Fungal Endophytes: Out of Sight but Should Not Be out of Mind

Nordic Society Oikos

Fungal Endophytes: Out of Sight but Should Not Be out of MindAuthor(s): Dennis WilsonSource: Oikos, Vol. 68, Fasc. 2 (Nov., 1993), pp. 379-384Published by: Wiley on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3544856 .

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FO+RU tM FORUM is intended for new ideas or new ways of interpreting existing information. It provides a chance for suggesting hypotheses and for challenging current thinking on

FORUM ecological issues. A lighter prose, designed to attract readers, will be permitted. Formal research reports, albeit short, will not be accepted, and all contributions should be concise

FORAUM~l with a relatively short list of references. A summary is not required.

Fungal endophytes: out of sight but should not be out of mind

Dennis Wilson, Dept of Biology, Univ. of Oregon, Eugene, OR 97403, USA (present address: Dept of Zoology, Arizona State Univ., Tempe, AZ 85287-1501, USA)

Ecologists are becoming increasingly aware that a plant out in the field is not simply a plant but rather a merger of fungal cells with plant tissues; from endophytic fungi in the stems and leaves to mycorrhizal fungi in the roots (endophytic fungi are fungi which invade the stems and leaves of plants but cause no symptoms of disease). Moreover, ecologists know that these fungi can influence the outcome of plant-herbivore interactions. For instance, endophytic fungi in grasses have been shown to confer anti-herbivore and possibly anti-pathogen properties to their hosts (White and Cole 1985, Chris- tensen and Latch 1991, Christensen et al. 1991, Clay 1991). Consequences of endophyte infection have been well studied only in certain grasses for which the anti- herbivore properties have received particular attention. However, anti-herbivore effects of endophytes might be widespread among plants since endophytes have been discovered in almost all examined plants and are probably ubiquitous in the plant kingdom (Carroll 1986, Petrini 1986). In this paper, I shall discuss some hypotheses regarding the important role endophytes might play in plant-herbivore interactions. My main aim is to stimulate the testing of hypotheses about the ecological and evolutionary consequences of endophyte infection. First, I propose that certain plant defense traits are for protection against fungal endophytes and are an evolutionary consequence of endophyte infection. Second, I propose that leaf senescence, as well as nutrient reabsorption, are affected by endophytes. Finally, I wish to caution both plant and insect ecologists in the way they choose controls for experiments involving insect feeding, plant allelochemicals, and DNA gel electrophore- Sis.

Influences of endophytes on plant defenses Have endophytes caused the loss of plant defenses? Herbivores are usually credited with causing selective pressures for the evolution of chemical defenses of

plants (Ehrlich and Raven 1964, Janzen 1966, Rhoades and Cates 1976). However, it has been argued that herbivory alone is not always a strong enough selective force to account for the secondary chemistry of plants (Jermy 1984). Fungal endophytes have a very intimate and most likely coevolutionary relationship with their host plant, and therefore have the potential to influence the evolutionary trajectory of the plant defenses. When the endophyte-plant symbiosis is strongly mutualistic and one of the benefits the host gains is defense against herbivores, the host might largely or wholly rely on the endophytes for their resistance. Since defense against herbivores is assumed to be costly, the host might lose its innate defensive capability and instead rely on endophyte mediated defense. For example, non-ant acacias produce cyanogenic glycosides whereas acacias defended by ants do not (Rehr et al. 1973). This example demonstrates that a plant host with a mutualistic sym- biont may lose its ability to produce defensive com- pounds. (Alternative explanations are that ant acacias never evolved the ability to produce cyanogenic glycosides, or that ants colonized only non-glycosidic producing acacias. Both of these alternative explanations as- sume that the ant-acacias never produced glycosides which leaves the question of how the plants defended themselves from herbivores before the ants were present.)

Consider two other mutualistic symbioses between perennial ryegrass (Lolium perenne L.) and tall fescue (Festuca arundinacea Schreb.) infected with their re- spective endophytes Acremonium lolii Latch, Christen- sen & Samuels and A. coenophialum Morgan-Jones & Gams. Because the endophytes in these grasses are transmitted only vertically, via the seed, from parent to offspring, infected plants are descendents from long lineages of infected individuals where the plant and fungus have evolved together to produce a suite of defense chemicals, notably alkaloids (Siegel and Schardl 1991). If the grasses' own defense from herbivores is more costly than the endophyte-mediated defense (endophyte infection presumably has a cost since

OIKOS 68:2 (1993) 379



the endophyte derives all carbon and nutrients, includ- ing nitrogen for alkaloid production from the host plant) and the risk of losing the endophyte is low, these infected lineages without their own defenses would be favoured by selection and the grasses would rely on defense derived from endophyte infection. Therefore, plants from infected lineages which have lost the endophyte would have reduced defenses compared to uninfected lineages which have never had endophyte-mediated protection from herbivores. (Of course, it may be difficult to determine if an uninfected plant were descended from plants which were never infected or from plants which lost the endophyte.) Thus, in a population of grasses, three morphs are likely to exist: endophyte infected plants, and two types of uninfected plants. Some uninfected plants would be descended from lines which have never been endophyte infected and never lost their own defenses against herbivores, and some from infected lines which have lost the endophyte. The former two morphs would have chemical defenses to deter insect herbivores; whereas plants which grew from seeds where the fungal hyphae lost viability would not have an effective defense against herbivores so would be very scarce.

Results from laboratory feeding trials (Clay 1991) suggest that many insect herbivores find infected plants so unsuitable compared to uninfected plants that uninfected plants could not persist. Yet in almost all samples collected from the field, uninfected plants and infected plants coexist, although the former is often at lower frequencies, especially in older pastures (Lewis and Clements 1986). However, the lineage of plants used for feeding trials might not have been considered. For instance uninfected plants in feeding trial experiments might have been obtained from infected lines where the endophyte has been eliminated from the seed rather than uninfected plants from natural pastures (as in Barker et al. 1984, Johnson et al. 1985). If the grass lineage is not considered, results from feeding trial experiments might be misleading as uninfected plants obtained from infected lineages would be much less resistant to herbivores than uninfected plants from uninfected lineages.

The life cycle of seed-borne endophytes is inexorably tied to their grass hosts. Some plant lineages may be infected for many generations, whilst others uninfected for generations. Since the presence of the endophytes affects such characters as suitability of the plant to insect herbivores, infected and uninfected linages of plants might be under selection to evolve different defensive strategies. Therefore, it is important that the lineage of the plants be considered and controlled for in studies of endophyte-plant-insect interactions.

Have endophytes caused the evolution of some plant defenses?

Plants have evolved a multitude of chemical and mechanical defenses against herbivores and seed predators. It is assumed that feeding damage with a concomitant reduction in plant fitness is the selective pressure driving the evolution of these characters (Krischik and Denno 1983). Despite these defenses all plants have an associated suite of herbivores and seed predators. For example, insect and vertebrate seed predators feed on dry fruits such as acorns despite the thick mechanical and often repugnant chemical protection afforded by the pericarp and to a lesser extent the seed coat. Fruits and seeds may escape predation because they are not detected at low densities or are so abundant that they satiate the seed predators, rather than because they are found then rejected because of their mechanical or chemical properties (Janzen 1969, 1971).

I propose that mechanical and chemical defenses of hard-shelled seeds evolved partly in response to attack by fungi, in particular fungal endophytes that normally asymptomatically inhabit the leaves or other parts of the seed-producing parent. These fungi are already pre- disposed to grow on and within the plant tissue. For instance, Discula quercina (West.) Arx. (Coelomycete), a species of fungal endophyte common in the leaves of Quercus garryana Dougl. (Fagaceae) is also commonly isolated from the pericarps and cotyledons of the acorns collected under oak trees (Wilson 1992). Although present within the seed, this endophyte infects its host tissues horizontally, not vertically, by injection of rain- dispersed spores washed off of old leaves and the bark on young twigs where the endophyte sporulates (Wilson 1992). Germination levels of such acorns in the lab is almost 100%. Even acorns in which beetle larvae have bored large holes and severely damaged the cotyledons have a high germination level if the meristem region is left undamaged. However, if the pericarp and seed coat are removed (i.e., all protective layers exterior to the cotyledons), the fleshy cotyledons and meristem surface sterilized and incubated under low humidity in a sterile chamber, only about 8% of acorns germinate. Most acorns shelled in this way either do not germinate or just start to put out a radicle before they become over- grown by the fungal endophyte. When common con- taminating fungi (which are accidently introduced onto the sterile shelled acorns) grow on the shelled seeds, they do not usually kill the seed and survival rates are much higher. The endophyte appears to infect small localized sites in the cotyledons of a high proportion of the seeds but only grows and damages the seed if the pericarp is removed. If the infected areas of the cotyledons are excised, i.e., in the absence of the endophyte, the acorns usually germinate and grow. Thus, any acorns under a parent oak tree (where high numbers of endophyte spores are present in the rain falling through the canopy) without the particular characteristics of the

380 OIKOS 68:2 (1993)



pericarp to inhibit spore infection or limit subsequent endophyte growth would certainly perish. Hence the parent tree should be under intense selective pressure to evolve a mechanism to prevent endophyte-caused mortality of its acorns.

Undoubtedly, the thick pericarp also protects the seed from nonspecialist predators such as the small arthropods which inhabit the soil, but I argue that without the pericarp and its ability to prevent growth of the endophyte which is lethal to the acorn, acorn mortality from generalist fungi and arthropods would be insignif- icant compared to the endophyte-caused mortality. The fact that the pericarp specifically prevents, or reduces to sublethal levels, growth of the endophyte and that mortality of shelled acorns caused by common lab contam- inating fungi is low, supports the idea that the pericarp may have evolved to protect the fleshy part of the acorn for the endophyte. Endophyte-caused mortality of the seed might be part of the "hidden cost" of endophytism, in addition to the photosynthates the fungi use while inside the healthy plant tissue. Furthermore, endophyte-caused mortality of the acorns might also be a selecting force promoting seed dispersal away from the parent tree. The above evolutionary argument is easy to make but is difficult, at best, to prove. Since the pericarps do play a variety of roles, they may be a pre- adaptation to prevent endophyte-caused mortality of the seed.

Endophytes and leaf senescence Are endophytes the gatekeepers of leaf senescence?

Leaf senescence is a programmed developmental process preceding tissue death during which photosynthetic activity stops and many leaf constituents are broken down and retrieved. This process is followed by leaf abscission, then colonization and decomposition by saprophytic fungi. Because endophytic fungi are present in the healthy leaves of many plants before senescence, they will be the first fungi to capitalize on senescing and abscised leaves, so will be the first species in the succes- sion of decomposing fungi. Although the production of enzymes which degrade certain plant cell wall constituents such as pectin, cellulose, and polygalacturonic acid is widespread amongst endophytes (Petrini et al. 1992), the role of endophytic fungi in decomposition is probably limited to utilizing low molecular weight carbo- hydrates (Carroll and Petrini 1983) before being suc- ceeded by saprophytic fungi which are stronger compet- itors.

Senescence events differ slightly in detached leaf parts compared to whole leaves attached to the plant (Wareing and Phillips 1981). Experiments with detached Quercus garryana leaf discs suggest endophytes could have a role in leaf senescence (Wilson pers. obs.).

Leaf discs cut from surface-sterilized Q. garryana leaves and placed on a nutrient agar medium follow one of two fates depending on whether the endophyte is present or absent from that disc. First, if the endophyte is present, they turn brown and support prolific endophyte growth and sporulation. After several weeks under warm hu- mid conditions these leaf discs are mostly decomposed with only veins left. Second, uninfected leaf discs can remain green for over 18 months and are devoid of fungal growth. Here, the "normal" events of senescence do not appear to take place as the leaf tissue does not turn yellow or brown, a typical visible symptom of senescence (Wareing and Phillips 1981); in addition, decomposition does not take place as there are no microorganisms present. However, some uninfected leaf discs do not remain green indefinitely, after a time they slowly turn brown but remain intact (Wilson pers. obs.).

Do endophytes compete with the host for mobilized nutrients?

Leaf senescence may trigger growth of the endophyte or conversely, endophyte growth may trigger the onset of leaf senescence. In either situation, in Q. garryana, leaf senescence and growth of the endophyte from a quies- cent state within the leaf occur at the same time. Carroll (1990) suggested that the co-occurrence of senescence and endophyte growth could lead to competition between the plant and endophyte for mobilized nutrients which were destined for reabsorption. The presence or absence and relative level of endophyte infection will influence what proportion of leaf nutrients, for example nitrogen, the tree can reabsorb and how much of the nutrients are left in the abscised leaf as endophyte, verses leaf biomass. Furthermore, Stacey (1993) showed that senescent maple leaves infected with tarspot (Rhy- tisma punctata) retained more nitrogen and phosphorus compared to nearest neighbor uninfected leaves. Pre- sumably the fungus utilized some of the nitrogen and phosphorus which was destined for reabsorption from the leaves back into the tree. Although tarspot might not be considered as a completely asymptomatic endophyte, it does reside asymptomatically within the leaf for most of the season. Varying endophyte levels could explain the large variance in amount of nutrients reab- sorbed from leaves between: species, individuals of one species, and leaves from a single plant as observed by Jonasson (1989). In addition, varying endophyte levels could explain why few factors so far studied explain the observed variance in nutrient reabsorption of senescing plants (Chapin and Moilanen 1991, del Arco et al. 1991).

OIKOS 68:2 (1993) 381



Words of caution about controls When should endophytes be controlled for? These words of caution are intended for any biologist who has carried out experiments on plants involving the following: insect host choice, insect performance on plant tissue, biochemical analysis of plant allelochemicals, and nucleic acid or isozyme electrophoresis. Host choice and insect performance experiments usually in- volve placing insects on many replicates of host plant tissue for different treatments (Hardy et al. 1985, Wei- bull 1990). Steps are usually taken to ensure replicates are similar and most variation in plant tissue is controlled for, for example using clones or genetically iden- tical material. However, in the real world plants are usually mosaics of endophyte-infected and endophyte- uninfected tissues with variation in both fungal endophyte species and amount of fungal hyphae present even in apparently comparable tissues which may be from the same individual plant (Carroll and Carroll 1978, Stone 1986, Sieber and Hugentobler 1987, Clark et al. 1989). Despite the widespread occurrence of fungal endophytes in plant tissues, even in well studied systems such as the grasses and their seed-borne endophytes (where the fungi impart herbivore resistance to the infected host plant via the production of alkaloids), fungal endophytes have never been controlled for in any host choice or insect performance experiment if they are not the main focus of the study (Rautapaa 1970, Kieckhefer and Stoner 1978, Weibull 1990 and references therein). The effects of endophytes might not be random with respect to treatment as infection might be correlated with the treatment. For example, two grass cultivars could be tested for differences in insect resistance. One cultivar could have been stored differently causing the endophyte to lose viability (Sie- gel et al. 1984) compared to the other cultivar. Simi- larly, when isolating or estimating amounts of allelochemicals in plants (Schultz et al. 1981, Zucker 1982, 1983) endophytes have never been controlled for. The only adequate control would be to test for the presence of endophytes in the plants being used and use known endophyte-free individuals or include in the design a comparison between infected and uninfected plants. Al- though few infection cycles of endophytes have been worked out, many endophytic fungi appear to infect the host plant horizontally by penetration of plant tissues by spores which land on the plant surface (Stone 1986, Wilson 1992). Systemic growth within the plant of vertically transmitted seed-borne hyphae appears to be mostly restricted to cool season grasses. Endophyte-free leaves of many plants might be obtained by allowing new leaves to grow in isolation from the outside envi- ronment, in particular the rain, e.g., by growing the plant in greenhouses or for large trees by using plastic bags placed over twigs. Endophyte-free Q. garryana leaves were obtained in the field by placing large plastic

bags over twigs, then allowing buds to burst, and leaves to grow inside the bags.

Endophytes and plant allelochemicals

The following will explain why endophytes should be controlled for in the above types of experiments by discussing how endophytes would be expected to change host plant allelochemistry. The plant patholog- ical literature includes abundant descriptions of plant responses to infection by both pathogenic and nonpathogenic fungi. For instance, plants may respond to fungal infection by producing tannins (Bell and Mace 1980), flavonoids (Cruickshank 1980), coumarins (Bell 1980), alkaloids (Cruickshank 1963), terpenoids (Naka- jima et al. 1975), and benzoic acid (Swinburne 1971); all of these allelochemicals are known inhibitors of fungal growth. Moreover, all have been shown to negatively affect insect feeding or performance (Hedin et al. 1974, Jones 1983, Paxton 1991). When endophytes infect plants they would be expected to cause similar induction of defensive chemicals in the tissues they infect, thereby creating mosaics of favorable and less favorable tissue to an insect herbivore. Cross resistance of this type has been demonstrated with cotton. When the cotton plants are infected with a vascular wilt fungus, they are more resistant to mites (Karban et al. 1987). In fact many plant allelochemicals, both induced and constitutive, are repellant or toxic to generalist insect herbivores but are attractants or feeding and oviposition stimulants to specialist insect herbivores. Thus, endophyte infection with a concomitant induction of plant allelochemicals could affect both absolute resistance of plants to insect herbivores, i.e., whether any insect herbivore will feed on the plant or plant part, as well as the type of insects (specialist verses generalist) that find the plant attrac- tive.

Colonization of plant tissues with nonpathogenic strains or species of fungi often renders the plant more resistant to pathogenic fungi because of the production of phytoalexins (Matta 1971, Suzuki 1980). Hence endophyte infection status could explain the acute suscep- tibility to both insect and fungal diseases of greenhouse- raised plants after they are planted in the field, since in the greenhouse the plants would not have received the same inoculum of endophyte and other fungal spores, that they usually experience outside. Therefore, they would not have been exposed to microorganisms which attempt infection and cause a defense response that can also act to "immunize" the plants against subsequent infection.

Endophytes could produce the allelochemical Endophytes may not simply cause plants to produce anti-fungal agents which also have anti-insect proper-

382 OIKOS 68:2 (1993)



ties, the fungi may actually produce the allelochemical. Before the anti-insect properties of alkaloids produced by grass endophytes were known, alkaloids were identified as a chemical defense of grass plants (Jeffrey 1970). It was assumed the alkaloids were of plant origin but it is now known that certain of the alkaloids found in grasses with anti-insect properties are endophyte produced. Patric Dowd (1991 symposium on the biology of fungal secondary metabolites at the annual meeting of the Mycological Society of America) noted the simi- larity of both structure and properties between many plant secondary metabolites and fungal toxins. For example, macrocyclic trichothecenes, potent protein-synthesis inhibiting mycotoxins produced by several common genera of fungi such as Fusarium, Trichothecium, and Trichoderma, have been isolated from extracts of the Brazilian shrub Baccharis megapotamica Spreng (Asteraceae) (Jarvis et al. 1987). However, no endophytes were found in this shrub after microscopic exam- ination of certain plant parts (Jarvis and Midiwo 1988). Related to this, seeds of the West Indian tree, Maytenus rothiana (Walp.) Lobreau-Callen, and bark of the Texan gulf tree, M. phyllanthoides Benth (M. texana (Benth) Lundell), contain maytansine, a maytansinoid typically produced by fungi (Nettleton et al. 1981). En- dophytic fungi are good candidates which are respon- sible for producing chemicals which are typically produced by fungi but which are also identified as plant allelochemicals. Alternatively, if endophytes are not the allelochemical producer, they could be vehicles of hori- zontal gene transfer (Jarvis and Midiwo 1988) which would also explain how certain plants can produce toxins otherwise only found in fungi.

Controls in isozyme and electrophoretic studies

When genetic or isozyme electrophoretic studies are conducted on plant tissue it is assumed that it is the plant's genetic material and isozymes which are being extracted to run on a gel. In reality, when the tissue is ground for extraction both the fungal endophyte, if present, and plant nucleic acids and enzymes are present. How much fungal DNA is present in plant extracts used in restriction fragment length DNA polymor- phism, and how much fungal DNA has been extracted, then amplified, in PCR (Polymerase Chain Reaction) machines? Moreover, how much difference in band pat- tern or band "noise" is caused by fungal endophyte DNA? Although investigators carefully control for contaminants, endophytes are not accidental contaminants; rather they are integrated with the plant tissue. Unless separated from the plant DNA, endophyte DNA will always be present in the DNA extract. Because endophytes have never been controlled for, biologists should be aware of interpretive problems which may be caused by the presence of endophytes. Possible solutions are to use known endophyte free plant tissues

for a comparison, or use probes which specifically bind to DNA sequences in the target organism.

The significance of endophyte infection probably ex- tends far beyond enhanced resistance to herbivores. Indeed, the grasses might be a special case with regard to the mechanism endophytes mediate host resistance to herbivores; furthermore many endophyte-plant symbioses might not be mutualistic in all respects. In the real world, functionally, plants are not solely plant tissues, so they should be treated as evolving integrated symbiotic units of plant and fungal cells which can affect many ecological and physiological processes.

Acknowledgements - I would like to thank G. C. Carroll, W. E. Bradshaw, J. Stone, 0. Petrini, C. G. Jones, T. G. Whitham, and D. R. Strong for inspirational conversation and comments. I am grateful for support from Sigma Xi, American Natural History Museum, and a Mary Aldon Scholarship.

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Fungal Endophytes: Out of Sight but Should Not Be out of Mind