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Glucosinolates and Their Hydrolysis Products in Arabidopsis thaliana Influence Performance and Feeding Choice of Pieris rapae and Spodoptera exigua

DOI: 10.4236/ae.2023.114020, PP. 285-299

Keywords: Arabidopsis thaliana, Glucosinolates, Hydrolysis Products, Specialist and Generalist Insects

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Abstract:

Glucosinolates and their hydrolysis products, found in plants of the order Brassicales, are well-known for their defensive properties against insect herbivores. Arabidopsis thaliana (Col-0) genetic lines with mutations that modify the type of glucosinolates (i.e. myb28myb29 and cyp79B2cyp79B3 are deficient in the production of aliphatic and indolyl glucosinolates, respectively) make it possible to test for the specific effects of these secondary chemicals on insect herbivores. The Pad3 mutant (deficient in camalexin), which has a role in resistance to pathogens, was also tested. Likewise, the effects of different glucosinolate hydrolysis products can be evaluated using genetically modified (GM) lines of the wild type Col-0 ecotype, which naturally produces isothiocyanates. These GM lines include the nitrile-producing 35S: ESP and the double knockout tgg1tgg2, which virtually lacks hydrolysis products. In both no-choice and choice experiments, the crucifer specialist Pieris rapae was virtually unaffected by differences in the type of glucosinolates or hydrolysis products. In contrast, the generalist insect Spodoptera exigua had statistically significant increases in pupae/adult weight and faster developmental times when reared on mutants deficient in the production of aliphatic and indolyl glucosinolates and their hydrolysis products. There were no differences in the performance of either insect species when reared on wild type Col-0 or Pad3. Results from feeding choice trials showed that Pieris rapae had no statistically significant preference for any of the genetic lines. In contrast, Spodoptera exigua had a significant feeding preference for the double mutant tgg1tgg2. This study provides evidence that variation in the type of glucosinolates and their hydrolysis products can influence insect performance and feeding choices, and that responses are species-specific.

References

[1]  Schoonhoven, L.M., Jermey, T. and van Loon, J.J.A. (1998) Insect-Plant Biology: From Physiology to Evolution. Chapman and Hall, London.
https://doi.org/10.1007/978-1-4899-3200-6
[2]  Ehrlich, P.R. and Raven, P.H. (1964) Butterflies and Plants: A Study in Coevolution. Evolution, 18, 586-608.
https://doi.org/10.2307/2406212
[3]  Bruce, T.J.A. (2015) Interplay between Insects and Plants: Dynamic and Complex Interactions That Have Coevolved over Millions of Years but Act in Milliseconds. Journal of Experimental Botany, 66, 455-465.
https://doi.org/10.1093/jxb/eru391
[4]  Wittstock, U. and Gershenzon, J. (2002) Constitutive Plant Toxins and Their Role in Defense against Herbivores and Pathogens. Current Opinion in Plant Biology, 5, 300-307.
https://doi.org/10.1016/S1369-5266(02)00264-9
[5]  Hopkins, R.J., van Dam, N.M. and van Loon, J.J.A. (2009) Role of Glucosinolates in Insect-Plant Relationships and Multi-Trophic Interactions. Annual Review of Entomology, 54, 57-83.
https://doi.org/10.1146/annurev.ento.54.110807.090623
[6]  Wittstock, U., Kliebenstein, D.J., Lambrix, V., Reichelt, M. and Gershenzon, J. (2003) Glucosinolate Hydrolysis and Its Impact on Generalist and Specialist Insect Herbivores. In: Romeo, J.T., Ed., Integrative Phytochemistry: From Ethnobotany to Molecular Ecology, Elsevier, Amsterdam, 101-126.
https://doi.org/10.1016/S0079-9920(03)80020-5
[7]  Ali, J.G. and Agrawal, A.A. (2012) Specialist versus Generalist Insect Herbivores and Plant Defense. Trends in Plant Science, 17, 293-302.
https://doi.org/10.1016/j.tplants.2012.02.006
[8]  Li, Q., Eigenbrode, S.D., Stringam, G.R. and Thiagarajah, M.R. (2000) Feeding and Growth of Plutella xylostella and Spodoptera juncea with Varying Glucosinolate Concentrations and Myrosinase Activities. Journal of Chemical Ecology, 26, 2401-2419.
https://doi.org/10.1023/A:1005535129399
[9]  Arany, M., de Jong, T.J., Kim, H.K., van Dam, N.M., Choi, Y.H., Verpoorte, R. and van der Meijden, E. (2008) Glucosinolates and Other Metabolites in the Leaves of Arabidopsis thaliana from Natural Populations and Their Effects on a Generalist and a Specialist Herbivore. Chemoecology, 18, 65-71.
https://doi.org/10.1007/s00049-007-0394-8
[10]  Wu, G., Guo, J.Y., Wan, F.H. and Xiao, N.W. (2010) Responses of Three Successive Generations of Beet Armyworm, Spodoptera exigua, Fed Exclusively on Different Levels of Gossypol in Cotton Leaves. Journal of Insect Science, 10, Article 165.
https://doi.org/10.1673/031.010.14125
[11]  Krieger, R.I., Feeny, P.P. and Wilkinson, C.F. (1971) Detoxication Enzymes in the Guts of Caterpillars: An Evolutionary Answer to Plant Defenses? Science, 172, 579-580.
https://doi.org/10.1126/science.172.3983.579
[12]  Ratza, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T. and Kroymann, J. (2002) Disarming the Mustard Oil Bomb. Proceedings of the National Academy of Sciences of the United States of America, 99, 11223-11228.
https://doi.org/10.1073/pnas.172112899
[13]  Agrawal, A.A. and Kurashige, N.S. (2003) A Role for Isothiocyanates in Plant Resistance against the Specialist Herbivore Pieris rapae. Journal of Chemical Ecology, 29, 1403-1415.
https://doi.org/10.1023/A:1024265420375
[14]  Wittstock, U., Agerbirk, N., Stauber, E.J., Olsen, C.E., Hippler, M., Mitchell-Olds, T., Gershenzon, J. and Vogel, H. (2004) Successful Herbivore Attack Due to Metabolic Diversion of a Plant Chemical Defense. Proceedings of the National Academy of Sciences of the United States of America, 101, 4859-1536.
https://doi.org/10.1073/pnas.0308007101
[15]  Agrawal, A.A. (2000) Specificity of Induced Resistance in Wild Radish: Causes and Consequences for Two Specialist and Two Generalist Caterpillars. Oikos, 89, 493-500.
https://doi.org/10.1034/j.1600-0706.2000.890308.x
[16]  Van Dam, N.M., Hadwich, K. and Baldwin, I.T. (2000) Induced Responses in Nicotiana Attenuate Affect Behavior and Growth of the Specialist Herbivore Manduca sexta. Oecologia, 122, 371-379.
https://doi.org/10.1007/s004420050043
[17]  Bidart-Bouzat, M.G. and Kliebenstein, D. (2011) An Ecological Genomic Approach Challenging the Paradigm of Differential Plant Responses to Specialist versus Generalist Insect Herbivores. Oecologia, 167, 677-689.
https://doi.org/10.1007/s00442-011-2015-z
[18]  Onkokesung, N., Reichelt, M., van Doorn, A., Schuurink, R.C., van Loon, J.J.A. and Dicke, M. (2014) Modulation of Flavonoid Metabolites in Arabidopsis thaliana through Overexpression of the MYB75 Transcription Factor: Role of Kaempferol-3,7-Dirhamnoside in Resistance to the Specialist Insect Herbivore Pieris brassicae. Journal of Experimental Botany, 65, 2203-2217.
https://doi.org/10.1093/jxb/eru096
[19]  Richards, L.A., Glassmire, A.E., Ochsenrider, K.M., Smilanich, A.M., Dodson, C.D., Jeffrey, C.S. and Dyer, L.A. (2016) Phytochemical Diversity and Synergistic Effects on Herbivores. Phytochemistry Reviews, 15, 1153-1166.
https://doi.org/10.1007/s11101-016-9479-8
[20]  Cornell, H. and Hawkins, B. (2003) Herbivore Responses to Plant Secondary Compounds: A Test of Phytochemical Coevolution Theory. American Naturalist, 161, 507-522.
https://doi.org/10.1086/368346
[21]  Volf, M., Hrcek, J., Julkunen-Tiitto, R. and Novotny, V. (2015) To Each Its Own: Differential Response of Specialist and Generalist Herbivores to Plant Defence in Willows. Journal of Animal Ecology, 84, 1123-1132.
https://doi.org/10.1111/1365-2656.12349
[22]  Fahey, J.W., Zalcmann, A.T. and Talalay, P. (2001) The Chemical Diversity and Distribution of Glucosinolates and Isothiocyanates among Plants. Phytochemistry, 56, 5-51.
https://doi.org/10.1016/S0031-9422(00)00316-2
[23]  Halkier, B.A. and Gershenzon, J. (2006) Biology and Biochemistry of Glucosinolates. Annual Review of Plant Biology, 57, 303-333.
https://doi.org/10.1146/annurev.arplant.57.032905.105228
[24]  Barth, C. and Jander, G. (2006) Arabidopsis Myrosinases TGG1 and TGG2 Have Redundant Function in Glucosinolate Breakdown and Insect Defense. Plant Journal, 46, 549-562.
https://doi.org/10.1111/j.1365-313X.2006.02716.x
[25]  Bidart-Bouzat, M.G. and Kliebenstein, D. (2008) Differential Levels of Insect Herbivory in the Field Associated with Genotypic Variation in Glucosinolates in Arabidopsis thaliana. Journal of Chemical Ecology, 34, 1026-1037.
https://doi.org/10.1007/s10886-008-9498-z
[26]  Ikeura, H., Kobayashi, F. and Hayata, Y. (2010) How do Pieris rapae Search for Host Plants? Biochemical Systematics and Ecology, 38, 1199-1203.
https://doi.org/10.1016/j.bse.2010.12.007
[27]  Van der Meijden, E. (1996) Plant Defence, an Evolutionary Dilemma: Contrasting Effects of (Specialist and Generalist) Herbivores and Natural Enemies. Entomologia Experimentalis et Applicata, 80, 307-310.
https://doi.org/10.1111/j.1570-7458.1996.tb00941.x
[28]  Burow, M., Müller, R., Gershenzon, J. and Wittstock, U. (2006) Altered Glucosinolate Hydrolysis in Genetically Engineered Arabidopsis thaliana and Its Influence on the Larval Development of Spodoptera littoralis. Journal of Chemical Ecology, 32, 2333-2349.
https://doi.org/10.1007/s10886-006-9149-1
[29]  Robin, A.H., Hossain, M.R., Park, J.-I., Kim, H.R. and Nou, I.-S. (2017) Glucosinolate Profiles in Cabbage Genotypes Influence the Preferential Feeding of Diamondback Moth (Plutella xylostella). Frontiers in Plant Science, 8, Article 1244.
https://doi.org/10.3389/fpls.2017.01244
[30]  Ishida, M., Hara, M., Fukino, N., Kakizaki, T. and Morimitsu, Y. (2014) Glucosinolate Metabolism, Functionality and Breeding for the Improvement of Brassicaceae Vegetables. Breeding Science, 64, 48-59.
https://doi.org/10.1270/jsbbs.64.48
[31]  Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pederson, D., Gershenzon, J. and Mitchell-Olds, T. (2001) Genetic Control of Natural Variation in Arabidopsis Glucosinolate Accumulation. Plant Physiology, 126, 811-825.
https://doi.org/10.1104/pp.126.2.811
[32]  Wittstock, U. and Burow, M. (2010) Glucosinolate Breakdown in Arabidopsis: Mechanism, Regulation and Biological Significance. Arabidopsis Book, 8, e0134.
https://doi.org/10.1199/tab.0134
[33]  Müller, R., de Vos, M., Sun, J., Sønderby, I.E., Halkier, B.A., Wittstock, U. and Jander, G. (2010) Differential Effects of Indole and Aliphatic Glucosinolates on Lepidopteran Herbivores. Journal of Chemical Ecology, 36, 905-913.
https://doi.org/10.1007/s10886-010-9825-z
[34]  Zhou, N., Tootle, T.L. and Glazebrook, J. (1999) Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase. Plant Cell, 11, 2419-2428.
https://doi.org/10.1105/tpc.11.12.2419
[35]  Burow, M., Markert, J., Gershenzon, J. and Wittstock, U. (2006) Comparative Biochemical Characterization of Nitrile-Forming Proteins from Plants and Insects That Alter Myrosinase Catalyzed Hydrolysis of Glucosinolates. FEBS Journal, 273, 2432-2446.
https://doi.org/10.1111/j.1742-4658.2006.05252.x
[36]  Zhao, Y., Hull, A.K., Gupta, N., Goss, K.A., Alonso, J., Eckler, J.R., Normanly, J., Chory, J. and Celenza, J.L. (2002) Trp-Dependent Auxin Biosynthesis in Arabidopsis: Involvement of Cytochrome P450s CYP79B2 and CYP79B3. Genes & Development, 16, 3100-3112.
https://doi.org/10.1101/gad.1035402
[37]  Beekwilder, J., van Leeuwen, W., van Dam, N.M., Bertossi, M., Grandi, V., Mizzi, L., Soloviev, M., Szabados, L., Molthoff, J.W., Schipper, B., Verbocht, H., de Vos, R.C.H., Morandini, P., Aarts, M.G.M. and Bovy, A. (2008) The Impact of the Absence of Aliphatic Glucosinolates on Insect Herbivory in Arabidopsis. PLOS ONE, 3, e2068.
https://doi.org/10.1371/journal.pone.0002068
[38]  Tingle, F.C. and Mitchell, E.R. (1977) Seasonal Populations of Armyworms and Loopers at Hastings, Florida. Florida Entomologist, 60, 115-122.
https://doi.org/10.2307/3494389
[39]  Zheng, S., Zhang, P., van Loon, J.J.A. and Dicke, M. (2011) Silencing Defense Pathways in Arabidopsis by Heterologous Gene Sequences from Brassica oleracea Enhances the Performance of a Specialist and a Generalist Herbivorous Insect. Journal of Chemical Ecology, 37, 818-829.
https://doi.org/10.1007/s10886-011-9984-6
[40]  Wilson, J.W. (1934) The Asparagus Caterpillar: It’s Life History and Control. Florida Agricultural Experiment Station Bulletin, 271, 1-26.
[41]  Scudder, S.H. (1887) The Introduction and Spread of Pieris rapae in North America, 1860-1886. Memoirs of the Boston Society of Natural History, 4, 53-69.
https://doi.org/10.5962/bhl.title.38374
[42]  Richards, O.W. (1940) The Biology of the Small White Butterfly (Pieris rapae), with Special Reference to the Factors Controlling Its Abundance. Journal of Animal Ecology, 9, 243-288.
https://doi.org/10.2307/1459
[43]  Tang, Z.H., Gong, K.Y. and You, Z.P. (1988) Present Status and Countermeasures of Insecticide Resistance in Agricultural Pests in China. Pesticide Science, 23, 189-198.
https://doi.org/10.1002/ps.2780230212
[44]  Zhou, C., Liu, Y., Yu, W., Deng, Z., Gao, M., Liu, F. and Mu, W. (2011) Resistance of Spodoptera exigua to Ten Insecticides in Shandong, China. Phytoparasitica, 39, 315-324.
https://doi.org/10.1007/s12600-011-0157-5
[45]  Pearson, A.C. (1982) Biology, Population Dynamics, and Pest Status of the Beet Armyworm (Spodoptera exigua) in the Imperial Valley of California. Ph.D. Dissertation, University of California, Riverside.
[46]  Badenes-Pérez, F.R. (2023) Plant Glucosinolate Content and Host-Plant Preference and Suitability in the Small White Butterfly (Lepidoptera: Pieridae) and Comparison with Another Specialist Lepidopteran. Plants, 12, Article 2148.
https://doi.org/10.3390/plants12112148
[47]  Mumm, R., Burow, M., Bukovinszkine’Kiss, G., Kazantzidou, E., Wittstock, U., Dicke, M. and Gershenzon, J. (2008) Formation of Simple Nitriles upon Glucosinolate Hydrolysis Affects Direct and Indirect Defense against the Specialist Herbivore, Pieris rapae. Chemical Ecology, 34, 1311-1321.
https://doi.org/10.1007/s10886-008-9534-z
[48]  Voelckel, C. and Baldwin, I.T. (2004) Generalist and Specialist Lepidopteran Larvae Elicit Different Transcriptional Responses in Nicotiana attenuata, Which Correlate with Larval FAC Profiles. Ecology Letters, 7, 770-775.
https://doi.org/10.1111/j.1461-0248.2004.00633.x
[49]  Eckardt, N.A. (2001) Some Like It with Nitriles: A Nitrile-Specifying Protein Linked to Herbivore Feeding Behaviors in Arabidopsis. Plant Cell, 13, 2565-2568.
https://doi.org/10.1105/tpc.131210
[50]  Lambrix, V., Reichelt, M., Mitchell-Olds, T., Kliebenstein, D.J. and Gershenzon, J. (2001) The Arabidopsis Epithiospecifier Protein Promotes the Hydrolysis of Glucosinolates to Nitrile and Influences Trichoplusia ni Herbivory. Plant Cell, 13, 2793-2807.
https://doi.org/10.1105/tpc.010261
[51]  Ryan, S.F. and Bidart-Bouzat, M.G. (2014) Natal Insect Experience with Arabidopsis thaliana Plant Genotypes Influences Plasticity in Oviposition Behavior. Entomologia Experimentalis et Applicata, 152, 216-227.
https://doi.org/10.1111/eea.12221

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