Abstract
A central component in understanding plant–enemy interactions is to determine whether plant enemies, such as herbivores and pathogens, mediate the evolution of plant secondary metabolites. Using 26 populations of a broadly distributed plant species, sagebrush (Artemisia tridentata), we examined whether sagebrush populations in habitats with a greater prevalence of fungi contained antifungal secondary metabolites on leaf surfaces that were more active and diverse than sagebrush populations in habitats less favorable to fungi. Because moisture and temperature play a key role in the epidemiology of most plant–pathogen interactions, we also examined the relationship between the antifungal activity of secondary metabolites and the climate of a site. We evaluated the antifungal activity of sagebrush secondary metabolites against two fungi, a wild Penicillium sp. and a laboratory yeast, Saccharomyces cerevisiae, using a filter-paper disk assay and bioautography. Comparing the 26 sagebrush populations, we found that fungal abundance was a good predictor of both the activity (r 2 = 0.36 for Saccharomyces, r 2 = 0.37 for Penicillium) and number (r 2 = 0.34 for Saccharomyces) of antifungal secondary metabolites. This suggests that selection imposed by fungal pathogens has led to more effective antifungal secondary metabolites. We found that the antifungal activity of sagebrush secondary metabolites was negatively related to average vapor pressure deficit of the habitat (r 2 = 0.60 for Saccharomyces, r 2 = 0.61 for Penicillium). Differences in antifungal activity among populations were not due to the amount of secondary metabolites, but rather to qualitative differences in the composition of antifungal compounds. Although all populations in habitats with high fungal prevalence had secondary metabolites with high antifungal activity, different suites of compounds were responsible for this activity, suggesting independent outcomes of selection on plants by fungal pathogens. The location of antifungal secondary metabolites on the leaf surface is consistent with their putative defense role, and we found no evidence supporting other functions, such as protection from ultraviolet light or oxidation. That the antifungal activity of sagebrush secondary metabolites was similar for two different fungi provides support for broad antifungal defenses. The incidence and severity of fungal disease in the field (caused by Puccinia tanaceti) were similar in moist and dry habitats, possibly reflecting an equilibrium between plant defense and fungal attack, as sites with greater fungal abundance compensated with more effective secondary metabolites. The geographic correlation between fungal abundance and antifungal secondary metabolites of sagebrush, coupled with our other data showing heritable variation in these metabolites, suggests that pathogenic fungi have selected for antifungal secondary metabolites in sagebrush.
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REFERENCES
Anderson, A. J. 1982. Preformed resistance mechanisms, pp. 119–137, in M. S. Mount and G. H. Lacy (eds.). Phytopathogenic Prokaryotes. Academic Press, New York.
Atkinson, P. and Blakeman, J. P. 1982. Seasonal occurrence of an antimicrobial flavanone, sakuranetin, associated with glands on leaves of Ribes nigrum. New Phytol. 92:63–74.
Berenbaum, M. R. 1978. Toxicity of a furanocoumarin to armyworms: a case of biosynthetic escape from insect herbivores. Science 201:532–534.
Berenbaum, M. R. 1995. The chemistry of defense: theory and practice. Proc. Natl. Acad. Sci. USA 92:2–8.
Berenbaum, M. R., Zanderl, A. R., and Nitao, J. K. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40:1215–1228.
Bhadane, N. R., Kelsey, R. G., and Shafizadeh, R. 1975. Sesquiterpene lactones of Artemisia tridentata ssp. vasayana. Phytochemistry 14:2084–2085.
Blakeman, J. P. and Atkinson, P. 1981. Antimicrobial substances associated with the aerial surfaces of plants, pp. 245–263, in J. P. Blakeman (ed.). Microbial Ecology of the Phylloplane. Academic Press, New York.
Brown, D., Asplund, R. O., and McMahon, V.A. 1975. Phenolic constituents of Artemisia tridentata ssp. vasayana. Phytochemistry 14:1083–1084.
Burdon, J. J. and Thrall, P. H. 1999. Spatial and temporal patterns in coevolving plant and pathogen associations. Am. Nat. Suppl. 153:15–33.
Burrage, S.W. 1970. Environmental factors influencing the infection of wheat by Puccinia graminis. Ann. Appl. Biol. 66:429–440.
Clay, K. and KOVER, P. 1996. Evolution and stasis in plant-pathogen associations. Ecology 77:997–1003.
Cooke, R. C. and WHIPPS, J. M. 1993. Ecophysiology of Fungi. Blackwell Scientific Publications, Oxford, United Kingdom.
De Vallavielle-Pope, C., Huber, L., Leconte, M., and Goyeau, H. 1995. Comparative effects of temperature and interrupted wet periods on germination, penetration and infection of Puccinia striiformis f.sp tritici and P. striiformis urediniospores on wheat seedlings. Phytophathology 85:409–415.
Dhingra, O. D. and Sinclair, J. B. 1995. Basic Plant Pathology Methods, 2nd ed. Lewis Publishers, Boca Raton, Florida.
Dirzo, R. and Harper, J. L. 1982. Experimental studies on slug-plant interactions: the performance of cyanogenic and acyanogenic morphs of Trifolium repens in the field. J. Ecol. 70:119–138.
Dolinger, P. M., Ehrlich, P. R., Fitch, W. L., and Breedlove, D. E. 1973. Alkaloid and predation patterns in Colorado lupine populations. Oecologia 13:191–204.
Duke, S. O. and Paul, R. N. 1993. Development and fine structure of the glandular trichomes of Artemesia annua L. Int. J. Plant Sci. 154:107–118. 2166 TALLEY, COLEY, AND KURSAR
Edwards, P. G. 1992. Resistance and defense: the role of secondary plant substances, pp. 69–84, in P.G. Ayres (ed.). Pests and Pathogens. Plant Responses to Foliar Attack, BIOS Scientific Publishers Limited, Oxford, United Kingdom.
Ehleringer, J. R. and Mooney, H. A. 1978. Leaf hairs: effects on physiological activity and adaptive value to a desert shrub. Oecologia 37:183–200.
Ehrlich, P. R. and Raven, P. H. 1964. Butterflies and plants: a study in plant coevolution. Evolution 18:586–608.
Elleman, C. J. and Entwistle, P. F. 1985. Inactivation of a nuclear polyhedrosis-virus on cotton by the substances produced by the cotton leaf surface glands. Ann. Appl. Biol. 106:83–92.
Endler, J. A. 1986. Natural Selection in theWild. Princeton University Press, Princeton, New Jersey.
Farr, D. F., Bills, G. F., Chamuris, G. P., and Rossman, A. Y. 1989. Fungi on Plants and Plant Products in the United States. The American Phytopathological Society, St. Paul, Minnesota.
Ferguson, C.W. 1964. Annual Rings in Big Sagebrush. University of Arizona Press, Tucson, Arizona.
Futuyma, D. J. 1983. Evolutionary interactions among herbivorous insects and plants, pp. 207–231, in D. J. Futuyma and M. Slatkin (eds.). Coevolution. Sinauer Associates, Sunderland, Massachusetts.
Geagea, L., Huber, L., and Sache, I. 1999. Dry dispersal and rain splash of brown (Puccinia recondita f.sp. tritici) and yellow(P. striiformis) rust spores from infected wheat leaves exposed to simulated raindrops. Plant Pathol. 48:472–482.
Gomulkiewicz, R., Thompson, J. N., Holt, R. D., Nuismer, S. L., and Hochberg, M. E. 2000. Hot-spots, cold spots, and the geographic mosaic theory of coevolution. Am. Nat. 156:156–174.
Hakulinen, J., Sorjonen, S., and Julkunen-Tiitto, R. 1999. Leaf phenolics of three willow clones differing in resistance to Melampsora rust infection. Physiol. Plant 105:662–669.
Hammerschmidt, R. 1999. Phytoalexins—what have we learned after 60 years. Annu. Rev. Phytopathol. 37:285–306.
Hargreaves, J. A., Brown, G. A., and Holloway, P. J. 1982. The structural and chemical characteristics of the leaf surface of Lupinus albus L. in relation to the distribution of antifungal compounds, pp. 331–340, in D. F. Cutler, K. L. Alvin and C. E. Price (eds.). The Plant Cuticle. Linnean Society Symposium No. 10. Academic Press, London.
Harrison, J. G., Lowe, R., and Williams, N. A. 1994. Humidity and fungal diseases of plants—problems, pp. 79–97, in J. P. Blakeman and B. Williamson (eds.). Ecology of Plant Pathogens. CAB International, Wallingford, United Kingdom.
Hau, B. and De Vallavieille-Pope, C. 1998. Wind-dispersed diseases, pp. 323–347, in D. G. Jones (ed.). The Epidemiology of Plant Diseases. Kluwer Academic Publishers, Boston Massachusetts.
Hermann, G. J., King, E. J., and Shaw, J. M. 1997. The yeast gene, MDM20, is necessary for mitochondrial inheritance and organization of the actin cytoskeleton. J. Cell Biol. 137:141–153.
Homans, A. L. and Fuchs, A. 1970. Direct bioautography on thin-layer chromatograms as a method for selecting fungitoxic substances. J. Chromatogr. 51:327–329.
Jermy, T. 1984. Evolution of insect/host plant relationships. Am. Nat. 124:609–630.
Jones, D. 1998. The Epidemiology of Plant Diseases. Kluwer Academic Publishers, Boston Massachusetts.
Jones, D. A. 1972. Cyanogenic glycosides and their function, pp. 103–124, in J. B. Harborne (ed.). Phytochemical Ecology. Academic Press, London.
Jones, D.A. 1988. Cyanogenesis in animal-plant interactions, pp. 151–164, in D. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. John Wiley & Sons, New York.
Kelsey, R. G. 1974. The systematic usefulness of the sesquiterpene lactones in the genus Artemisia, section Tridentatae (sagebrush) of Montana. PhD dissertation. University of Montana, Missoula, Montana.
Kelsey, R. G. 1982. Rapid extraction of sesquiterpene lactones from sagebrush for use as taxonomic markers. J. Range Manage. 35:269. ANTIFUNGAL LEAF-SURFACE METABOLITES 2167
Kelsey, R. G. AND Shafizadeh, F. 1980. Glandular trichomes and sesquiterpene lactones of Artemisia nova (Asteraceae). Biochem. Syst. Ecol. 8:371–377.
Kelsey, R. G., Morris, M. S., Bhadane, N. R., and Shafizadeh, F. 1973. Sesquiterpene lactones of Artemisia. TLC analysis and taxonomic significance. Phytochemistry 12:1345–1350.
Kelsey, R. G., Thomas, J. W., Watson, T. J., and Shafizadeh, F. 1975. Population studies in Artemisia tridentata ssp. vaseyana: chromosome numbers and sesquiterpene lactone races. Biochem. Syst. Ecol. 3:209–213.
Kelsey, R. G., Morris, M. S., and Shafizadeh, F. 1976. The use of sesquiterpene lactones as taxonomic markers in the shrubby species of Artemisia (section tridentatae) in Montana. J. Range Manage. 29:502–505.
Kelsey, R. G., Stephens, J. R., and Shafizadeh, F. 1982. The chemical constituents of sagebrush foliage and their isolation. J. Range Manage. 35:617–622.
Kelsey, R. G., Wright, W. E., Sneva, F., Winward, A., and Britton, C. 1983. The concentrations and composition of big sagebrush essential oils from Oregon. Biochem. Syst. Ecol. 11:353–360.
Lively, C. M. 1999. Migration, virulence, and the geographic mosaic of adaptation by parasites. Am. Nat. Suppl. 153:34–47.
Marquis, R. J. 1992. The selective impact of herbivores, pp. 301–325, in R. S. Fritz and E. L. Simms (eds.). Plant Resistance to Herbivores and Pathogens. The University of Chicago, Chicago Illionois.
Marquis, R. J. and Alexander, H.M. 1992. Evolution of resistance and virulence in plant-herbivore and plant-pathogen interactions. Trends Ecol. Evol. 6:290–293.
Mauricio, R. and Rausher, M. D. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defenses. Evolution 51:1435–1444.
May, R. M. and Anderson, R. M. 1990. Parasite-host coevolution. Parasitology Suppl. 100:89–101.
Osbourn, A. E. 1999. Antimicrobial phytoprotectants and fungal pathogens—a commentary. Fung. Gen. Biol. 26:163–168.
Pratt, D. E. and Miller, E. E. 1984. A flavonoid antioxidant in Spanish peanut (Arachia hypogoea). J. Am. Oil Chem. Soc. 61:1064–1067.
Rausher, M. D. 1992. Natural Selection and the Evolution of Plant–Insect Interactions. Chapman and Hall, New York.
Rice, R. L., Lincoln, D. E., and Langenheim, J. H. 1978. Palatability of monoterpenoid compositional types of Satureja douglasii to a generalist molluscan herbivore, Ariolimax dolichophallus. Biochem. Syst. Ecol. 6:45–53.
Rosenthal, G. A. and Berenbaum, M. R. (eds.). 1992. Herbivores: Their Interactions with Secondary Plant Metabolites, 2nd ed. Academic Press, New York.
Shafizadeh, F. and Melnikoff, A. B. 1970. Coumarins of Artemisia tridentata ssp. vaseyana. Phytochemistry 9:1311–1316.
Shafizadeh, F., Bhadane, N. R., Morris, M. S., Kelsey, R. G., and Khanna, S. N. 1971. Sesquiterpene lactones of big sagebrush. Phytochemistry 10:2745–2754.
Sicker, D., Frey, M., Schulz, M., and Gierl, A. 2000. Role of natural benzoxazinones in the survival strategy of plants. Int. Rev. Cytol. 198:319–346.
Simms, E. L. 1996. The evolutionary genetics of plant pathogen systems. Bioscience 46:136–145.
Slone, J. H. and Kelsey, R. G. 1985. Isolation and purification of glandular secretory cells from Artemisia tridentata (ssp. vaseyana) by percoll density gradient centrifugation. Am. J. Bot. 72:1445–1451.
Talley, S. M. 2001. The evolution of anti-fungal metabolites among sagebrush from habitats that differ in fungal prevalence. PhD dissertation. University of Utah, Salt Lake City, Utah. 2168 TALLEY, COLEY, AND KURSAR
Talley, S. M., Coley, P. D., and Kursar, T. A. 2002. The effects of weather on fungal abundance and richness among twenty-five communities in the IntermountainWest. BioMed Central Ecology 2:7.
Tucker, S. L. and Talbot, N. J. 2001. Surface attachment and pre-penetration stage development by plant-pathogenic fungi. Annu. Rev. Phytopathol. 39:385–417.
Van Etten, H. D., Mansfield, J. W., Bailey, J. A., and Farmer, E. E. 1994. Two classes of plant antibiotics—phytoalexins versus phytoanticipins. Plant Cell 6:1191–1192.
Weber, D. J., Hess, W. M., Gul, B., Khan, M. A., and Clair, S. S. 2000. Halophytic fungi from an inland salt playa of the Great Basin. Am. J. Bot. Suppl. 87:56.
Welch, B. L. and Nelson, D. L. 1995. Black stem rust reduces big sagebrush seed production. J. Range Manage. 48:398–401.
Werker, E. 2000. Trichome diversity and development. Adv. Bot. Res. Inc. Adv. Plant Pathol. 31:1–35.
Wilkerson, L. 1988. SYSTAT: The System for Statistics. SYSTAT Inc., Evanston, Illinois.
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Talley, S.M., Coley, P.D. & Kursar, T.A. Antifungal Leaf-Surface Metabolites Correlate with Fungal Abundance in Sagebrush Populations. J Chem Ecol 28, 2141–2168 (2002). https://doi.org/10.1023/A:1021037029684
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DOI: https://doi.org/10.1023/A:1021037029684