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Costs of glucosinolates in Brassica rapa: Are they context dependent?

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DOI: 10.4236/oje.2013.32022    3,758 Downloads   6,636 Views   Citations

ABSTRACT

Models predicting optimal levels of plant defense against herbivores typically include two assumptions: 1) defense is both beneficial and costly; and 2) the relationship between costs and benefits of a defense is consistent across environments. However, the expression of costs and benefits of defense may be environmentally dependent. We examined lines of Brassica rapa, previously divergently selected for the defensive trait foliar glucosinolate content. In one set of experiments (Experiment #1), plants were grown in herbivore-free and herbivore-present environments to investigate the costs and benefits of this defense. In a second set of experiments (Experiment #2), plants were grown at two nutrient levels and two temperatures to examine the environmental context of costs of defense. In Experiment #1, increased levels of damage resulted in decreased flower production and plants from high glucosinolate lines received less damage than those from low glucosinolate lines, suggesting a benefit of this defense. In this experiment no cost of defense was detected. In Experiment #2, nutrients had a significant positive effect on flower production at 23°C, but not at 32°C. No significant effects of glucosinolate line nor interaction between nutrient environment and glucosinolate line were detected at 23°C, suggesting that no cost of defense occurred at this lower temperature. Similarly, no significant nutrient environment by glucosenolate line interaction was detected at 32°C. However, a significant effect of glucosinolate line was observed suggesting that at 32°C costs were incurred, but nutrient environment had no mitigating effect. While results from Experiment #1 suggested that defense was beneficial, but not costly, results from Experiment #2 suggested that costs of defense were temperature dependent. For species occupying broad geographic ranges, these findings of temperature-dependent costs are especially insightful with regard to the evolution of defense because differing geographic populations are likely to experience differing temperature environments.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Stowe, K. , Hochwender, C. , Fleck, K. , Duvall, N. , Lewkiewicz, D. , Trimble, S. and Peters, S. (2013) Costs of glucosinolates in Brassica rapa: Are they context dependent?. Open Journal of Ecology, 3, 185-195. doi: 10.4236/oje.2013.32022.

References

[1] Marquis, R.J. (1984) Leaf herbivores decrease fitness of a tropical plant. Science, 226, 537-539. doi:10.1126/science.226.4674.537
[2] Marquis, R.J. (1992) The selective impact of herbivores. In: Fritz, R.S. and Simms, E.L., Eds., Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics, The University of Chicago Press, Chicago, 310-325.
[3] Fritz, R.S., Hochwender, C.G., Lewkiewicz, D.A., Bothwells, S. and Orians, C.M. (2001) Seedling herbivory by slugs in a willow hybrid system: Developmental changes in damage, chemical defense, and plant performance. Oecologia, 129, 87-97. doi:10.1007/s004420100703
[4] Hochwender, C.G., Sork, V.L. and Marquis, R.J. (2003) Fitness consequences of herbivory on Quercus alba. American Midland Naturalist, 150, 246-253. doi:10.1674/0003-0031(2003)150[0246:FCOHOQ]2.0.CO;2
[5] Kettenring, K.M., Weekley, C.W. and Menges, E.S. (2009) Herbivory delays flowering time and reduces fecundity of Liatris ohlingerae (Asteraceae), an endangered, endemic plant of the Florida scrub. The Journal of the Torrey Botanical Society, 136, 350-362. doi:10.3159/08-RA-113.1
[6] Paige, K.N. and Whitham, T.G. (1987) Overcompensation in response to mammalian herbivory: The advantage of being eaten. The American Naturalist, 129, 407-416. doi:10.1086/284645
[7] Becklin, K.M. and Kirkpatrick, H.E. (2006) Compensation through rosette formation: The response of scarlet gilia (Ipomosis aggregate: Polemoniaceae) to mammalian herbivory. Canadian Journal of Botany, 84, 1298-1303. doi:10.1139/b06-099
[8] Huttunen, L., Miemela, P., Peltola, H., Heiska, S., Rousi, M. and Kellom?ki, S. (2007) Is a defoliated silver birch seedling able to overcompensate the growth under changing climate? Environmental and Experimental Botany, 60, 227-238. doi:10.1016/j.envexpbot.2006.10.010
[9] Simms, E.L. and Rausher, M.D. (1987) Costs and benefits of plant defense to herbivory. The American Naturalist, 130, 570-581. doi:10.1086/284731
[10] Simms, E.L. and Rausher, M.D. (1989) The evolution of resistance to herbivory in Ipomoea purpurea II. Natural selection by insects and cost of defense. Evolution, 43, 575-585. doi:10.2307/2409060
[11] Herms, D.A. and Mattson, W.J. (1992) The dilemma of plants: To grow or defend. Quarterly Review of Biology, 67, 283-335. doi:10.1086/417659
[12] Simms, E.L. (1992) Costs of plant resistance to herbivory. In: Fritz, R.S. and Simms, E.L., Eds., Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics, The University of Chicago Press, Chicago, 392-425.
[13] Stowe, K.A. and Marquis, R.J. (2011) Costs of Defense: Correlated responses to divergent selection for foliar glucosinolate content in Brassica rapa. Ecology and Evolution, 25, 763-775. doi:10.1007/s10682-010-9443-9
[14] Chew, F.S. and Renwick J.A.A. (1994) Host plant choice in Pieris butterflies. In: Carde, R.T. and Bell, W.B., Eds., Chemical Ecology of Insects II, Chapman and Hall, New York, 214-238.
[15] Huang, X., Renwick, J.A.A., and Chew, F. (1995) Oviposition stimulants and deterrents control acceptance of Alliaria petiole by Pieris rapae and P. napi oleracea. Chemoecology, 6, 79-87. doi:10.1007/BF01259436
[16] Siemens, D.H. and Mitchell-Olds, T. (1996) Glucosinolates and herbivory by specialists (Coleoptera: Chrysomelidae. Lepidoptera: Plutellidae): Consequences of concentration and induced resistance. Environmental Entomology, 25, 1344-1353.
[17] Stowe, K.A. (1998) Realized defense of artificially selected line of Brassica rapa: Effects of quantitative genetic variation in foliar glucosinolate content. Environmental Entomology, 27, 1166-1174.
[18] Bergelson, J. and Purrington, C.B. (1996) Surveying patterns in the cost of resistance in plants. The American Naturalist, 14, 536-558. doi:10.1086/285938
[19] Purrington, C.B. (2000) Costs of resistance. Current Opinion in Plant Biology, 3, 305-308. doi:10.1016/S1369-5266(00)00085-6
[20] Korchieva, J. (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defense. Ecology, 83, 176-190. doi:10.1890/0012-9658(2002)083[0176:MAOSOV]2.0.CO;2
[21] Stevens, M.T., Waller, D.M. and Lindroth, R.L. (2007) Resistance and tolerance in Populus tremuloides: Genetic variation, costs, and environmental dependency. Ecology and Evolution, 21, 829-847. doi:10.1007/s10682-006-9154-4
[22] Coley, P.D., Bryant, J.P. and Chapin III, F.S. (1985) Resource availability and plant antiherbivore defense. Science, 230, 895-899. doi:10.1126/science.230.4728.895
[23] Asare, E. and Scarisbrick, D.H. (1995) Rate of nitrogen and sulphur fertilizers on yield, yield components and seed quality of oilseed rape (Brassica napus L.). Field Crop Research, 44, 41-46. doi:10.1016/0378-4290(95)00051-7
[24] Marak, H.B., Biere, A. and van Damme, J.M.M. (2003) Fitness costs of chemical defense in Plantago lanceolata L.: Effects of nutrient and competition stress. Evolution, 57, 2519-2530.
[25] Donaldson, J.R. and Lindroth, R.L. (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology, 88, 729-739. doi:10.1890/06-0064
[26] Hendriks, R.J.J., Luijten, L. and van Groenendael, J.M. (2009) Context-dependent defence in terrestrial plants: The effects of light and nutrient availability on plant resistance against herbivory. Entomologia Experimentalis et Applicata, 131, 233-242. doi:10.1111/j.1570-7458.2009.00852.x
[27] Hirata, K., Asada, M., Yarani, E., Miyamoto, K. and Miura, Y. (1993) Affects of near-ultraviolet light on alkaloid production in Catharanthus roseues plants. Planta Medica, 59, 46-50.
[28] Dixon, R.A. and Paiva, N.L. (1995) Stress-induced phenylpropanoid metabolism. Plant Cell, 7, 1085-1097.
[29] Haugen, R., Steffes, L., Wolf, J., Brown, P., Matzner, S. and Siemens, D.H. (2008) Evolution of drought tolerance and defense: Dependence of tradeoffs on mechanism, environment and defense switching. Oikos, 117, 231-244. doi:10.1111/j.2007.0030-1299.16111.x
[30] Ramirez, C.C. and Verdugo, J.A. (2009) Water availability affects tolerance and resistance to aphids but not the trade-off between the two. Ecological Research, 24, 881- 888. doi:10.1007/s11284-008-0565-2
[31] Siemens, D.H., Garner, S.H. and Mitchell-Olds, T. (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology, 83, 505-517.
[32] Gershenzon, J. (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress. Recent Advances in Phytochemistry, 18, 273-320.
[33] Hare, J.D., Elle, E. and van Dam N.M. (2003) Costs of glandular trichomes in Datura wrightii: A three year study. Evolution, 57, 793-805.
[34] Hare, J.D. and Elle, E. (2004) Survival and seed production of sticky and velvety Datura wrightii in the field: A five year study. Ecology, 85, 615-622. doi:10.1890/03-3069
[35] Francescangeli, N., Sangiacomo, M.A. and Marti, H.R. (2007) Vegetative and reproductive plasticity of broccoli at three levels of incident photosynthetically active radiation. Spanish Journal of Agricultural Research, 5, 389- 401.
[36] Zhang, H., Schonhof, I., Krumbein, A., Gutezeit, B., Li, L., Stützel, H. and Schreiner, M. (2008) Water supply and growing season influence glucosinolate concentration and composition in turnip root (Brassica rapa ssp. Rapifera L.). Journal of Plant Nutrition and Soil Science, 171, 255-265. doi:10.1002/jpln.200700079
[37] Qaderi, M.M., Kurepin, L.V. and Reid, D.M. (2006) Growth and physiological responses of canola (Brassica napus) to three components of global climate change: Temperature, carbon dioxide and drought. Physiologia Plantarum, 128, 710-721. doi:10.1111/j.1399-3054.2006.00804.x
[38] Lincoln, D.E. and Langenheim, J.H. (1978) Effect of light and temperature on monoterpenoid yield and composition. Biochemical Systematics and Ecology, 6, 21-32. doi:10.1016/0305-1978(78)90021-2
[39] Plowman, A.B. and Richards, A.J. (1997) The effect of light and temperature on competition between atrzine susceptible and resistant Brassica rapa. Annals of Botany, 80, 583-590. doi:10.1006/anbo.1997.0496
[40] Schonhof, I., Blaring, H.-P., Krumbein, A., Clau?en, W. and Schreiner, W. (2007) Effect of temperature increase under low radiation conditions on phytochemicals and ascorbic acid in greenhouse grown broccoli. Agriculture, Ecosystems, and Environment, 119, 103-111. doi:10.1016/j.agee.2006.06.018
[41] Jahangir, M., Abdel-Farid, I.B., Kim, H.K., Choi, Y.H. and Verpoorte, R. (2009) Healthy and unhealthy plants: The effects of stress on the metabolism of Brassicaceae. Environmental and Experimental Botany, 67, 23-33. doi:10.1016/j.envexpbot.2009.06.007
[42] Grubb, C.D. and Abel, S. (2006) Glucosinolate metabolism and its control. Trends in Plant Science, 11, 89-100. doi:10.1016/j.tplants.2005.12.006
[43] Salisbury, F.B. and Ross, C.W. (1985) Plant physiology. Wadsworth Publishing Co., Belmont.
[44] Louda, S.M. and Mole, S. (1991) Glucosinolates: Chemistry and ecology. In: Rosenthal, G.A. and Berenbaum, M.R., Eds., Herbivores, Their Interactions with Secondary Plant Metabolites, Academic Press, San Diego, 123- 163. doi:10.1016/B978-0-12-597183-6.50009-7
[45] Louda, S.M. (1987) Variation in methylglucosinolate and insect damage to Cleome serrulata (Capparaceae) along a natural soil moisture gradient. Journal of Chemical Ecology, 1, 569-581. doi:10.1016/B978-0-12-597183-6.50009-7
[46] Mauricio, R., Rausher, M.D. and Burdick, D.S. (1997) Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive? Ecology, 78, 1301-1311. doi:10.1890/0012-9658(1997)078[1301:VITDSO]2.0.CO;2
[47] Van Dam, N.M., Tygat, T.O.G. and Kirkland, J.A. (2009) Root and shoot glucosinolates: A comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochemistry Reviews, 8, 171-186. doi:10.1007/s11101-008-9101-9
[48] Steyermark, J.A. (1963) Flora of Missouri. The Iowa State University Press, Ames.
[49] USDA, NRCS (2010) PLANTS Profile: Brassica rapa L. http://plants.usda.gov/java/profile?symbol=BRRA
[50] United States Census Bureau. (2006) Daily mean temperature. http://www.allcountries.org/uscensus/408_normal_daily_mean_temperature_selected_cities.html
[51] Williams, P.H. and Hill, C.B. (1986) Rapid-cycling populations of Brassica. Science, 232, 1385-1389. doi:10.1126/science.232.4756.1385
[52] Borror, D.J., Triplehorn, C.A. and Johnson, N.F. (1989) An introduction to the study of insects. Saunders, Philadelphia.
[53] Shorey, H.H. and Hale, R.L. (1965) Mass-rearing of the larvae of nine Noctuid species on a simple artificial medium. Journal of Economic Entomology, 58, 522-524.
[54] Conner, J.K., Rush, S. and Jennetten, P. (1996) Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). I. Selection through lifetime female fitness. Evolution, 50, 1127-1136. doi:10.2307/2410653
[55] Strauss, S., Conner, J.K. and Rush, S.L. (1996) Foliar herbivory affects floral characters and plant attractiveness to pollinators: Implications for male and female fitness. The American Naturalist, 147, 1098-1107. doi:10.1086/285896
[56] Strauss, S.Y., Siemens, D.H., Decher, M.B. and Mitchell-Olds, T. (1999) Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution, 53, 1105-1113. doi:10.2307/2640815
[57] Strauss, S., Rudgers, J.A., Lau, J.A. and Irwin, R.E. (2002) Direct costs of resistance to herbivory. Trends in Ecology and Evolution, 17, 278-285. doi:10.1016/S0169-5347(02)02483-7
[58] JMP Version 5 (2005) SAS Institute Inc., Cary.
[59] Cipollini, D.F. (2002) Variation in the expression of chemical defenses in Alliaria petiole (Brassicaeae) in the field and common garden. American Journal of Botany, 89, 1422-1430. doi:10.3732/ajb.89.9.1422
[60] Cipollini, D.F., Busch, J.W., Stowe, K.A., Simms, E.L. and Bergelson, J. (2003) Genetic variation and relationships of constitutive and herbivore-induced glucosinolates, trypsin inhibitors, and herbivore resistance in Brassica rapa. Journal of Chemical Ecology, 29, 285-302. doi:10.1023/A:1022673726325
[61] Stowe, K.A. (1998) Experimental evolution of resistance in Brassica rapa: Correlated response of tolerance in lines selected for glucosinolate content. Evolution, 52, 703-712. doi:10.2307/2411265
[62] Simms, E.L. and Triplett, J. (1994) Costs and benefits of plant responses to disease: Resistance and tolerance. Evolution, 48, 1973-1985. doi:10.2307/2410521
[63] Lankau, R.A. and Strauss, S.Y. (2008) Community complexity drives patterns of natural selection on a chemical defense of Brassica rapa. The American Naturalist, 171, 150-161. doi:10.1086/524959
[64] Cipollini, D.F. and Bergelson, J. (2002) Interspecific competition affects growth and herbivore damage of Brassica napus in the field. Plant Ecology, 162, 227-231. doi:10.1023/A:1020377627529
[65] Glawe, G.A., Zavala, J.A., Kessler, A., van Dam, N.M. and Baldwin, I.T. (2003) Ecological costs and benefits correlated with trypsin inhibitor production in Nicotiana attentuata. Ecology, 84, 79-90. doi:10.1890/0012-9658(2003)084[0079:ECABCW]2.0.CO;2
[66] Nu?ez-Faran, J., Fornoni, J. and Valverde, P.L. (2007) The evolution of resistance and tolerance to herbivores. Annual Review of Ecology, Evolution, and Systematics, 38, 541-566. doi:10.1146/annurev.ecolsys.38.091206.095822
[67] Agren, J. and Schemske, D.W. (1993) The cost of defense against herbivores: An experimental study of trichome production in Brassica rapa. The American Naturalist, 141, 338-350. doi:10.1086/285477
[68] Agren, J. and Schemske, D.W. (1994) Evolution of trichome number in a naturalized population of Brassica rapa. The American Naturalist, 143, 1-13. doi:10.1086/285593
[69] Windle, P.N. and Franz, E.H. (1979) The effects of insect parasitism on plant competition: Greenbugs and barley. Ecology, 60, 521-529. doi:10.2307/1936072
[70] Cheplick, G.P., Clay, K. and Marks, S. (1989) Interactions between infection by endophytic fungi and nutrient limitation in grasses Lolium perenne and Festuca arundinaceae. New Phytologist, 111, 89-97. doi:10.1111/j.1469-8137.1989.tb04222.x
[71] Rousi, M. (1988) Resistance breeding against voles in birch: Possibilities for increasing resistance by provenance transfers. European and Mediterranean Plant Protection Organization Bulletin, 18, 257-263.
[72] Rousi, M. (1989) Susceptibility of winter-dormant Pinus sylvestris families to vole damage. Scandinavian Journal of Forest Research, 4, 149-161. doi:10.1080/02827588909382554
[73] Sagers, C.L. and Coley, P.D. (1995) Benefits and costs of defense in a neotropical shrub. Ecology, 76, 1835-1843. doi:10.2307/1940715
[74] Preisser, E.L., Gibson, S.E., Adler, L.S. and Lewis, E.E. (2007) Underground herbivory and the cost of constitutive defense in tobacco. International Journal of Ecology, 31, 210-215.
[75] Ivey, C.T., Carr, D.E. and Eubanks, M.D. (2009) Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus. Heredity, 10, 303-311. doi:10.1038/hdy.2008.122
[76] McKenzie, J.A., Whitten, M.J., and Adena, M.A. (1982) The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity, 49, 1-9. doi:10.1038/hdy.1982.60
[77] McKenzie, J.A. and Purvis, A. (1984) Chromosomal localization of fitness modifiers of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity, 53, 625-634. doi:10.1038/hdy.1984.120
[78] Lenski, R.E. (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution, 42, 425-432. doi:10.2307/2409028
[79] Lenski, R.E. (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. II. Compensation for maladaptive effects associated with resistance to virus T4. Evolution, 42, 433-440. doi:10.2307/2409029
[80] Bezemer, T.M., Jones, T.H. and Newington, J.E. (2000) Effect of carbon dioxide and nutrient fertilization on phenolic content in Poa annua L. Biochemical Systematics and Ecology, 28, 839-846. doi:10.1016/S0305-1978(99)00130-1
[81] Coviella, C.E., Stipanovic, R.D. and Trumble, J.T. (2002) Plant allocation to defensive compounds: Interactions between elevated CO2 and nitrogen in transgenic cotton plants. Journal of Experimental Botany, 53, 323-331. doi:10.1093/jexbot/53.367.323
[82] Prudic, K.L., Oliver, J.C. and Bowers, D.M. (2005) Soil nutrient effects on ovipositon preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia, 143, 578-587. doi:10.1007/s00442-005-0008-5
[83] Kliebenstein, D.J., Kroymann, J. and Mitchell-Olds, T. (2005) The glucosinolate-myrosinase system in an ecological and evolutionary context. Current Opinion in Plant Biology, 8, 263-271. doi:10.1016/j.pbi.2005.03.002
[84] Campbell, N.A. and Reece, J.B. (2005) Biology. Benjamin Cummings, San Francisco.
[85] Agerbirk, N., Olsen, C.E. and Neilsen, J.K. (2001) Seasonal variation in leaf glucosinolate and insect resistance in two types of Barbarea vulgaris spp. arcuata. Phytochemistry, 58, 91-100. doi:10.1016/S0031-9422(01)00151-0
[86] Gols, R., Raaijmakers, C.E., van Dam, N.M., Dicke, M., Bukovinsky, T. and Harvey, J.A. (2007). Temporal changes affect plant chemistry and tritrophic interactions. Basic and Applied Ecology, 8, 421-433. doi:10.1016/j.baae.2006.09.005

  
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