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The role of carotenoids and their derivatives in mediating interactions between insects and their environment

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Abstract

Carotenoids are long conjugated isoprenoid molecules derived mainly from plants and microbial organisms. They are highly diverse, with over 700 identified structures, and are widespread in nature. In addition to their fundamental roles as light-harvesting molecules in photosynthesis, carotenoids serve a variety of functions including visual and colouring pigments, antioxidants and hormone precursors. Although the functions of carotenoids are relatively well studied in plants and vertebrates, studies are severely lacking in insect systems. There is a particular dearth of knowledge on how carotenoids move among trophic levels, influence insect multitrophic interactions and affect evolutionary outcomes. This review explores the known and potential roles that carotenoids and their derivatives have in mediating the ecological interaction of insects with their environment. Throughout the review, we highlight how the fundamental roles of carotenoids in insect physiology might be linked to ecological and evolutionary processes.

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References

  • Aarseth KA, Schram TA (2002) Susceptibility to ultraviolet radiation in Calanus finmarchicus and Lepeophtheirus salmonis and the adaptive value of external filtering (Crustacea : Copepoda). J Plankton Res 24:661–679

    Article  CAS  Google Scholar 

  • Achuo EA, Prinsen E, Hofte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol 55:178–186

    Article  CAS  Google Scholar 

  • Ahmad S (1992) Biochemical defense of prooxidant plant allelochemicals by herbivorous insects. Biochem Syst Ecol 20:269–296

    Article  CAS  Google Scholar 

  • Ahmad S, Pardini RS (1990) Mechanisms for regulating oxygen toxicity in phytophagous insects. Free Radic Biol Med 8:401–413

    Article  PubMed  CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  CAS  Google Scholar 

  • Alkhedir H, Karlovsky P, Vidal S (2010) Effect of light intensity on colour morph formation and performance of the grain aphid Sitobion avenae F (Homoptera: Aphididae). J Insect Physiol 56:1999–2005

    Article  PubMed  CAS  Google Scholar 

  • Altincicek B, Kovacs JL, Gerardo NM (2011) Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Lett 00:1–5

    Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  PubMed  CAS  Google Scholar 

  • Andersson J, Borg-Karlson A, Vongvanich N, Wiklund C (2007) Male sex pheromone release and female mate choice in a butterfly. J Exp Biol 210:964–970

    Article  PubMed  CAS  Google Scholar 

  • Aplin RT, Birch MC (1970) Identification of odorous compounds from male Lepidoptera. Experientia 26:1193–1194

    Article  PubMed  CAS  Google Scholar 

  • Arai K, Shimizu S, Miyajima H, Yamamoto Y (1989) Castaneiolide, abscisic acid and monorden, phytotoxic compounds isolated from fungi (Macrophoma castaneicola and Didymosporium radicicola) cause black root rot disease in chestnut trees. Chem Pharm Bull 37:2870–2872

    Article  CAS  Google Scholar 

  • Archetti M (2000) The origin of autumn colours by coevolution. J Theor Biol 205:625–630

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta Mol Cell Biol Lipids 1734:91–111

    Article  CAS  Google Scholar 

  • Asselbergh B, De Vieesschauwer D, Hofte M (2008) Global switches and fine-tuning—ABA modulates plant pathogen defense. Mol Plant Microbe Interact 21:709–719

    Article  PubMed  CAS  Google Scholar 

  • Assmann SM (2004) Abscisic acid signal transduction in stomatal responses. In: Davies PJ (ed) Plant hormones biosynthesis, signal transduction, action! 3rd edn. Kluwer Academic Publishers, Boston, pp 391–412

    Google Scholar 

  • Aucoin RR, Fields P, Lewis MA, Philogene BJR, Arnason JT (1990) The protective effect of antioxidants to a phototoxin-sensitive insect herbivore, Manduca sexta. J Chem Ecol 16:2913–2924

    Article  CAS  Google Scholar 

  • Aucoin R, Guillet G, Murray C, Philogene BJR, Arnason JT (1995) How do insect herbivores cope with the extreme oxidative stress of phototoxic host plants? Arch Insect Biochem Physiol 29:211–226

    Article  CAS  Google Scholar 

  • Audenaert K, De Meyer GB, Hofte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanism. Plant Physiol 128:491–501

    Article  PubMed  CAS  Google Scholar 

  • Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321

    Article  PubMed  CAS  Google Scholar 

  • Awad AA, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48:221–227

    CAS  Google Scholar 

  • Babin A, Biard C, Moret Y (2010) Dietary supplementation with carotenoids improves immunity without increasing its cost in a crustacean. Am Nat 176:234–241

    Article  PubMed  Google Scholar 

  • Badyaev AV (2011) Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology. Proc R Soc B 278:1921–1929

    Article  PubMed  Google Scholar 

  • Badyaev AV, Hill GE, Dunn PO, Glen JC (2001) Plumage color as a composite trait: developmental and functional integration of sexual ornamentation. Am Nat 158:221–235

    Article  PubMed  CAS  Google Scholar 

  • Baker TC (1985) Chemical control of behavior. In: Kerkut GA, Gilbert LI (eds) Behavior, vol 9, comprehensive insect physiology, biochemistry, and pharmacology, vol 9. Pergamon Press, Oxford, pp 621–672

    Google Scholar 

  • Baker TC, Vickers NJ (1997) Pheromone-mediated flight in moths. In: Carde RT, Minks AK (eds) Insect pheromone research: new directions. Chapman & Hall, New York, pp 248–264

    Chapter  Google Scholar 

  • Baldermann S, Naim M, Fleischmann P (2005) Enzymatic carotenoid degradation and aroma formation in nectarines (Prunus persica). Food Res Int 38:833–836

    Article  CAS  Google Scholar 

  • Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661–1672

    Article  PubMed  CAS  Google Scholar 

  • Bentz BJ, Six DL (2006) Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Ann Entomol Soc Am 99:189–194

    Article  CAS  Google Scholar 

  • Berenbaum MR (1987) Charge of the light brigade: phototoxicity as a defense against insects. ACS Symp Ser 339:206–216

    Article  CAS  Google Scholar 

  • Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399

    Article  Google Scholar 

  • Bezzerides AL, McGraw KJ, Parker RS, Husseini J (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav Ecol Sociobiol 61:1401–1408

    Article  Google Scholar 

  • Bhosale P, Bernstein PS (2007) Vertebrate and invertebrate carotenoid-binding proteins. Arch Biochem Biophys 458:121–127

    Article  PubMed  CAS  Google Scholar 

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory—primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530

    Article  CAS  Google Scholar 

  • Birch M (1970) Pre-courtship use of abdominal brushes by nocturnal moth, Phlogophora meticulosa (L.) (Lepidoptera-Noctuidae). Anim Behav 18:310–316

    Article  Google Scholar 

  • Birch ML, Brewer JW, Rohfritsch O (1992) Biology of Dasineura affinis Cecidomyiidae and influence of its gall on Viola odorata. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 174–184

    Google Scholar 

  • Bissett J, Borkent A (1988) Ambrosia galls: the significance of fungal nutrition in the evolution of the Cecidomyiidae. In: Pirozynski KA, Hawksworth DL (eds) Coevolution of fungi with plants and animals. Academic Press, San Diego, CA, pp 203–225

    Google Scholar 

  • Blount JD, McGraw KJ (2008) Signal functions of carotenoid colouration. In: Britton G, LiaaenJensen S, Pfander H (eds) Carotenoids, vol 4: natural functions. Birkhäuser Verlag, Boston, pp 213–236

    Google Scholar 

  • Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc B 276:871–877

    Article  PubMed  Google Scholar 

  • Bondi A, Meyer H (1946) Carotene in Palestinian crops. J Agric Sci 36:1–5

    Article  CAS  Google Scholar 

  • Borkent A, Bissett J (1985) Gall midges (Diptera: Cecidomyiidae) are vectors of their fungal symbionts. Symbiosis 1:185–194

    Google Scholar 

  • Bouvier F, Isner JC, Dogbo O, Camara B (2005) Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci 10:187–194

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178

    Article  PubMed  CAS  Google Scholar 

  • Britton G (1995a) Structure and properties of carotenoids in relation to function. Faseb J 9:1551–1558

    PubMed  CAS  Google Scholar 

  • Britton G (1995b) Chapter 7: worked examples of isolation and analysis, example 1, higher plants. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, volume 1A: isolation and analysis. Birkhäuser Verlag, Boston, MA, pp 201–214

    Google Scholar 

  • Britton G (2008) Chapter 15: functions of carotenoid metabolites and breakdown products. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, volume 4: natural functions. Birkhäuser Verlag, Boston, pp 309–323

    Google Scholar 

  • Britton G, Helliwell JR (2008) Chapter 6: carotenoid-protein interactions. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, volume 4: natural functions. Birkhäuser Verlag, Boston, pp 99–117

    Google Scholar 

  • Britton G, Lockley WJS, Harriman GA, Goodwin TW (1977) Pigmentation of ladybird beetle Coccinella septempunctata by carotenoids not of plant origin. Nature 266:49–50

    Article  PubMed  CAS  Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids handbook. Birkhäuser Verlag, Boston, MA

    Book  Google Scholar 

  • Bronner R (1992) The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 118–140

    Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Wiley Interscience, New York

    Google Scholar 

  • Burmester A, Richter M, Schultze K, Voelz K, Schachtschabel D, Boland W, Woestemeyer J, Schimek C (2007) Cleavage of beta-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated beta-carotene oxygenase. Fungal Genet Biol 44:1096–1108

    Article  PubMed  CAS  Google Scholar 

  • Camp RR (1981) Insect fungus blister galls on Solidago graminifolia and Solidago rugosa.1. A macroscopic and light microscopic study of the host-parasite relationship. Can J Bot 59:2466–2477

    Article  Google Scholar 

  • Carroll MJ, Berenbaum MR (2006) Lutein sequestration and furanocoumarin metabolism in parsnip webworms under different ultraviolet light regimes in the montane west. J Chem Ecol 32:277–305

    Article  PubMed  CAS  Google Scholar 

  • Carroll M, Hanlon A, Hanlon T, Zangerl AR, Berenbaum MR (1997) Behavioral effects of carotenoid sequestration by the parsnip webworm, Depressaria pastinacella. J Chem Ecol 23:2707–2719

    Article  CAS  Google Scholar 

  • Catoni C, Peters A, Schaefer HM (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim Behav 76:1107–1119

    Article  Google Scholar 

  • Cherrett JM, Powell RJ, Stradling DJ (1989) The mutualism between leaf-cutting ants and their fungus. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, New York, pp 93–116

    Chapter  Google Scholar 

  • Cipollini ML (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440

    Article  Google Scholar 

  • Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653

    Article  PubMed  CAS  Google Scholar 

  • Coleman RA, Barker AM, Fenner M, King FC (1997) Relative effect of different host feeding site on long-range host location and electroantennogram response in the parasitoid Cotesia glomerata (Hym., Braconidae). J Appl Entomol 121:487–494

    Article  Google Scholar 

  • Cook CE, Coggon P, Mcphail AT, Wall ME, Whichard LP, Egley GH, Luhan PA (1972) Germination stimulants. II. Structure of strigol—potent seed-germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199

    Article  CAS  Google Scholar 

  • Cornet S, Biard C, Moret Y (2007) Is there a role for antioxidant carotenoids in limiting self-harming immune response in invertebrates? Biol Lett 3:284–288

    Article  PubMed  CAS  Google Scholar 

  • Crocoll C, Kettner J, Dorffling K (1991) Abscisic acid in saprophytic and parasitic species of fungi. Phytochemistry 30:1059–1060

    Article  CAS  Google Scholar 

  • Czeczuga B (1976) Investigations on the carotenoids in 19 species of aphids and their host plants. Zool Pol 25:27–46

    CAS  Google Scholar 

  • Czeczuga B (1980) Investigations on carotenoids in insects. I. The presence and metabolism of carotenoid pigments in the aphids. Rocz Akad Med Im Juliana Marchlewskiego Bialymst 25:113–120

    PubMed  CAS  Google Scholar 

  • Czeczuga B (1981) Investigations on carotenoids in insects. 4. The occurrence of particular carotenoids in Apis melifera L (Apidae). Apidologie 12:107–112

    Article  CAS  Google Scholar 

  • Czeczuga B (1982) Investigations on carotenoids in insects.6. Occurrence of alpha-doradexanthin in some Insects. Folia Biol (Krakow, Pol) 30:143–148

    CAS  Google Scholar 

  • Czeczuga B (1985) Investigations on carotenoids in insects. 7. Contents of carotenoids in worker bees feeding on flowers of different plants. Zool Pol 32:183–190

    CAS  Google Scholar 

  • Czeczuga B (1986) Investigations on carotenoids in insects. 8. The presence of carotenoids in various species of Lepidoptera. Biochem Syst Ecol 14:345–351

    Article  CAS  Google Scholar 

  • Czeczuga B (1988) Investigations on carotenoids in insects. 9. Apocarotenals in representatives of the Cerambycidae family. Folia Biol (Krakow, Pol) 36:167–172

    CAS  Google Scholar 

  • Czeczuga B (1990) Investigations on carotenoids in insects. 10. Changes in the carotenoids in butterflies (Lepidoptera). Folia Biol (Krakow, Pol) 38:5–12

    CAS  Google Scholar 

  • Czeczuga B (1991) Investigations on insects. 11. Carotenoids in some cave-dwelling insects. Folia Biol (Krakow, Pol) 39:17–20

    CAS  Google Scholar 

  • Czeczuga B, Mironiuk W (1980) Investigations on carotenoids in insects. 2. Water insects. Acta Hydrobiol 22:29–36

    CAS  Google Scholar 

  • Czeczuga B, Weyda F (1982) Investigation on carotenoids in insects. 5. Archaeognatha Insecta Apterygota. Zool Pol 29:23–32

    CAS  Google Scholar 

  • Dahiya JS, Tewari JP, Woods DL (1988) Abscisic acid from Alternaria brassicae. Phytochemistry 27:2983–2984

    Article  CAS  Google Scholar 

  • Davidson BS, Eisner T, Meinwald J (1991) 3,4-Didehydro-beta, beta-caroten-2-one, a new carotenoid from the eggs of the stick insect Anisomorpha buprestoides. Tetrahedron Lett 32:5651–5654

    Article  CAS  Google Scholar 

  • Davis AK, Cope N, Smith A, Solensky MJ (2007) Wing color predicts future mating success in male monarch butterflies. Ann Entomol Soc Am 100:339–344

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Dorffling K, Petersen W, Sprecher E, Urbasch I, Hanssen HP (1984) Abscisic acid in phytopathogenic fungi of the genera Botrytis, Ceratocystis, Fusarium, and Rhizoctonia. Z Naturforsch, C: J Biosci 39:683–684

    Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod Plant Interact 1:45–55

    Article  Google Scholar 

  • Edmunds M, Grayson J (1991) Camouflage and selective predation in caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata). Biol J Linn Soc 42:467–480

    Article  Google Scholar 

  • Eichenseer H, Murphy JB, Felton GW (2002) Sequestration of host plant carotenoids in the larval tissues of Helicoverpa zea. J Insect Physiol 48:311–318

    Article  PubMed  CAS  Google Scholar 

  • Eisenreich W, Rohdich F, Bacher A (2001) Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci 6:78–84

    Article  PubMed  CAS  Google Scholar 

  • El-Sayed AM (2011) The pherobase: database of insect pheromones and semiochemicals. http://www.pherobase.com. Accessed 12 Mar 2012

  • Enright S, Cipollini D (2011) Overlapping defense responses to water limitation and pathogen attack and their consequences for resistance to powdery mildew disease in garlic mustard, Alliaria petiolata. Chemoecology 21:89–98

    Article  CAS  Google Scholar 

  • Escobar JA, Rubio MA, Lissi EA (1996) SOD and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radical Biol Med 20:285–290

    Article  CAS  Google Scholar 

  • Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    PubMed  CAS  Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197

    Article  PubMed  CAS  Google Scholar 

  • Feltwell J, Rothschild M (1974) Carotenoids in 38 species of Lepidoptera. J Zool 174:441–465

    Article  Google Scholar 

  • Feltwell JS, Valadon LRG (1974) Carotenoid changes in Brassica oleracea var. capitata L. with age, in relation to large white butterfly, Pieris brassicae L. J Agric Sci 83:19–26

    Article  Google Scholar 

  • Fermaud M, Lemenn R (1989) Association of Botrytis cinerea with grape berry moth larvae. Phytopathology 79:651–656

    Article  Google Scholar 

  • Ferreira ACS, Monteiro J, Oliveira C, Pinho PG (2008) Study of major aromatic compounds in Port wines from carotenoid degradation. Food Chem 110:83–87

    Article  CAS  Google Scholar 

  • Finkelstein RR (2004) The role of hormones during seed development and germination. In: Davies PJ (ed) Plant hormones biosynthesis, signal transduction, action!, 3rd edn. Kluwer Academic Publishers, Boston, pp 513–537

    Google Scholar 

  • Fox DL (1976) Animal biochromes and structural colours. University of California Press, Los Angeles

    Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gagné RJ (1989) The plant-feeding gall midges of North America. Cornell University Press, Ithaca, NY

    Google Scholar 

  • Gao HY, Zhu HL, Shao Y, Chen AJ, Lu CW, Zhu BZ, Luo YB (2008) Lycopene accumulation affects the biosynthesis of some carotenoid-related volatiles independent of ethylene in tomato. J Integr Plant Biol 50:991–996

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Limones C, Schnabele K, Blanco-Portales R, Bellido ML, Caballero JL, Schwab W, Munoz-Blanco J (2008) Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. J Agric Food Chem 56:9277–9285

    Article  PubMed  CAS  Google Scholar 

  • Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE (2006) Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509

    Article  PubMed  CAS  Google Scholar 

  • Gebbinck EAK, Jansen BJM, de Groot A (2002) Insect antifeedant activity of clerodane diterpenes and related model compounds. Phytochemistry 61:737–770

    Article  Google Scholar 

  • Georgiou CD (1997) Lipid peroxidation in Sclerotium rolfsii: a new look into the mechanism of sclerotial biogenesis in fungi. Mycol Res 101:460–464

    Article  CAS  Google Scholar 

  • Georgiou CD, Tairis N, Polycratis A (2001a) Production of beta-carotene by Sclerotinia sclerotiorum and its role in sclerotium differentiation. Mycol Res 105:1110–1115

    Article  CAS  Google Scholar 

  • Georgiou CD, Zervoudakis G, Tairis N, Kornaros M (2001b) Beta-carotene production and its role in sclerotial differentiation of Sclerotium rolfsii. Fungal Genet Biol 34:11–20

    Article  PubMed  CAS  Google Scholar 

  • Gerould JH (1921) Blue-green caterpillars: the origin and ecology of a mutation in hemolymph color in Colias (Eurymus) philodice. J Exp Zool 34:385–415

    Article  CAS  Google Scholar 

  • Gessler NN, Sokolov AV, Belozerskaya TA (2002) Initial stages of trisporic acid synthesis in Blakeslea trispora. Appl Biochem Microbiol 38:536–543

    Article  CAS  Google Scholar 

  • Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815–819

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6:273–297

    Article  PubMed  CAS  Google Scholar 

  • Gouinguene S, Pickett JA, Wadhams LJ, Birkett MA, Turlings TCJ (2005) Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J Chem Ecol 31:1023–1038

    Article  PubMed  CAS  Google Scholar 

  • Grayson J, Edmunds M (1989) The causes of color and color change in caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata). Biol J Linn Soc 37:263–279

    Article  Google Scholar 

  • Grayson J, Edmunds M, Evans EH, Britton G (1991) Carotenoids and coloration of poplar hawkmoth caterpillars (Laothoe populi). Biol J Linn Soc 42:457–465

    Article  Google Scholar 

  • Greene E (1996) Effect of light quality and larval diet on morph induction in the polymorphic caterpillar Nemoria arizonaria (Lepidoptera: Geometridae). Biol J Linn Soc 58:277–285

    Google Scholar 

  • Grime JP, Pierce S (2012) The evolutionary strategies that shape ecosystems. Wiley-Blackwell, New Jersey

    Book  Google Scholar 

  • Grunewald K, Hirschberg J, Hagen C (2001) Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. J Biol Chem 276:6023–6029

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD, Brown SP (2001) Autumn tree colours as a handicap signal. Proc R Soc B 268:1489–1493

    Article  PubMed  CAS  Google Scholar 

  • Hartel H, Grimm B (1998) Consequences of chlorophyll deficiency for leaf carotenoid composition in tobacco synthesizing glutamate 1-semialdehyde aminotransferase antisense RNA: dependency on developmental age and growth light. J Exp Bot 49:535–546

    CAS  Google Scholar 

  • Heath JJ, Stireman JO III (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomol Exp Appl 137:36–49

    Article  Google Scholar 

  • Heath JJ, Williams RN, Phelan PL (2001) High light intensity: a critical factor in the wind-tunnel flight of two scarabs, the rose chafer and Japanese beetle. J Chem Ecol 27:419–429

    Article  PubMed  CAS  Google Scholar 

  • Heath JJ, Williams RN, Phelan PL (2002) Aggregation and male attraction to feeding virgin females in Macrodactylus subspinosus (F.) (Coleoptera: Scarabaeidae: Melolonthinae). Environ Entomol 31:934–940

    Article  Google Scholar 

  • Heath JJ, Zhang AJ, Roelofs WL, Smith RF (2005) Flight activity and further evidence for a female-produced sex pheromone of the apple leaf midge, Dasineura mali, in Nova Scotia. Northeast Nat 12:93–102

    Article  Google Scholar 

  • Heath JJ, Wells B, Cipollini D, Stireman III JO (2012) Carnivores and carotenoids are associated with adaptive behavioural divergence in a radiation of gall midges. Ecol Entomol. doi:10.1111/j.1365-2311.2012.01397.x

  • Henfling JWDM, Bostock RM, Kuc J (1980) Effect of abscisic acid on rishitin and lubimin accumulation and resistance to Phytophthora infestans and Cladosporium cucumerinum in potato-tuber tissue-slices. Phytopathology 70:1074–1078

    Article  CAS  Google Scholar 

  • Heng-Moss TM, Ni X, Macedo T, Markwell JP, Baxendale FP, Quisenberry SS, Tolmay V (2003) Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J Econ Entomol 96:475–481

    Article  PubMed  CAS  Google Scholar 

  • Hildebrand DF, Rodriguez JG, Brown GC, Luu KT, Volden CS (1986a) Peroxidative responses of leaves in 2 soybean genotypes injured by 2-spotted spider mites (Acari, Tetranychidae). J Econ Entomol 79:1459–1465

    Google Scholar 

  • Hildebrand DF, Rodriguez JG, Brown GC, Volden CS (1986b) 2-spotted spider mite (Acari, Tetranychidae) infestations on soybeans—effect on composition and growth of susceptible and resistant cultivars. J Econ Entomol 79:915–921

    CAS  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  PubMed  CAS  Google Scholar 

  • Holopainen JK (2008) Importance of olfactory and visual signals of autumn leaves in the coevolution of aphids and trees. BioEssays 30:889–896

    Article  PubMed  Google Scholar 

  • Humphrey AJ, Beale MH (2006) Strigol: biogenesis and physiological activity. Phytochemistry 67:636–640

    Article  PubMed  CAS  Google Scholar 

  • Humphrey AJ, Galster AM, Beale MH (2006) Strigolactones in chemical ecology: waste products or vital allelochemicals? Nat Prod Rep 23:592–614

    Article  PubMed  CAS  Google Scholar 

  • Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N, Tadmor Y, Lewinsohn E (2006) Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67:1579–1589

    Article  PubMed  CAS  Google Scholar 

  • Inbar M, Izhaki I, Koplovich A, Lupo I, Silanikove N, Glasser T, Gerchman Y, Perevolotsky A, Lev-Yadun S (2010a) Why do many galls have conspicuous colours? An alternative hypothesis revisited conspicuous gall colors: a response to T. C. R. White. Arthropod Plant Interact 4:151–152

    Article  Google Scholar 

  • Inbar M, Izhaki I, Koplovich A, Lupo I, Silanikove N, Glasser T, Gerchman Y, Perevolotsky A, Lev-Yadun S (2010b) Why do many galls have conspicuous colors? A new hypothesis. Arthropod Plant Interact 4:1–6

    Article  Google Scholar 

  • Inomata M, Hirai N, Yoshida R, Ohigashi H (2004a) Biosynthesis of abscisic acid by the direct pathway via ionylideneethane in a fungus, Cercospora cruenta. Biosci Biotechnol Biochem 68:2571–2580

    Article  PubMed  CAS  Google Scholar 

  • Inomata M, Hirai N, Yoshida R, Ohigashi H (2004b) The biosynthetic pathway to abscisic acid via ionylideneethane in the fungus Botrytis cinerea. Phytochemistry 65:2667–2678

    Article  PubMed  CAS  Google Scholar 

  • Janson EM, Stireman JO III, Singer MS, Abbot P (2008) Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62:997–1012

    Article  PubMed  Google Scholar 

  • Janson EM, Grebenok RJ, Behmer ST, Abbot P (2009) Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. J Chem Ecol 35:1309–1319

    Article  PubMed  CAS  Google Scholar 

  • Janson EM, Peeden ER, Stireman JO III, Abbot P (2010) Symbiont-mediated phenotypic variation without co-evolution in an insect–fungus association. J Evol Biol 23:2212–2228

    Article  PubMed  CAS  Google Scholar 

  • Jenkins RL, Loxdale HD, Brookes CP, Dixon AFG (1999) The major carotenoid pigments of the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae). Physiol Entomol 24:171–178

    Article  CAS  Google Scholar 

  • Jurkiewicz BA, Buettner GR (1994) Ultraviolet light induced free-radical formation in skin—an electron paramagnetic resonance study. Photochem Photobiol 59:1–4

    Article  PubMed  CAS  Google Scholar 

  • Kaissling KE (1996) Peripheral mechanisms of pheromone reception in moths. Chem Senses 21:257–268

    Article  PubMed  CAS  Google Scholar 

  • Kayser H (1982) Carotenoids in insects. In: Britton G, Goodwin TW (eds) Carotenoid chemistry and biochemistry: proceedings of the 6th international symposium on carotenoids. Pergamon Press, New York, pp 195–210

    Google Scholar 

  • Kende H, Zeevaart JAD (1997) The five ‘‘classical’’ plant hormones. Plant Cell 9:1197–1210

    Article  PubMed  CAS  Google Scholar 

  • Kettner J, Dorffling K (1995) Biosynthesis and metabolism of abscisic acid in tomato leaves infected with Botrytis cinerea. Planta 196:627–634

    Article  CAS  Google Scholar 

  • Kiefer C, Sumser E, Wernet MF, von Lintig J (2002) A class B scavenger receptor mediates the cellular uptake of carotenoids in Drosophila. Proc Natl Acad Sci USA 99:10581–10586

    Article  PubMed  CAS  Google Scholar 

  • Kodric-Brown A, Brown JH (1984) Truth in advertising—the kinds of traits favored by sexual selection. Am Nat 124:309–323

    Article  Google Scholar 

  • Koga H, Dohi K, Mori M (2004) Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol Mol Plant Pathol 65:3–9

    Article  CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  PubMed  CAS  Google Scholar 

  • Langley SA, Tilmon KJ, Cardinale BJ, Ives AR (2006) Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs. Oecologia 150:172–179

    Article  PubMed  Google Scholar 

  • Lev-Yadun S, Gould KS (2007) What do red and yellow autumn leaves signal? Bot Rev 73:279–289

    Article  Google Scholar 

  • Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Ibdah M, Meir A, Yosef E, Zamir D, Tadmor Y (2005a) Not just colors—carotenoid degradation as a link between pigmentation and aroma in tomato and watermelon fruit. Trends Food Sci Technol 16:407–415

    Article  CAS  Google Scholar 

  • Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Meir A, Zamir D, Tadmor Y (2005b) Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analyses. J Agric Food Chem 53:3142–3148

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540

    Article  PubMed  CAS  Google Scholar 

  • Losey JE, Ives AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272

    Article  CAS  Google Scholar 

  • Ma ZH, Morgan DP, Michailides TJ (2001) Effects of water stress on Botryosphaeria blight of pistachio caused by Botryosphaeria dothidea. Plant Dis 85:745–749

    Article  Google Scholar 

  • Maffei M, Bossi S, Spiteller D, Mithofer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134:1752–1762

    Article  PubMed  CAS  Google Scholar 

  • Maleck K, Dietrich RA (1999) Defense on multiple fronts: how do plants cope with diverse enemies? Trends Plant Sci 4:215–219

    Article  PubMed  Google Scholar 

  • Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    Article  PubMed  CAS  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414

    Article  PubMed  CAS  Google Scholar 

  • Mayek-Perez N, Garcia-Espinosa R, Lopez-Castaneda C, Acosta-Gallegos JA, Simpson J (2002) Water relations, histopathology and growth of common bean (Phaseolus vulgaris L.) during pathogenesis of Macrophomina phaseolina under drought stress. Physiol Mol Plant Pathol 60:185–195

    Article  Google Scholar 

  • McAuslane HJ, Chen J, Carle RB, Schmalstig J (2004) Influence of Bemisia argentifolii (Homoptera: Aleyrodidae) infestation and squash silverleaf disorder on zucchini seedling growth. J Econ Entomol 97:1096–1105

    Article  PubMed  CAS  Google Scholar 

  • McDonald KL, Cahill DM (1999) Influence of abscisic acid and the abscisic acid biosynthesis inhibitor, norflurazon, on interactions between Phytophthora sojae and soybean (Glycine max). Eur J Plant Pathol 105:651–658

    Article  CAS  Google Scholar 

  • Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467–472

    PubMed  CAS  Google Scholar 

  • Meinwald J, Erickson K, Hartshor M, Meinwald YC, Eisner T (1968) Defensive mechanisms of arthropods. 23. An allenic sesquiterpenoid from grasshopper Romalea microptera. Tetrahedron Lett 9:2959–2962

    Article  Google Scholar 

  • Mikheyev AS, Mueller UG, Abbot P (2006) Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis. Proc Natl Acad Sci USA 103:10702–10706

    Article  PubMed  CAS  Google Scholar 

  • Moczek A, Nijhout H (2002) Developmental mechanisms of threshold evolution in a polyphenic beetle. Evol Dev 4:252–264

    Article  PubMed  Google Scholar 

  • Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30:461–469

    Article  CAS  Google Scholar 

  • Mohr PG, Cahill DM (2007) Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct Integr Genomics 7:181–191

    Article  PubMed  CAS  Google Scholar 

  • Moran NA (2002) The ubiquitous and varied role of infection in the lives of animals and plants. Am Nat 160:S1–S8

    Article  PubMed  Google Scholar 

  • Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627

    Article  PubMed  CAS  Google Scholar 

  • Mothes U, Seitz KA (1982) Fine structural alterations of bean plant leaves by feeding injury of Tetranychus urticae Koch (Acari, Tetranychidae). Acarologia 23:149–157

    Google Scholar 

  • Ni XZ, Quisenberry SS, Heng-Moss T, Markwell J, Higley L, Baxendale F, Sarath G, Klucas R (2002) Dynamic change in photosynthetic pigments and chlorophyll degradation elicited by cereal aphid feeding. Entomol Exp Appl 105:43–53

    Article  CAS  Google Scholar 

  • Nijhout HF (1991) The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Nishida R, Rothschild M, Mummery R (1994) Cyanoglucoside, sarmentosin, from the magpie moth, Abraxas grossulariata, Geometridae, Lepidoptera. Phytochemistry 36:37–38

    Article  CAS  Google Scholar 

  • Noor MAF, Parnell RS, Grant BS (2008) A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars. PLoS ONE. doi:10.1371/journal.pone.0003142

    Google Scholar 

  • Norman SM, Maier VP, Pon DL (1990) Abscisic acid accumulation and carotenoid and chlorophyll content in relation to water stress and leaf age of different types of citrus. J Agric Food Chem 38:1326–1334

    Article  CAS  Google Scholar 

  • Oberhauser KS, Cansler D, Feitl A (1996) Genetics of a “zebra” pigment mutation in the larvae of Danaus plexippus, L. (Nymphalidae: Danainae). J Lepid Soc 50:237–244

    Google Scholar 

  • Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201

    Article  PubMed  CAS  Google Scholar 

  • Ojala K, Julkunen-Tiito R, Lindstrom L, Mappes J (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170

    Google Scholar 

  • Oliveira DC, Isaias RMS, Moreira ASFP, Magalhaes TA, Lemos-Filho JP (2011) Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis? Plant Sci 180:489–495

    Article  PubMed  CAS  Google Scholar 

  • Owen CR, Bradshaw HD (2011) Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod Plant Interact 5:235–244

    Article  Google Scholar 

  • Pfander H (1992) Carotenoids—an overview. Meth Enzymol 213:3–13

    Article  CAS  Google Scholar 

  • Pichersky E (2008) Raging hormones in plants. Nat Chem Biol 4:584–586

    Article  PubMed  CAS  Google Scholar 

  • Poff JM (1976) Carotenoids of some aposematic and cryptic Leptinotarsa (Coleoptera: Chrysomelidae). Am Zool 16:271

    Google Scholar 

  • Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8:1627–1639

    PubMed  CAS  Google Scholar 

  • Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylides C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci U S A 109:5535–5540

    Article  PubMed  CAS  Google Scholar 

  • Rey LA (1992) Developmental morphology of two types of hymenopterous galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 87–101

    Google Scholar 

  • Rhainds M, Doyon J, Rivoal J, Brodeur J (2007) Thrips-induced damage of chrysanthemum inflorescences: evidence for enhanced leakage of carotenoid pigments. Entomol Exp Appl 123:247–252

    Article  CAS  Google Scholar 

  • Ritland DB, Brower LP (1991) The viceroy butterfly is not a batesian mimic. Nature 350:497–498

    Article  Google Scholar 

  • Rothschild M (1991) Is the viceroy a batesian mimic? Nature 351:611–612

    Article  Google Scholar 

  • Rothschild M, Mummery R (1985) Carotenoids and bile pigments in danaid and swallowtail butterflies. Biol J Linn Soc 24:1–14

    Article  Google Scholar 

  • Rothschild M, Gardiner B, Mummery R (1978) Role of carotenoids in “golden glance” of danaid pupae (Insecta: Lepidoptera). J Zool 186:351–358

    Article  Google Scholar 

  • Rothschild M, Mummery R, Farrell C (1986) Carotenoids of butterfly models and their mimics (Lep, Papilionidae and Nymphalidae). Biol J Linn Soc 28:359–372

    Article  Google Scholar 

  • Sakudoh T, Sezutsu H, Nakashima T, Kobayashi I, Fujimoto H, Uchino K, Banno Y, Iwano H, Maekawa H, Tamura T, Kataoka H, Tsuchida K (2007) Carotenoid silk coloration is controlled by a carotenoid-binding protein, a product of the yellow blood gene. Proc Natl Acad Sci USA 104:8941–8946

    Article  PubMed  CAS  Google Scholar 

  • Salt SD, Tuzun S, Kuc J (1986) Effects of beta-ionone and abscisic acid on the growth of tobacco and resistance to blue mold. Mimicry of effects of stem infection by Peronospora tabacina Adam. Physiol Mol Plant Pathol 28:287–297

    Article  CAS  Google Scholar 

  • Sandre S, Tammaru T, Esperk T, Julkunen-Tiitto R, Mappes J (2007) Carotenoid-based colour polyphenism in a moth species: search for fitness correlates. Entomol Exp Appl 124:269–277

    Article  CAS  Google Scholar 

  • Schaefer HM, Rolshausen G (2006) Plants on red alert: do insects pay attention? BioEssays 28:65–71

    Article  PubMed  Google Scholar 

  • Scherzinger D, Al-Babili S (2008) In vitro characterization of a carotenoid cleavage dioxygenase from Nostoc sp. PCC 7120 reveals a novel cleavage pattern, cytosolic localization and induction by highlight. Mol Microbiol 69:231–244

    Article  PubMed  CAS  Google Scholar 

  • Schiestl FP, Steinebrunner F, Schulz C, von Reuss S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’—attracting signals in fungi. Biol Lett (London, U K) 2:401–404

    CAS  Google Scholar 

  • Schimek C, Wöstemeyer J (2006) Pheromone action in the fungal groups Chytridiomycota, and Zygomycota, and in the Oomycota. In: Kues U, Fischer R (eds) The Mycota: volume I: growth, differentiation, and sexuality, 2nd edn. Springer-Verlag, New York, pp 215–231

  • Schmidt K, Pflugmacher M, Klages S, Maeser A, Mock A, Stahl DJ (2008) Accumulation of the hormone abscisic acid (ABA) at the infection site of the fungus Cercospora beticola supports the role of ABA as a repressor of plant defence in sugar beet. Mol Plant Pathol 9:661–673

    Article  PubMed  CAS  Google Scholar 

  • Scholes JD, Press MC (2008) Striga infestation of cereal crops—an unsolved problem in resource limited agriculture. Curr Opin Plant Biol 11:180–186

    Article  PubMed  Google Scholar 

  • Schulz S, Boppre M, Vanewright RI (1993) Specific mixtures of secretions from male scent organs of African milkweed butterflies (Danainae). Philos Trans R Soc B 342:161–181

    Article  CAS  Google Scholar 

  • Schuster DJ, Mueller TF, Kring JB, Price JF (1990) Relationship of the sweet-potato whitefly to a new tomato fruit disorder in Florida. HortScience 25:1618–1620

    Google Scholar 

  • Schwartz SH, Zeevaart JAD (2004) Abscisic acid biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones biosynthesis, signal transduction, action!, 3rd edn. Kluwer Academic Publishers, Boston, pp 137–155

    Google Scholar 

  • Shao Y, Spiteller D, Tang X, Ping L, Colesie C, Muenchberg U, Bartram S, Schneider B, Buedel B, Popp J, Heckel DG, Boland W (2011) Crystallization of alpha- and beta-carotene in the foregut of Spodoptera larvae feeding on a toxic food plant. Insect Biochem Mol Biol 41:273–281

    Article  PubMed  CAS  Google Scholar 

  • Shawkey MD, Morehouse NI, Vukusic P (2009) A protean palette: colour materials and mixing in birds and butterflies. J R Soc Interface 6:S221–S231

    Article  PubMed  Google Scholar 

  • Shindo Y, Witt E, Han D, Packer L (1994) Dose-response effects of acute ultraviolet-irradiation on antioxidants and molecular markers of oxidation in murine epidermis and dermis. J Invest Dermatol 102:470–475

    Article  PubMed  CAS  Google Scholar 

  • Shukolyukov SA, Saakov VS (2001) American cockroach (Periplaneta americana) synthesizes carotenoids from the precursor [C-14] mevalonic acid pyrophosphate. Biochemistry (Moscow) 66:535–540

    Article  CAS  Google Scholar 

  • Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892

    Article  PubMed  CAS  Google Scholar 

  • Smilanich AM, Mason PA, Sprung L, Chase TR, Singer MS (2011) Complex effects of parasitoids on pharmacophagy and diet choice of a polyphagous caterpillar. Oecologia 165:995–1005

    Article  PubMed  Google Scholar 

  • Sommerburg O, Langhans CD, Arnhold J, Leichsenring M, Salerno C, Crifo C, Hoffmann GF, Debatin KM, Siems WG (2003) Beta-carotene cleavage products after oxidation mediated by hypochlorous acid—a model for neutrophil-derived degradation. Free Radical Biol Med 35:1480–1490

    Article  CAS  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Article  PubMed  CAS  Google Scholar 

  • Starnecker G (1997) Hormonal control of lutein incorporation into pupal cuticle of the butterfly Inachis io and the pupal melanization reducing factor. Physiol Entomol 22:65–72

    Article  CAS  Google Scholar 

  • Stavenga DG (2006) Invertebrate photoreceptor optics. In: Warrant E, Nilsson DE (eds) Invertebrate vision. Cambridge University Press, New York, pp 1–42

    Google Scholar 

  • Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306

    Article  PubMed  CAS  Google Scholar 

  • Stevens MA (1970) Relationship between polyene carotene content and volatile compound composition of tomatoes. J Am Soc Hort Sci 95:461–464

    CAS  Google Scholar 

  • Stireman JO III, Janson EM, Carr TG, Devlin H, Abbot P (2008) Evolutionary radiation of Asteromyia carbonifera (Diptera: Cecidomyiidae) gall morphotypes on the goldenrod Solidago altissima (Asteraceae). Biol J Linn Soc 95:840–858

    Article  Google Scholar 

  • Stireman JO III, Devlin H, Carr TG, Abbot P (2010) Evolutionary diversification of the gall midge genus Asteromyia (Cecidomyiidae) in a multitrophic ecological context. Mol Phylogenet Evol 54:194–210

    Article  PubMed  Google Scholar 

  • Stratton SP, Schaefer WH, Liebler DC (1993) Isolation and identification of singlet oxygen oxidation-products of beta-carotene. Chem Res Toxicol 6:542–547

    Article  PubMed  CAS  Google Scholar 

  • Suzuki S, Nishihara M, Nakatsuka T, Misawa N, Ogiwara I, Yamamura S (2007) Flower color alteration in Lotus japonicus by modification of the carotenoid biosynthetic pathway. Plant Cell Rep 26:951–959

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Watanabe M, Takeda M (2009) UV tolerance in the two-spotted spider mite, Tetranychus urticae. J Insect Physiol 55:649–654

    Article  PubMed  CAS  Google Scholar 

  • Telfer A, Pascal A, Gall A (2008) Carotenoids in photosynthesis. In: Britton G, Liaane-Jensen S, Pfander H (eds) Carotenoids volume 4: natural functions. Birkhäuser Verlag, Boston, pp 265–308

  • Tewksbury JJ, Nabhan GP (2001) Seed dispersal—directed deterrence by capsaicin in chillies. Nature 412:403–404

    Article  PubMed  CAS  Google Scholar 

  • Tewksbury JJ, Reagan KM, Machnicki NJ, Carlo TA, Haak DC, Penaloza ALC, Levey DJ (2008) Evolutionary ecology of pungency in wild chilies. Proc Natl Acad Sci USA 105:11808–11811

    Article  PubMed  CAS  Google Scholar 

  • Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58

    Article  Google Scholar 

  • Tooker JF, De Moraes CM (2007) Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol Entomol 32:153–161

    Article  Google Scholar 

  • Tooker JF, De Moraes CM (2008) Gall insects and indirect plant defenses: a case of active manipulation? Plant Signal Behav 3:503–504

    Article  PubMed  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Van der Veen IT (2005) Costly carotenoids: a trade-off between predation and infection risk? J Evol Biol 18:992–999

    Article  CAS  Google Scholar 

  • Vasyuk VA, Andrianova TV, Musatenko LI (1996) Abscisic acid of phytopathogenic fungi Septoria tritici Rob. ex Desm. and Stagonospora nodorum (Berk.) Cast. et Germ. Ukrayins’kyi Botanichnyi Zhurnal 53:58–62

    CAS  Google Scholar 

  • Veerman A (2001) Photoperiodic time measurement in insects and mites: a critical evaluation of the oscillator-clock hypothesis. J Insect Physiol 47:1097–1109

    Article  PubMed  CAS  Google Scholar 

  • Veerman A, Veenendaal RL (2003) Experimental evidence for a non-clock role of the circadian system in spider mite photoperiodism. J Insect Physiol 49:727–732

    Article  PubMed  CAS  Google Scholar 

  • Vizarova G, Chalanyova M, Janitor A, Dugova O, Bacigalova K, Takac L (1997) Secretion of abscisic acid by hemibiotrophic fungi. Biologia 52:807–809

    CAS  Google Scholar 

  • Vogel JT, Tan BC, McCarty DR, Klee HJ (2008) The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem 283:11364–11373

    Article  PubMed  CAS  Google Scholar 

  • von Lintig J, Dreher A, Kiefer C, Wernet MF, Vogt K (2001) Analysis of the blind Drosophila mutant ninaB identifies the gene encoding the key enzyme for vitamin A formation in vivo. Proc Natl Acad Sci USA 98:1130–1135

    Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    Article  PubMed  CAS  Google Scholar 

  • Ward EWB, Cahill DM, Bhattacharyya MK (1989) Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f.sp. glycinea. Plant Physiol 91:23–27

    Article  PubMed  CAS  Google Scholar 

  • Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey NFD, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217

    Article  PubMed  CAS  Google Scholar 

  • Wei S, Hannoufa A, Soroka J, Xu N, Li X, Zebarjadi A, Gruber M (2011) Enhanced beta-ionone emission in Arabidopsis over-expressing AtCCD1 reduces feeding damage in vivo by the crucifer flea beetle. Environ Entomol 40:1622–1630

    Article  PubMed  CAS  Google Scholar 

  • Weisgraber KH, Lousberg RJ, Weiss U (1971) Chemical basis of color dimorphism of an aphid, Macrosiphum liriodendri (Monell), and a locust, Amblycorypha sp. novel carotenoids. Experientia 27:1017–1018

    Article  CAS  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Westphal E (1992) Cecidogenesis and resistance phenomena in mite-induced galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 141–156

    Google Scholar 

  • White TCR (2010) Why do many galls have conspicuous colours? An alternative hypothesis revisited. Arthropod Plant Interact 4:149–150

    Article  Google Scholar 

  • Whitney HM, Glover BJ (2007) Morphology and development of floral features recognised by pollinators. Arthropod Plant Interact 1:147–158

    Article  Google Scholar 

  • Whitney KD, Stanton ML (2004) Insect seed predators as novel agents of selection on fruit color. Ecology 85:2153–2160

    Article  Google Scholar 

  • Wilkinson DM, Sherratt TN, Phillip DM, Wratten SD, Dixon AFG, Young AJ (2002) The adaptive significance of autumn leaf colours. Oikos 99:402–407

    Article  Google Scholar 

  • Williams RN, Fickle DS, McGovern TP, Klein MG (2000) Development of an attractant for the scarab pest Macrodactylus subspinosus (Coleoptera: Scarabaeidae). J Econ Entomol 93:1480–1484

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie XN, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038

    Article  PubMed  CAS  Google Scholar 

  • Zahavi A (1975) Mate selection—selection for a handicap. J Theor Biol 53:205–214

    Article  PubMed  CAS  Google Scholar 

  • Zervoudakis G, Tairis N, Salahas G, Georgiou CD (2003) Beta-carotene production and sclerotial differentiation in Sclerotinia minor. Mycol Res 107:624–631

    Article  PubMed  CAS  Google Scholar 

  • Zheng SJ, Snoeren TAL, Hogewoning SW, van Loon JJA, Dicke M (2010) Disruption of plant carotenoid biosynthesis through virus-induced gene silencing affects oviposition behaviour of the butterfly Pieris rapae. New Phytol 186:733–745

    Article  PubMed  CAS  Google Scholar 

  • Zorn H, Langhoff S, Scheibner M, Nimtz M, Berger RG (2003) A peroxidase from Lepista irina cleaves ß, ß-carotene to flavor compounds. Biol Chem 384:1049–1056

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Jennifer L. Heath and several anonymous reviewers provided helpful comments on earlier versions of the manuscript. This work was supported by a National Science Foundation grant DEB-0614433 to JOS and the Wright State University Environmental Science PhD program.

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  1. Department of Biological Sciences, Environmental Sciences PhD Program, Wright State University, 3640 Colonel Glenn Hwy, Dayton, OH, 45435, USA

    Jeremy J. Heath, Don F. Cipollini & John O. Stireman III

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  1. Jeremy J. Heath
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  2. Don F. Cipollini
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Correspondence to Jeremy J. Heath.

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Heath, J.J., Cipollini, D.F. & Stireman III, J.O. The role of carotenoids and their derivatives in mediating interactions between insects and their environment. Arthropod-Plant Interactions 7, 1–20 (2013). https://doi.org/10.1007/s11829-012-9239-7

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