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

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

  1. 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

    CAS  Article  Google Scholar 

  2. 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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  6. 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

    PubMed  CAS  Article  Google Scholar 

  7. 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 

  8. 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

    PubMed  CAS  Article  Google Scholar 

  9. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  11. 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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  14. 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

    PubMed  CAS  Article  Google Scholar 

  15. 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 

  16. 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

    CAS  Article  Google Scholar 

  17. 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

    CAS  Article  Google Scholar 

  18. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  20. 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 

  21. 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

    PubMed  Article  Google Scholar 

  22. 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

    PubMed  Article  Google Scholar 

  23. 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

    PubMed  CAS  Article  Google Scholar 

  24. 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 

  25. 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

    Google Scholar 

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

    CAS  Article  Google Scholar 

  27. 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

    PubMed  CAS  Article  Google Scholar 

  28. 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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  30. 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 

  31. 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 

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

    PubMed  CAS  Article  Google Scholar 

  33. 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

    CAS  Article  Google Scholar 

  34. 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 

  35. 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 

  36. 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 

  37. 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 

  38. 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

    PubMed  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  41. 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

    PubMed  CAS  Article  Google Scholar 

  42. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  45. 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 

  46. 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 

  47. 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 

  48. 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

    PubMed  CAS  Article  Google Scholar 

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

    Google Scholar 

  50. 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 

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

    Google Scholar 

  52. 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

    PubMed  CAS  Article  Google Scholar 

  53. 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 

  54. 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

    PubMed  CAS  Article  Google Scholar 

  55. 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

    CAS  Article  Google Scholar 

  56. 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 

  57. 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

    Google Scholar 

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

    Article  Google Scholar 

  59. 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

    PubMed  CAS  Article  Google Scholar 

  60. 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 

  61. 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

    CAS  Article  Google Scholar 

  62. 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

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Google Scholar 

  65. 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 

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

    CAS  Article  Google Scholar 

  67. 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 

  68. 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 

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

    CAS  Article  Google Scholar 

  70. 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 

  71. 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 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Article  Google Scholar 

  76. 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

    CAS  Article  Google Scholar 

  77. 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 

  78. 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 

  79. 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 

  80. 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 

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

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  83. 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 

  84. 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 

  85. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

  88. 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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  90. 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 

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

    PubMed  CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  93. 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 

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

    Article  Google Scholar 

  95. 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 

  96. 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 

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

    Google Scholar 

  98. 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

    PubMed  Article  Google Scholar 

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

    Google Scholar 

  100. 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

    PubMed  CAS  Article  Google Scholar 

  101. 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

    PubMed  CAS  Article  Google Scholar 

  102. 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

    PubMed  CAS  Article  Google Scholar 

  103. 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 

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

    CAS  Article  Google Scholar 

  105. 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

    CAS  Article  Google Scholar 

  106. 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

    PubMed  CAS  Article  Google Scholar 

  107. 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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  110. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  112. 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

    PubMed  CAS  Article  Google Scholar 

  113. 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 

  114. 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 

  115. 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 

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

    Google Scholar 

  117. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  119. 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 

  120. 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 

  121. 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

    PubMed  CAS  Article  Google Scholar 

  122. 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 

  123. 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 

  124. 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

  125. 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

    CAS  Article  Google Scholar 

  126. 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

    PubMed  CAS  Article  Google Scholar 

  127. 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 

  128. 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 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  133. 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

    PubMed  CAS  Article  Google Scholar 

  134. 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 

  135. 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 

  136. 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

    PubMed  CAS  Article  Google Scholar 

  137. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  139. 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

    PubMed  CAS  Article  Google Scholar 

  140. 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

    PubMed  CAS  Article  Google Scholar 

  141. 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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  144. 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 

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

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  147. 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

    PubMed  CAS  Article  Google Scholar 

  148. 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 

  149. 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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  151. 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

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  153. 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

    CAS  Article  Google Scholar 

  154. 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

    PubMed  CAS  Article  Google Scholar 

  155. 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

    PubMed  CAS  Article  Google Scholar 

  156. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  158. 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

    CAS  Article  Google Scholar 

  159. 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 

  160. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  162. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  164. 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 

  165. 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

    PubMed  CAS  Article  Google Scholar 

  166. 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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  168. 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 

  169. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  171. 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

    CAS  Article  Google Scholar 

  172. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  175. 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 

  176. 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

    CAS  Article  Google Scholar 

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

    Google Scholar 

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

    CAS  Article  Google Scholar 

  179. 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 

  180. 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

    CAS  Article  Google Scholar 

  181. 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 

  182. 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

    PubMed  CAS  Article  Google Scholar 

  183. 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 

  184. 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

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    Google Scholar 

  189. 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 

  190. 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

    PubMed  CAS  Article  Google Scholar 

  191. 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 

  192. 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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  196. 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 

  197. 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 

  198. 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

    PubMed  CAS  Article  Google Scholar 

  199. 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

    CAS  Article  Google Scholar 

  200. 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

    CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  202. 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

    PubMed  CAS  Article  Google Scholar 

  203. 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 

  204. 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

  205. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  207. 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

    CAS  Article  Google Scholar 

  208. 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 

  209. 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 

  210. 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

    PubMed  CAS  Article  Google Scholar 

  211. 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

    PubMed  Article  Google Scholar 

  212. 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

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  214. 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

    PubMed  CAS  Article  Google Scholar 

  215. 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

    PubMed  Article  Google Scholar 

  216. 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

    CAS  Article  Google Scholar 

  217. 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

    PubMed  CAS  Article  Google Scholar 

  218. 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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  220. 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

    PubMed  CAS  Article  Google Scholar 

  221. 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 

  222. 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 

  223. 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

    PubMed  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  225. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  227. 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

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

    PubMed  CAS  Article  Google Scholar 

  229. 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

    PubMed  CAS  Article  Google Scholar 

  230. 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 

  231. 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 

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

    PubMed  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  234. 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

    PubMed  CAS  Article  Google Scholar 

  235. 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 

  236. 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 

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

    PubMed  CAS  Article  Google Scholar 

  238. 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

    PubMed  CAS  Article  Google Scholar 

  239. 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 

  240. 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

    PubMed  CAS  Article  Google Scholar 

  241. 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 

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

    PubMed  CAS  Article  Google Scholar 

  243. 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

    PubMed  CAS  Article  Google Scholar 

  244. 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

    PubMed  CAS  Article  Google Scholar 

  245. 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

    PubMed  CAS  Article  Google Scholar 

  246. 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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  248. 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 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  252. 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 

  253. 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

    PubMed  CAS  Article  Google Scholar 

  254. 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

    PubMed  CAS  Article  Google Scholar 

  255. 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

    PubMed  CAS  Article  Google Scholar 

  256. 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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  259. 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

    PubMed  CAS  Article  Google Scholar 

  260. 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

    PubMed  CAS  Article  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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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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Keywords

  • Apocarotenoids
  • Chemical ecology
  • Plant hormones
  • Abscisic acid
  • Strigolactones
  • Insect semiochemicals