses. For example, Neotyphodium infections in most native grasses are not toxic to livestock and other vertebrates (Schulthess and Faeth, 1998; Saikkonen et al., 1998; Faeth, 2002; Faeth and Bultman, 2002) or invertebrates (Lopez et al., 1995; Tibbets and Faeth, 1999). Endophyte frequencies also tend to be more variable than agronomic grasses (see references in Leuchtmann, 1992; Bucheli and Leuchtmann, 1996; Clay, 1997, 1998; Saikkonen et al., 1998, 2000; Faeth, 2002; Faeth and Bultman, 2002), although often high in some populations. Neotyphodium-linked alkaloids, the main mechanism for endophyte-related benefits for the host grass, are also more variable in native grasses. Generally, alkaloid types tend be fewer and levels of individual alkaloids lower and more variable than agronomic grasses (Saikkonen et al., 1998; Leuchtmann et al., 2000; Faeth, 2002). Variation in alkaloid levels and types in native grasses are probably linked to: 1) increased genetic heterogeneity of both host grass and endophyte, 2) more variable environments and 3) the interaction between variable genotypes and environments. In general, there are relatively few cases of strong effects of systemic endophytes in native grasses on native herbivores (Faeth, 2002). Even well-known cases of native toxic grasses appear limited to restricted few populations (Kaiser et al., 1996; Jones et al., 2000; Nan and Li 2001; Faeth, 2002).
We propose here that variable frequencies and toxicity of systemic endophytic infections in natural populations may be explained by relative costs and benefits of harboring the endophyte and their associated alkaloids. We first show that alkaloid levels are highly variable for Neotyphodium-infected plants within and among populations of Arizona fescue. We then develop a graphical model using nitrogen as a common denominator for costs and benefits of harboring endophytes. From this model, we make predictions when uninfected and low and high alkaloid-producing endophytes should persist in populations. Finally, we describe an experiment testing the effects of nutrients on growth rate of four grass genotypes that harbor Neotyphodium infections, and the same genotypes from which the endophyte has been experimentally removed.
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Study system
Festuca arizonica (Vasey), Arizona fescue, in the subfamily Pooidaceae, is a dense, perennial bunch grass that reproduces primarily by seed (USDA, 1988
) and is native and widespread in the Southwest (Kearney and Peebles, 1960). Arizona fescue occurs in semi-arid ponderosa pine (Pinus ponderosa)/bunch-grass communities above 2,000 m elevation (Kearney and Peebles, 1960).
Neotyphodium is common in Arizona fescue populations in Arizona (Lopez et al., 1995; Hammon and Faeth, 1992; Schulthess and Faeth, 1998). At least two varieties have been described from Arizona fescue based upon variable spore size and color that appear in culture (White et al., 1993) and molecular DNA (An et al., 1992, 1993) and microsatellite DNA haplotypes (Sullivan and Faeth, 2001).
Alkaloids
Alkaloids were determined from samples of infected plants from two Arizona fescue populations, Merritt Draw and Buck Spring, which are separate drainages about about 3 km apart. Infected plants produce only peramine, often at low levels (Saikkonen et al., 1998, 1999). Peramine concentrations were determined by L. P. Bush at University of Kentucky. Methods for peramine determination can be found in Bush et al. (1997) and Leuchtmann et al. (2000).
Model development and parameters
We developed a graphical model using nitrogen as the common currency for plant growth, endophyte growth and alkaloid production and herbivore consumption of the host plant. This approach seems reasonable because available nitrogen, especially in Arizona soils (Schulthess and Faeth, 1998), is very low, and often limits plant growth (Ettershank et al., 1978; Fisher et al., 1988). Furthermore, the primary basis for herbivore resistance via endophyte symbionts in grasses is fungal production of alklaloids, which are nitrogen-rich compounds. Alkaloids are well-known as plant-based defenses but are costly to produce and may compete with other metabolic processes in plants which produce them (e.g., Ohnmeiss and Baldwin, 1994). Herbivores, alternatively, are deterred by alkaloids in plants, but often respond positively to and increase consumption of plant tissues with increased nitrogen levels (e.g., Slansky and Rodriquez, 1982). Finally, endophytes may alter nitrogen metabolism (e.g., Lyons et al., 1990) and increase nutrient uptake of host grasses by altering fine root structure and changing chemical environments near root zones (Malinowski and Belesky, 1999; Malinowski et al., 1999). Alternatively, endophytes that produce alkaloids also may compete with the plant for nutrients, much like constitutively-based alkaloidal defenses (see references in Karban and Baldwin, 1997). However, endophytes vary in their capacity to produce alkaloid types and amounts, both genetically and environmentally. Thus, nitrogen demand appears as a common thread among endophytes, host grasses and herbivore, and our model is based upon nitrogen flux from the perspective of the host.
We model nitrogen flux in three hypothetical host grasses—an uninfected host grass, one infected with a systemic seed borne endophyte such as Neotyphodium, which produces low alkaloids and an infected grass with an endophyte that produces high alkaloid levels. The graphical model was based upon the following assumptions: 1) presence of systemic endophytes can alter fine root structure and local soil environments (e.g., release of phenolic acids) such that nutrient uptake is enhanced at low soil nitrogen, 2) the endophyte uses nitrogen for its own growth and production of nitrogen-based alkaloids, 3) herbivores reduce plant nitrogen through consumption and, 4) the magnitude of 2) and 3) depend on the amount of alkaloids produced by the endophyte. Finally, we assume that 1–4 are functions of soil nitrogen content.
Experimental test
Four infected ‘mother’ plants from the Merritt Draw study site were split into ramets and treated hydroponically with low levels of the fungicide propiconazole to remove the endophyte. Treatment removes Neotyphodium from about 50% of ramets (hereafter E–); the remaining infected ramets served as infected controls (hereafter, E+F). Other ramets were treated hydroponically but without fungicide and thus remain infected (hereafter E+). The four mother genotypes were selected based upon their peramine alkaloid content, such that two genotypes were low in peramine (<0.3 ppm) and the other two relatively high (>1.8 ppm). After hydroponic treatment, all ramets were planted individually into 16 oz. cups with native soil, and continually split and re-potted as they grew to provide cloned replicates (at least 5 of each).
After one year in the greenhouse, these plants were transplanted into a plot at the Arboretum of Flagstaff (1 m apart) in spring 1998 and randomly assigned the following treatments: 1) ambient water and ambient nutrients 2) supplemented water (1,000 ml per plant every 3 days), 3) added nutrients (1.5 g/liter– 30–15–30 fertilizer, every two weeks and 4) added water (every 3 days) plus supplemented nutrients (every 2 wk). Ambient soil nutrients are very low (e.g., 1–2 ppm N) in native soils at the Arboretum (Schulthess and Faeth, 1998), and this level of fertilizer significantly increases nitrogen content of grass plants (Saikkonen et al., 1999). Likewise, ambient precipitation at the Arboretum is typically zero from the end of summer rains in late August to beginning of winter precipitation in November and December and very low during May–June. The plot (except for area near the plants) was covered with a weed barrier (Dalen Co.) that permits water and nutrient penetration but prevents weed growth and hence unwanted plant competition.
The Arboretum is fenced (4 m high) to exclude livestock and native grazers (elk and deer). Thus, this experiment was conducted under conditions of low herbivory; only small rodents and invertebrates have access to plots.
We measured the rate of growth (diameter and height to estimate plant volume) at the beginning and end of the first growing season. All plants were tested via tissue print immunoassay (Schulthess and Faeth, 1998) to confirm endophyte status. We used a factorial ANOVA to compare differences in mean rate of growth (change in volume within the first growing season). All assumptions of ANOVA were tested and met.
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Graphical model
To build our graphical model of plant nitrogen flux (Fig. 1), we first assume that endophytes stimulate nitrogen uptake according to a decaying exponential function as soil nitrogen increases. We only consider environmental conditions under which plant survival is possible. Here, "zero nitrogen" represents the minimum for survival, rather than zero soil nitrogen per se. Uninfected host grasses do not stimulate nitrogen uptake. For simplicity, we assume that infected plants exist in two states, those with endophytes that produce high levels of alkaloids and those that produce low levels. This assumption is supported by preliminary results on peramine levels in natural populations of Neotyphodium-infected Arizona fescue although infected plants in natural populations produce a wider range of peramine than simply low or high (Fig. 2). Infected plants ranged from zero levels of peramine to 2.3 ppm peramine, levels high enough to increase resistance to invertebrate herbivores (Siegel and Bush, 1996
). We model these two types of infected plants by assuming that high alkaloid endophytes (HAE) use most or all of the nitrogen whose uptake they stimulate, plus additional nitrogen whose rate increases linearly with increasing soil nitrogen (Fig. 1A, B). Alternatively, low alkaloid endophytes (LAE) use nitrogen at a constant rate (Fig. 1A, B). For uninfected plants (No E), the curve = 0 (not shown).
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Next, we assume herbivory removes nitrogen from the host plant via consumption at rates that are either independent of (Fig. 1C), or that depend on, soil nitrogen (Fig. 1D). The first case (Fig. 1C) may represent generalist herbivores such as large grazing ungulates that do not adjust consumption rate based upon plant nitrogen content, but do respond to toxic or noxious allelochemicals. In contrast, the soil nitrogen-dependent case (Fig. 1D) may represent more specialized herbivores that increase consumption based upon soil nitrogen and thus nitrogen content of the host plant. In both cases, herbivores consume at a higher rate from LAE plants HAE plants. As suggested by past studies of Arizona fescue (Lopez et al., 1995
; Schulthess and Faeth, 1998; Tibbets and Faeth, 1999), herbivory on uninfected plants (no E) is basically the same as that on LAE plants (same line as LAE in Fig. 1C, D).
Model outcomes
Summation of the underlying terms, stimulation and endophyte use (Fig. 1A, B) and losses to herbivory (Fig. 1C, D) predicts net nitrogen flux in the host grass and suggests when different endophyte strains should be favored (Fig. 1E, F). At low soil nitrogen, LAE plants should increase net nitrogen flux in their host plants more than HAE plants. Because they do not benefit from endophytic stimulation, no E plants should exhibit a net nitrogen loss through herbivory and thus be at disadvantage, relative to LAE and HAE, at low soil nitrogen. In contrast, at low soil nitrogen, both low and high alkaloid endophytes may produce a net positive nitrogen flux in their hosts. As least in terms of our nitrogen flux model, it is at low soil nitrogen levels that the interaction between host plants and endophytes are potentially mutualistic.
As soil nitrogen increases, however, all three host types (HAE, LAE, no E) show a net nitrogen loss (Fig. 1E, F). Under high soil nitrogen, No E hosts should be favored, followed by HAE and then LAE. Where on the soil nitrogen axis that the shift in advantage from LAE to no E plants occurs depends critically on the relative magnitudes of the stimulation, usage, and herbivory terms.
Experimental results
Presence of the endophyte increased growth rate, as estimated by change in above-ground volume during the growing season (Table 1, Fig. 3). However, plant genotype also strongly influenced growth rate (Table 1, Fig. 4). Furthermore, growth rate varied differently across plant genotypes depending on the presence or absence of the endophyte (significant genotype x endophyte interaction, Table 1), with genotypes 3 and 4 showing the largest positive response in growth rate when the endophyte was present (Fig. 5). No other effects or interactions were significant (Table 1); however we present the endophyte x treatment interaction (Fig. 6) for sake of discussion below.
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Fungicide-treated but infected plants (fungicide controls E+F) were not different in growth rate than fungicide-treated and endophyte-removed (E–) plants (F = 2.81; df =1, 19, P = 0.11), indicating no extraneous effect of fungicide on growth of grasses. Likewise, treatment and endophyte status (E– and E+F) did not interact significantly (F = 1.65, df = 3,19, P = 0.21).
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The simple graphical model suggests that the relative costs and benefits of harboring endophytes, at least in terms of nitrogen flux, change along soil nitrogen gradients. Furthermore, from the perspective of the host plant, relative benefits and costs of harboring endophytes depend on whether the endophyte produces high or low levels of alkaloids and the intensity of herbivory along these gradients. The curve intersections in Figure 1E, F also indicate a shift in advantage from grass hosts that contain symbiotic endophytes to host grasses that do not. The model further suggests that low alkaloid-producing endophytes have greater relative benefits at the lowest levels of soil nitrogen, with the magnitude of this benefit diminishing as soil nitrogen increases.
The parameters of these graphical models have been roughly estimated and more precise measures of endophyte-induced uptake, endophyte usage, and herbivore consumption may change the relationships, especially the location of intersection points for net nitrogen flux (Fig. 1E, F). Intersection points are of particular interest because they represent predicted shifts among host-endophyte types along a soil nitrogen gradient. Empirical data on model parameters are needed to pinpoint where, and how often, these intersections occur. Nevertheless, the graphical model serves as heuristic framework for how endophyte-host interactions may change in varying environments. This is especially important because almost all experimental studies of systemic endophytes in grasses have used the introduced grasses, tall fescue and perennial ryegrass, in agronomic settings, where nutrients are typically supplemented and herbivory is more chronic than in natural settings (Saikkonen et al., 1998; Faeth and Bultman, 2002; Faeth, 2002). For many native grasses, such as Arizona fescue, which are found in low nutrient soils and experience sporadic herbivory (Schulthess and Faeth, 1998), the interactions among endophyte-types and host grasses may be occurring to the left or near the intersection points (Fig. 1E, F). If so we may expect a dynamic shifts in fitness advantages among uninfected and low alkaloid and high alkaloid endophyte-infected plants with relatively small changes in herbivory and available nutrients.
The models also indicate that simply considering whether a host plant is infected or uninfected with an endophyte is not adequate, because costs and benefits to host plants depend on how much alkaloid the endophytic symbiont produces. Most previous experimental studies of the effect of systemic endophytes on host performance or resistance to herbivores have used varieties of infected tall fescue or perennial ryegrass grass compared to an uninfected counterpart. These varieties often have less host and endophyte genetic variation and therefore less variation in alkaloids than native grasses (Faeth, 2002). Recent studies have identified genes responsible for alkaloid production, but abiotic environments can also modify expression (e.g., Wilkinson et al., 2000). For Arizona fescue, it is clear that even within a natural population, infection by Neotyphodium can result in a wide range of peramine levels (Fig. 2). This variation appears mostly determined by endophyte haplotype but also modified by host genotype and local environments (Faeth et al., 2002). For Arizona fescue (Fig. 2), as well as other native grasses harboring systemic endophytes (e.g., Faeth, 2002), most natural populations are mosaics of uninfected and infected host plants, the latter of which greatly vary in alkaloid levels. These mosaics may be maintained by shifting costs and benefits as suggested by our model.
Our experimental results partially support the possibilities outlined by the graphical model (Table 1). Notably, the presence of the endophyte increases growth rate overall (Fig. 3), suggesting an overall advantage to harboring the endophyte in Arizona fescue, at least in terms of growth rate and under restricted herbivory (large grazing vertebrates were excluded). Furthermore, although the interaction of endophyte and treatment is not significant (Table 1), the mean growth rate of infected plants increased in all treatments except the high water and high nutrient treatment (Fig. 6), suggesting that advantages of infection diminish with increased soil moisture and nutrients. These results corroborate those involving agronomic tall fescue, where host performance of infected plants diminished at high soil nutrient levels (e.g., Cheplick et al., 1989).
More notable, however, is the strong effect of plant genotype on growth rate and the interaction of plant genotype with the presence or absence of the endophyte (Table 1, Figs. 4, 5). Plant genotype 3 and especially 4 (genotypes 3 and 4 are significantly different from 1 and 2, P < 0.01, Bonferroni post hoc pairwise test of means), grew much faster when the endophyte was present relative to genotypes 1 and 2. Growth rates of genotypes 1 and 2 appear unaffected by the presence of the endophyte. Interestingly, genotypes 3 and 4 are the high alkaloid producers (>1.8 ppm peramine) while genotypes 1 and 2 produce either zero or only trace amounts (<0.3 ppm peramine). These results suggest that plant and endophyte genotypic combinations are another important source of variation in endophyte-plant interactions. In almost all studies of the ecological effects of endophytes on host grass performance, variation in plant-endophyte genotype combinations has either been ignored or uncontrolled (Saikkonen et al., 1998; Faeth and Bultman, 2002). The experimental results generally indicate that plant genotype is a key, if not overriding factor, in determining how Neotyphodium infections alter plant performance under varying environmental conditions (Faeth et al., 2002). Therefore, plant genotype, and associated endophyte genotype, should be incorporated into future studies of the interactions of endophytes with host plants. Recent evidence (e.g., Wilkinson et al., 2000) shows, like our preliminary data on peramine levels suggests (Fig. 2) that endophyte genotype strongly influences alkaloid production, and our graphical model incorporates this aspect, albeit simplistically, into host plant-endophyte interactions.
Both the model and experiment suggest that the direction and strength of endophyte-host plant interactions depend on plant and endophyte genotype, and environmental conditions. The model included only nitrogen as the common currency, but clearly water availability also influences growth response of the host-endophyte symbioses (Fig. 6). Nevertheless, because many of the purported benefits, as well as the costs, of symbioses between endophytes and host grasses are related to nitrogen budgets, this may be an good starting point for explaining differences in endophyte frequencies among and within grass populations.
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Our model and experimental results suggest an explanation for the observed variation in Neotyphodium infection frequency and in alkaloid production by infected grasses in natural populations. Under varying herbivory and soil nutrients and moisture, cost and benefits of harboring the symbiotic endophyte shifts. Furthermore, all infected grasses are not equivalent but depend on host and endophyte genotype, which in turn influences alkaloid production and its associated cost and benefits. This view of variation in endophyte-host plant symbioses is necessarily more complex than previous ones involving endophyte-agronomic grass symbioses, but is more reflective of endophyte and grass interaction in natural populations and communities.
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ACKNOWLEDGMENTS |
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We thank C. Brillhart, J. M. Horne, N. Fuller, C. Hayes, C. E. Hamilton, R. Keithley, W. Marussich, K. Neil, J. L. Rambo, P. Steiner, and T. J. Sullivan for assistance in the field and lab. We are grateful to L. P. Bush for alkaloid analyses, and The Arboretum of Flagstaff, especially J. Maschinski, for access to field sites. S. Clement and T. J. Sullivan made helpful comments on the manuscript. This research was supported by NSF grants DEB 9727020 and 0128343 to SHF.
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FOOTNOTES |
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1 From the Symposium Living Together: The Dynamics of Symbiotic Interactions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
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References |
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