Abstract
Oligophagous insects can consume a wide range of different host plant species, but how these host plants vary in their metabolite compositions and the extent to which this variation affects the biochemistry of the insect herbivores is largely unknown. An understanding of how defensive metabolites from plants are processed by insects may help us develop more effective pesticides. We studied the interactions between the oligophagous insect herbivore Pieris rapae (Lepidoptera: Pieridae) and five species of its larval host plants (family Brassicaceae and Cleomaceae) by examining untargeted metabolic fingerprints of the plants and the larval herbivores feeding on them. Visualisation of the metabolic fingerprints of the different host plant species showed highly distinctive clusters in the PCA-X score plots. Larvae could also be distinguished based on the species of host plant they fed on but clusters overlapped to a greater extent. The fingerprints of larvae feeding on Cleome spinosa plants were most distinctive due to a large group of abundant metabolites also found in high abundance in C. spinosa, but not in the other host plants examined. We conclude that host plants influence the biochemistry of their larval herbivores, and that some metabolites are conserved from one trophic level to the next.
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References
Allwood JW, Ellis DI, Goodacre R (2008) Metabolomic technologies and their application to the study of plants and plant–host interactions. Physiol Plantarum 132:117–135
Asher J, Warren M, Fox R, Harding P, Jeffcoate G, Jeffcoate S (2001) The Millennium Atlas of butterflies in Britain and Ireland. Oxford University Press Inc., New York
Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA (2008) Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. Am J Bot 95:1307–1327. https://doi.org/10.3732/ajb.0800065
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289–300
Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol 50:1339–1354. https://doi.org/10.1111/j.1744-7909.2008.00751.x
Braby MF, Trueman JWH (2006) Evolution of larval host plant associations and adaptive radiation in Pierid butterflies. J Evol Bio 19:1677–1690. https://doi.org/10.1111/j.1420-9101.2006.01109.x
Brower LP, Brower JV, Corvino JM (1967) Plant poisons in a terrestrial food chain. Proc Natl Acad Sci USA 57:893–898. https://doi.org/10.1073/pnas.57.4.893
Cohen JA, Brower LP (1983) Cardenolide sequestration by the dogbane tiger moth (Cycnia tenera, Arctiidae). J Chem Ecol 9:521–532. https://doi.org/10.1007/bf00990224
Colinet H, Larvor V, Laparie M, Renault D (2012) Exploring the plastic response to cold acclimation through metabolomics. Funct Ecol 26:711–722. https://doi.org/10.1111/j.1365-2435.2012.01985.x
Davies HV, Shepherd LVT, Stewart D, Frank T, Rohlig RM, Engel KH (2010) Metabolome variability in crop plant species—when, where, how much and so what? Regul Toxicol Pharm 58:S54–S61. https://doi.org/10.1016/j.yrtph.2010.07.004
Eeles P (2018) Species Listings: Small White http://www.ukbutterflies.co.uk/species.php?species=rapae
Fahey JW, Zalcmann AT, Talalay P (2002) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants (vol 56, p. 5, 2001). Phytochemistry 59:237–237. https://doi.org/10.1016/s0031-9422(01)00419-8
Fiehn O (2001) Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comp Funct Genomics 2:155–168. https://doi.org/10.1002/cfg.82
Hasapis X, Macleod AJ, Moreau M (1981) Glucosinolates of 9 Cruciferae and 2 Capparaceae species. Phytochemistry 20:2355–2358. https://doi.org/10.1016/s0031-9422(00)82665-5
Hrydziuszko O, Viant MR (2012) Missing values in mass spectrometry based metabolomics: an undervalued step in the data processing pipeline. Metabolomics 8:S161–S174. https://doi.org/10.1007/s11306-011-0366-4
Huang XP, Renwick JAA (1994) Relative activities of glucosinolates as oviposition stimulants for Pieris rapae and P. napi oleracea. J Chem Ecol 20:1025–1037. https://doi.org/10.1007/bf02059739
Jansen JJ, Allwood JW, Marsden-Edwards E, van der Putten WH, Goodacre R, van Dam NM (2009) Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5:150–161. https://doi.org/10.1007/s11306-008-0124-4
Koritsas VM, Lewis JA, Fenwick GR (1991) Glucosinolate responses of oilseed rape, mustard and kale to mechanical wounding and infestation by cabbage stem flea beetle (Psylliodes chrysocephala). Ann Appl Biol 118:209–221. https://doi.org/10.1111/j.1744-7348.1991.tb06099.x
Kroymann J (2011) Natural diversity and adaptation in plant secondary metabolism. Curr Opin Plant Biol 14:246–251. https://doi.org/10.1016/j.pbi.2011.03.021
Ladhari A, Laarif A, Omezzine F, Haouala R (2013) Effect of the extracts of the spiderflower, Cleome arabica, on feeding and survival of larvae of the cotton leafworm, Spodoptera littoralis. J Insect Sci 13:1–14
Li Q, Eigenbrode SD, Stringham GR, Thiagarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419
Malmendal A, Overgaard J, Bundy JG, Sorensen JG, Nielsen NC, Loeschcke V, Holmstrup M (2006) Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. Am J Physiol Regul Integr Comp Physiol 291:R205–R212. https://doi.org/10.1152/ajpregu.00867.2005
Michaud MR, Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE, Denlinger DL (2008) Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J Insect Physiol 54:645–655. https://doi.org/10.1016/j.jinsphys.2008.01.003
Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154. https://doi.org/10.1007/s00049-009-0018-6
Perera MVL (2011) Metabolic profiling of plant disease: from data alignment to pathway predictions. Dissertation, University of Exeter
Prokhorov AV (2011) Hotelling’s T2 distribution. Encyclopedia of Mathematics: http://www.encyclopediaofmath.org/index.php?title=Hotelling-T%5E2-distribution&oldid=12614. Accessed 17 February 2016
R Core Team (2013) R; A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–113. https://doi.org/10.1023/a:1006380021658
Renwick JAA, Lopez K (1999) Experience-based food consumption by larvae of Pieris rapae: addiction to glucosinolates? Entomol Exp Appl 91:51–58. https://doi.org/10.1046/j.1570-7458.1999.00465.x
Robinson G, Ackery P, Kitching I, Beccaloni G, Hernández L (2001) Hostplants of the moth and butterfly caterpillars of the Oriental Region. Natural History Museum in association with Southdene Sdn Bhd, Malaysia
Rodman JE, Chew FS (1980) Phytochemical correlates of herbivory in a community of native and naturalized Cruciferae. Biochem Syst Ecol 8:43–50. https://doi.org/10.1016/0305-1978(80)90024-1
Rohr F, Ulrichs C, Mewis I (2009) Variability of aliphatic glucosinolates in Arabidopsis thaliana (L.)—impact on glucosinolate profile and insect resistance. J Appl Bot Food Qual 82:131–135
Schoonhoven L, van Loon J, Dicke M (2005) Insect–plant biology. Second edition. Oxford University Press, Oxford
Schroeder FC, del Campo ML, Grant JB, Weibel DB, Smedley SR, Bolton KL, Meinwald J, Eisner T (2006) Pinoresinol: a lignol of plant origin serving for defense in a caterpillar. Proc Nat Acad Sci USA 103:15497–15501. https://doi.org/10.1073/pnas.0605921103
Snart CJP, Hardy ICW, Barrett DA (2015) Entometabolomics:applications of modern analytical techniques to insect studies. Entomol Exp Appl 155:1–17. https://doi.org/10.1111/eea.12281
Soliman MMM (2012) Toxicity and biological effects of some wild plant extracts against potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Egypt J Biol Pest Control 22:19–25
Stevens PF (2001) Angiosperm Phylogeny Website. http://www.mobot.org/MOBOT/research/APweb/. Accessed 17 February 2016
Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry. https://doi.org/10.1016/s0031-9422(02)00708-2
Verberk WCEP, Sommer U, Davidson RL, Viant MR (2013) Anaerobic metabolism at thermal extremes: A metabolomic test of the oxygen limitation hypothesis in an aquatic insect. Integr Comp Biol 53:609–619. https://doi.org/10.1093/icb/ict015
Williams CM, Waranabe M, Guarracino MR, Ferraro MB, Edison AS, Morgan TJ, Boroujerdi AFB, Hahn DA (2014) Cold adaptationshapes the robustness of metabolic networks in Drosophila melanogaster. Evolution 68:3505–3523
Wu J, Baldwin IT (2010) New Insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
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ACR, SDP and JKH designed the study, ACR, HVF, LAR and MVLP analysed the data. ACR performed the experiments and instigated the writing of the paper and all authors commented on the paper.
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Riach, A.C., Perera, M.V.L., Florance, H.V. et al. Metabolic fingerprints reveal how an insect metabolome is affected by different larval host plant species. Arthropod-Plant Interactions 13, 571–579 (2019). https://doi.org/10.1007/s11829-019-09671-6
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DOI: https://doi.org/10.1007/s11829-019-09671-6