| Limitations to Production | |||||||||||||||||
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| Introduction | ||
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Research with tall fescue for much of the past 30 years focused on the detrimental effects of endophyte-infected (E+) plants on livestock performance and metabolism. Some symptoms of fescue toxicosis in livestock include grazing during cooler parts of the day, standing in water or shade, reduced forage intake, reproductive inefficiencies, rough hair coat, formation of hard fat (fat necrosis) in mature cows, and restricted circulation to the extremities (distal vasoconstriction) with the eventual loss of hooves or the tip of ears and tail. Emergent evidence suggests that many E+ plants grow and persist despite stressful conditions, and that plants lacking endophyte (E-) are likely to be at a competitive and adaptive disadvantage. Expression of responses to abiotic stress depends on specific host-endophyte associations (Bacon, 1993).
Most tall fescue plants in wild and naturalized stands are endophyte infected. It could be that infection increased plant vigor and ability to compete with other plants. Apparently, endophyte promotes survival, with or without grazing, through an array of physiological and morphological adjustments to external stresses (Figure 1). Enhanced ecological fitness may involve grazing deterrence (infected plants produce anti-herbivory compounds that affect grazer physiology or behavior). Larger plants have an advantage in resource capture (i.e., water and nutrient uptake) and ability to tolerate grazing in stressful conditions. The complex relationship between the host plant and endophyte is a function of direct and indirect effects of the endophyte on metabolic and developmental processes influencing plant production and persistence. We review the attributes of host plant-endophyte interactions with emphasis on tall fescue responses to abiotic stresses. |
| 1. Zone of adaptation and relation to endophyte | |||
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Tall fescue is the primary cool-season perennial forage grass adapted to the east-central, or mid-south of the US (Chapter I). Abiotic (e.g., weather extremes and physical and chemical soil properties) stresses in this zone include mineral nutrient extremes, and drought and high temperature stresses during summer. Nutrient imbalances occur because soils in much of the range in which tall fescue is adapted tend to be highly weathered and eroded. Field trials showed that E+ stands yielded more and persisted longer than E- stands in the southern portion of the adaptation zone, including Texas (Read and Camp, 1986), Louisiana (Joost and Coombs, 1988), Arkansas (West et al., 1993) and Georgia (Bouton et al., 1993). Endophyte helps tall fescue persist south of the dashed line drawn across the tall fescue zone map (Figure 2). The line represents a transition from north to south, of
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| 1.1 Water stress | |||
Tall fescue pastures in Texas that were dominated by E+ plants (94% infestation) had greater persistence than low-endophyte (12% infestation) pastures (Read and Camp, 1986). Greenhouse and small plot experiments showed that E+ plants had enhanced drought tolerance (Arachevalata et al., 1989; West et al., 1988, 1993). The mechanisms enabling this are complex, and probably involve numerous factors. Protecting growing points (apical meristems) from irreversible desiccation is one way to ameliorate the impact of drought. Osmotic adjustment (promotion of active solute accumulation in cell sap) was greater in the base of vegetative tillers (where cell growth occurs) of E+ than E- plants, with the magnitude of adjustment related to tiller survival (Elmi and West, 1995). Cell solute accumulation slowed the loss of cell turgor in or near growing points, protecting tissue capable of regenerating after drought. More simple sugars accumulated in leaf sheaths of drought-stressed E+ than E- plants, which could help minimize desiccation or freezing damage to cells (Richardson et al. 1992). | |||
In a field trial, water content of outer leaf sheath of vegetative tillers was greater in E+ than E- plants, suggesting that water loss would be less and the plant protected from wilting (Elbersen and West, 1996). Shoot mass and tiller numbers often are greater in E+ than in E- plants (Arachevaleta et al., 1989; De Battista et al., 1990; Hill et al., 1990; West et al., 1993); however, some tall fescue genotypes are unaffected or grow less when endophyte infected (Belesky et al., 1989). A greater rate of tillering by certain E+ plants delays tiller number decline (West et al. (1993). | |||
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West (unpublished data) observed that E+ plants were not grazed as much as E- plants, presumably because substances produced by the host-endophyte association reduced forage palatability. Abiotic stresses can enhance production of these substances.
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Stomates of E+ plants appeared to close earlier at the onset of drought compared with E- plants grown under highly controlled conditions (Belesky et al., 1987; Elmi and West, 1995). In contrast, field-grown E+ plants tended to have greater stomatal conductance and less leaf rolling (a symptom of water deficit stress) than E- plants of the same genotype (Elbersen and West, 1996). This might reflect the ability of E+ plants to develop large root systems that improve access to soil water, delaying onset of drought stress symptoms. | |||
Mechanisms of endophyte-enhanced host plant persistence include a range of cellular metabolism and whole-plant responses (Fig. 6). Endophyte infection produces populations with diverse responses to stress leading to a high degree of resilience within the population. In some instances, physiological and morphological adjustments to abiotic stresses influence plant response to biotic stresses (see Malinowski and Belesky, 2000). Involvement of endophyte on host plant response to temperature (often associated with water stress) is not well defined. |
| 2. Light-related factors |
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The amount and type of light reaching a plant canopy influences the ability of a plant to acquire water and nutrients, allocate dry matter and carry on energy-dependent metabolic processes. Unlike what we know about the influence of endophyte and water-related stress on the host, there is little information on endophyte-infection and host response to light quantity and quality. Belesky and Malinowski (1999) considered how light affects host-endophtye responses to abiotic stress. Light influences allocation of photosynthate among plant structures and regulates the expression of tillers. Since E+ plants appear to have greater rates of tillering, interacting effects of light quality and endophyte infection could influence this process and ultimately competitive ability in a range of canopy environments. Herbage production or plant size is linked to competitiveness of plants (Harper 1977). Dense swards influence light quality by absorbing more of certain light wavelengths within the canopy. The altered light environment leads to different amounts and quality of light that can influence tiller production, leaf elongation and phytomass. Changes in allocation affect the amount of photosynthate available for growth, storage or use in secondary metabolite production, as well as nutrient and water acquisition. High temperatures and high light intensities are likely to occur simultaneously, especially in southern portions of the tall fescue adaptation zone (Fig. 1). Ability to tolerate water deficit and maintain photosynthetic capability at high leaf temperature and light intensity is a competitive advantage for cool-temperate origin species in the southeastern US. This ability contributes to the versatility of tall fescue as a forage resource and provides pasture managers with a high-quality plant material for use in areas dominated by warm-season species. |
| 3. Mineral-related stresses and tall fescue-endophyte associations | |||
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Tall fescue persists under a wide range of soil conditions including high exchangeable Al, low pH, low phosphorus (P) availability, and shallow and eroded sites. Apparently, tall fescue can avoid or tolerate chemical and physical stresses by making physiological and morphological changes. For example, plant-available P often is limited on acidic soils. Endophyte, although localized in the aboveground portion of the plant, seems to elicit some of the same responses in tall fescue as observed in other plant species infected by mycorrhizal fungi. Mycorrhizae, live on and in roots of many plant species and facilitate mineral, especially P, and water acquisition by the host. The E+ plants can acquire P from soils with limited amounts of available P. Some of the earliest applied research on tall fescue toxicity considered alkaloid production as a function of nutrient inputs (Gentry et al. 1969). Nitrogen increased production of alkaloids, perloline in particular, compared to unfertilized controls. Perloline concentrations were less when P and K were applied. Nitrogen had large and predictable effects on alkaloid production in tall fescue that varied with specific host-endophyte association. Cheplick et al. (1989) suggested that the host plant incurred a metabolic cost to support endophyte. The cost, expressed in terms of smaller plants, would not be realized unless stressful environmental conditions occurred, with differences between infected and non-infected (E-) associations greater in young plants. Responses varied among cultivars and clones within cultivars with similar results observed in later experiments on mineral stress responses (Belesky and Fedders, 1995; Zaurov et al., 2001). Endophyte-infected plants either grew better, similar to or were impaired relative to E- plants when nutrients were limited. Growth of very young E+ plants was depressed relative to E- plants at low nutrient status and no differences in growth were apparent under high nutrient conditions. Early seedling development and resource allocation in host plants of similar genotype but with different endophyte strains, suggests that early seedling (up to six wk of age) growth and tiller production of certain E+ compared to E- plants is slow with unlimited nutrient supply (Belesky, unpublished data) | |||
| 3.1 Soil acidity | |||
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Tall fescue is grown on millions of hectares in the warmer portions of the humid eastern US. It is used on soils where pH and nutrient supply restrict plant productivity, because of prior land use practices, relatively high rainfall amounts and by soil geochemistry. Plants adapted to acidic soils have a variety of mechanisms that help them tolerate or overcome adverse soil chemical conditions. For example, soil acidity affects plant growth through a complex of chemical changes in the rhizosphere involving increased H+, Al and Mn. These include inhibition of metal cation (Ca, Mg) uptake, a decrease in P and Mo solubility and increased efflux of nutrients and metabolites from roots. Root morphology and function also change when soil chemical conditions are less than ideal for plant growth. The net effect is changed nutrient activity in the root zone and physiological and morphological adaptations to stress in root tissue. The widespread use of KY-31 tall fescue as a conservation resource and forage is partly related to endophyte infection. Some early evidence suggested that tall fescue excluded mineral elements harmful to plants. Jacobson et al. (1963) reported higher Al in nontoxic compared to toxic tall fescue hay fed to cattle. Although the involvement of endophyte infection was unknown at the time, it might have been that toxic hay was infected and nontoxic hay devoid of, or had much less endophyte, and as such E+ plants were able to minimize Al translocation to shoots. Endophyte-infected tall fescue produced less root mass than E- plants under simulated acid rain, although the response depended on plant age (Cheplick, 1993). Soil acidity influenced dry matter production and allocation differently in clones of five tall fescue-endophyte associations (Belesky and Fedders, 1995). In general, E+ plants tended to tolerate soil acidity, but not all associations did so to the same extent. Fine-leafed fescues (e.g., F. rubra, F. ovina, F. longifolia) tolerate modest soil fertility. When grown under Al-induced stress, E+ plants had longer and heavier roots, and heavier shoots relative to E- lines (Liu et al., 1996), suggesting that E+ plants were more Al tolerant than E- plants. Larger root systems could be a function of plant age or an expression of fine-leaf fescue morphology. Response to Al-induced stress varied among specific clonal lines and associated endophytes of fine-leaf fescues (Zaurov et al., 2001). Growth was influenced by plant genotype-endophyte interaction. In some cases, shoot mass was greater in E+ than in E- plants grown on high Al soil, but in most instances infection did not influence shoot mass. High Al suppressed growth of some E+ clones. Consequently, broad generalization about endophyte infection and tolerance to Al stress could not be made. | |||
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The mechanisms of soil acidity tolerance in grasses, particularly endophyte-infected grasses, are not understood in detail. Low soil pH and high soluble Al concentrations restrict root growth, and affect N uptake and N supply to growing leaves. Phenolic-like compounds can chelate Al, and may help plants transport Al in non-toxic forms (see Fig. 7). Tall fescue accumulated much less Al in shoots than roots, suggesting a means to sequester Al in the roots (Foy and Murray, 1998). Phenolic-like compounds exuded
Tall fescue often grows where pH and soil acidity related factors influence P availability and plant growth. Agronomic practices and growing conditions influence P availability and are important when managing E+ tall fescue. For example, P uptake and herbage production were greater in E+ than E- plants when soil P availability was low; however, mass was less in E+ than E- plants at high soil P availability (Malinowski et al., 1998b). Low P led to greater specific root length (i.e., finer roots) in E+ plants and greater concentrations of P, Mg, and Ca in roots and shoots of E+ than E- plants (Malinowski et al., 2000). Infected plants had more root DM (10%) and greater relative growth rate (16%) than E- plants when P was supplied as phosphate rock, but endophyte-mediated responses were minimal when conventional P fertilizer was applied (Malinowski & Belesky, 1999b). This was observed in a separate investigation of endophyte influence on mineral concentrations in tall fescue (Vazquez-de-Aldana et al., 1999). Endophytes accumulate P and apparently place some demand on P absorbed by the host (Azevedo and Welty, 1995). | |||
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Two endophyte-related mechanisms for P uptake appear in tall fescue grown in P-deficient conditions: 1) altered root morphology (Fig. 9); and 2) increased activity of root exudates (Fig. 7 & 8). Endophyte-infected tall fescue grown in nutrient solution produced roots with smaller diameter and longer root hairs than E- plants, regardless of the amount of P available for plant uptake (Malinowski et al., 1998a). They also showed that E+ tall fescue produced greater amounts of phenolic-like compounds in roots (as well as shoots) when P was limited. Zhou et al. (2003) reported similar findings for perennial ryegrass. These compounds could leak out of roots to change the availability of mineral nutrients or influence microbial or biological activity in the rhizosphere near the root surface. Since phenolic-like compounds were detected in E- plants as well, they might not be endophyte-specific but regulated by endophyte when the host plant encounters additional stresses. Garner et al., (1993) proposed that P was involved in ergot alkaloid biosynthesis for tall fescue endophytes, linking P nutrition with ergo-alkaloid production in infected grasses. Ergo-alkaloid concentrations increased as P availability increased in endophyte-tall fescue associations, especially those with low ergo-alkaloid production capability (Malinowski et al., 1998b). | |||
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| 3.3 Zinc | |||
Endophyte-infected perennial ryegrass (Lolium perenne) was able to grow in the presence of excessive Zn (Monnet, 2001), possibly because of a mechanism which appears to exclude Zn from roots and which is similar to that proposed by Malinowski et al. (1998a) and Malinowski and Belesky (1999a). Endophyte infection excludes Zn but allows Mn to accumulate in leaves. Zinc accumulates in some soils near industrial sites, and E+ plants might serve as reclamation or cover crops. | |||
| 3.4 Copper | |||
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Copper concentrations were less in E+ compared to E- plants (Dennis et al., 1998). Deficiency was expressed as decreased Cu-related immune function (Saker et al., 1998). Cattle grazing E+ tall fescue showed symptoms of deficiency (coat condition and hair color) by the end of the grazing season (Coffey et al., 1992). Copper concentrations in E- Kentucky-31 tall fescue grown in Virginia and Mississippi increased as the growing season progressed (Allen et al., 1997). Steers consuming E+ tall fescue grown in Virginia had lower serum Cu concentrations than steers fed E- plants, while no differences in serum Cu were observed in steers fed tall fescue grown in Mississippi. Apparently, Cu uptake is influenced by endophyte, as well as soil composition. Endophyte-infected plants seem to restrict translocation of potentially toxic metal ions to above-ground tissues; however, low concentrations of essential micro-nutrients and bioavailability factors could raise concerns about nutritive quality in extensively managed tall fescue pasture. Plants host specific endophyte races that may elicit toxic effects in grazers, or ecological benefit to the host-endophyte association. Some endophytes do not cause toxicity or produce toxic alkaloids when removed from their natural host and grown in a different plant genotype. One such endophyte (endophyte AR542) inserted into tall fescue, increased Cu2+-binding activity by root exudates of tall fescue when P was deficient in nutrient solution. Under experimental conditions, the phenomenon did not appear to interfere with Cu accumulation in shoot tissues; however, significance under field conditions, where Cu concentrations in soil are much lower and P may easily limit growth cannot be underestimated (Malinowski et al., 2003). This process may interfere with Cu uptake under field conditions, and influence concentrations of minerals antagonistic to Cu, such as Mo, affecting Cu absorption from forage by grazing animals. | |||
| 3.5 Nitrogen | |||
The influence of endophytes on N metabolism of tall fescue was one of the first mineral nutrient interactions discovered in endophyte-infected plants. The amount of N in leaves was less in E+ than in E- leaves at all rates of N (Lyons et al. 1990), suggesting a greater N economy in E+ plants. A number of experiments showed that N enhanced alkaloid production in E+ plants and thus could lead to plants that are more harmful to livestock than plants growing in N-poor soils. Nutrient deficiency, specifically N deficiency, could restrict the growth of some E+ plants of Festuca and Lolium species (Cheplick et al., 1989), and poverty grass (Danthonia spicata L.); a species common on marginal and low fertility sites (McCormick et al., 2001). | |||
| 3.6 Other minerals | |||
Information on the influence of endophyte on mineral composition of forage grasses is limited. Vazquez-de-Aldana et al. (1999) published results from the only experiment addressing the influence of endophyte infection that deals specifically with mineral composition of tall fescue. Nitrogen and Mg were greater in E+ than in E- tall fescue, and time and infection interacted to influence concentrations of certain mineral elements (Vazquez-de-Aldana et al. 1999). Hill (1995) noted that Ca fertilization increased ergoalkaloid production in E+ tall fescue independent of soil pH, but attempts to validate the observation with additional experiments proved inconclusive (N.S. Hill, personal communication). Less Ca and more Mg accumulated in E+ than E- plants, while P and K were not affected (Hoveland et al., 1984). Consistently higher concentrations of Fe occurred in E- than in E+ plants (Dennis et al., 1998). |
| Summary |
When Bacon (1993) reviewed the interaction of abiotic stresses and endophyte infected plants, he proposed that specific host-endophyte associations would have unique expression of the symbiosis. The expression would vary with the genetic signature of each component, the environment in which the association was growing and external stresses. The benefit of a particular association would be measured in terms of influences on survival of the symbiotic components. In the intervening years, new techniques and expanded understanding of the causes associated with host-endophyte toxicity led to development of transformed host-endophyte associations. The native endophyte of a particular host was replaced by a race with specific desirable biochemical features and expression of those characteristics in practical agricultural situations (e.g., herbage palatability; minimal harmful alkaloids). The ecological attributes of transformed associations are unknown, and warrant further investigation to determine whether the wide adaptation of host-endophyte associations persists when production of grazing deterrents is lessened and native endophytes are removed. |
| Acknowledgements |
The authors thank Professor Henry A. Fribourg and anonymous reviewers for supportive and constructive suggestions to improve the presentation. Thanks also to Ms S. Boyer for assistance with illustrations. |
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