Phytochemistry Reviews

, Volume 14, Issue 3, pp 367–380 | Cite as

New advances in chemical defenses of plants: researches in calceolariaceae

  • Carlos L. Cespedes
  • Pedro M. Aqueveque
  • José G. Avila
  • Julio Alarcon
  • Isao Kubo


Evidences about the biosynthesis of secondary metabolites from plants point to constitutive or induce chemical defense generated for protection against to different phytopathogenic attack. Calceolaria spp. is regarded both as a notorious weed and as a popular ornamental garden plant and have medicinal application. Some taxa of the America distributed Calceolaria genus are toxic to insects, fungi and several bacteria strains, and its effect has been associated with the presence of phenolics. Calceolaria spp. produces a number of iridoids, flavonoids, naphthoquinones and phenylpropanoids that have been shown to possess interesting biological activities. All these aspects are considered in this review to allow an evaluation of the potential for utilization of the large biodiversity of Calceolaria available. An up-to-date of the phytochemistry and biological activities of several members of the Calceolariaceae family is show. New iridoids, flavonoids and phenylpropanoids for these Calceolaria species have been isolated, identified and tested for their antifeedant, igr, insecticidal, antimicrobial, anticancer, proteinase, tyrosinase, and acetylcholinesterase inhibitory activities. Until now mixtures of flavonoids have been found to be potent insecticides and fungicides, followed by phenylpropanoids mixtures and iridoids showed to be antifeedant and in some cases repellent and attractant. Dose-dependent experiments shows that flavonoids are insecticidal against S. frugiperda and D. melanogaster at early growth stages. Bactericidal and fungicidal activity showed that dunnione (a naphthoquinone) have potent activity as fungistatic and fungicidal. O-methylflavonols, and different mixtures of them were very effective fungistatic. However, fungistatic quercetin and dunnione both combined with sublethal amount of kaempferol and gallic acid showed a strong fungicidal activity against phytopathogenic strains. Additionally, naphthoquinones possess a promissory activity as anticancer.


Biological activity Calceolariaceae Naphthoquinones Insecticidal Antimicrobial Anticancer 



The authors are indebted to M.Sc. Evelyn Muñoz (Phytochemical Ecology Lab, Basic Sciences Dept., Faculty of Sciences, University of Bio Bio, Chillan, Chile) for technical assistance with the antioxidant assay and for the help in performing many insect feeding assays. To Prof. Ana Ma. Garcıa-Bores (Laboratorio de Fitoquimica, Unidad UBIPRO, FES-Iztacala, UNAM, Mexico DF, Mexico) for proteinase assays and performing antimicrobial assay in part. To Prof. David S. Seigler, Ph.D. (Emeritus Professor, Department of Plant Biology, and Curator, Herbarium of University of Illinois at Urbana-Champaign) for identification of the plant samples. CLC is grateful to CONICYT Chile through FONDECYT Program, grants # 1101003 and # 1130242 for financial support in part. IK and CLC are grateful to UC Berkeley-Chile Seed Funds for grant. This paper is based on work supported by grants from the Comision Nacional de Investigacion Cientifica y Tecnologica de Chile (CONICYT), through FONDECYT Program grants 1101003 and 1130242.


  1. Akhtar Y, Isman MB (2013) Plant natural products for pest management: the magic of mixtures. In: Ishaaya I, Reddy Palli S, Rami Horowitz A (eds) Advanced technologies for managing insect pests. Springer, Netherland, pp 231–247Google Scholar
  2. Akhtar Y, Yeoung YR, Isman MB (2008) Comparative bioactivity of selected extracts from Meliaceae and some commercial botanical insecticides against two noctuid caterpillars, Trichoplusia ni and Pseudaletia unipuncta. Phytochem Rev 7:77–88Google Scholar
  3. Akhtar Y, Isman MB, Lee Ch-H, Lee S-G, Lee H-S (2012) Toxicity of quinones against two-spotted spider mite and three species of aphids in laboratory and green house conditions. Ind Crops Prod 37(1):536–541Google Scholar
  4. Alout H, Labbe P, Berthomieu A, Djogbenou L, Leonetti J-P, Fort Ph, Weill M (2012) Novel AChE inhibitors for sustainable insecticide resistance management. PLoS-ONE 7(10): e47125,1–8. doi: 10.1371/journal.pone.0047125
  5. Anderson S (2006) On the phylogeny of the genus Calceolaria (Calceolariaceae) as inferred from ITS and plastid matK sequences. Taxon 55(1):125–137Google Scholar
  6. Berenbaum MR (1989) North American ethnobotanicals as sources of novel-plant based insecticides. In: Arnason JT, Philogene BJR, Morand P (eds) Insecticides of plant origin. ACS symposium series. American Chemical Society, Washington, vol 387, pp 11–24)Google Scholar
  7. Berenbaum MR (1990) Evolution of specialization. In insect-umbellifer associations. Annu Rev Entomol 35:319–343Google Scholar
  8. Berenbaum MR (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. J Chem Ecol 28(5):873–896PubMedGoogle Scholar
  9. Bowers MD (1981) Unpalatability as a defense strategy of western checkerspot butterflies (Euphydrias Scudder, Nymphalidae). Evolution 35(2):367–375Google Scholar
  10. Bravo HR, Copaja SV, Figueroa-Duarte S, Lamborot M, San Martin J (2005) 1,4-Benzoxazin-3-one, 2-benzoxazolinone and Gallic acid from Calceolaria thyrsiflora Graham and their antibacterial activity. Z Naturforsch C 60(5/6):389–393PubMedGoogle Scholar
  11. Bruckner K, Bozic D, Manzano D, Papaefthimiou D, Pateraki I, Scheler U, Ferrer A, de Vos RCH, Kanellis AK, Tissier A (2014) Characterization of two genes for the biosynthesis of abietane-type diterpenes in rosemary (Rosmarinus officinalis) glandular trichomes. Phytochemistry 101:52–64PubMedGoogle Scholar
  12. Calderón JS, Cespedes CL, Rosas R, Gomez-Garibay F, Salazar JR, Lina L, Aranda E, Kubo I (2001) Acetylcholinesterase and insect growth inhibitory activities of Gutierrezia microcephala on fall armyworm Spodoptera frugiperda J. E. Smith. Z. Naturforschung 56c: 382–394Google Scholar
  13. Cao J, Xia X, Dai X, Xiao J, Wang Q, Andrae-Marobela K, Okatch H (2013) Flavonoids profiles, antioxidant, acetylcholinesterase inhibition activities of extract from Dryoathyrium boryanum (Willd.) Ching. Food Chem Toxicol 55:121–128PubMedGoogle Scholar
  14. Capanoglu E (2010) The potential of priming in food production. Trends Food Sci Technol 21:399–407Google Scholar
  15. Casida JE (2009) Pest toxicology: the primary mechanisms of pesticide action. Chem Res Toxicol 22:609–619PubMedGoogle Scholar
  16. Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Ann Rev Entomol 58:99–117 Google Scholar
  17. Cespedes CL, Calderón J, Lina L, Aranda E (2000) Growth inhibitory effects on fall armyworm Spodoptera frugiperda of some limonoids isolated from Cedrela spp. (Meliaceae). J Agric Food Chem 48:1903–1908Google Scholar
  18. Céspedes CL, Alarcón J, Aranda E, Becerra J, Silva M (2001a) Insect growth regulatory and insecticidal activity of b-dihydroagarofurans from Maytenus spp. (Celastraceae). Z Naturforsch C 56c:603–613Google Scholar
  19. Céspedes CL, Martínez-Vázquez M, Calderón JS, Salazar JR, Aranda E (2001b) Insect growth regulatory activity of some extracts and compounds from Parthenium argentatum on fall armyworm Spodoptera frugiperda. Z Naturforsch C 56c:95–105Google Scholar
  20. Cespedes CL, Avila JG, Marin JC, Domínguez M, Torres P, Aranda E (2006) Natural compounds as antioxidant and molting inhibitors can play a role as a model for search of new botanical pesticides. In: Rai M, Carpinella MC (eds) Naturally occurring bioactive compounds. Advances in phytomedicine series, vol 3. Elsevier, The Netherlands, pp 1–27Google Scholar
  21. Cespedes CL, Muñoz E, Lamilla L, Molina SF, Alarcon J (2013a) Insect growth regulatory, molting disruption and insecticidal activity of Calceolaria talcana (Calceolariaceae: Scrophulariaceae) and Condalia microphylla Cav@ (Rhamnaceae), Chapter 15. In: Cespedes CL, Sampietro DA, Seigler DS, Rai MK (eds) Natural antioxidants and biocides from wild medicinal plants. Cabi Publishing, WallingfordGoogle Scholar
  22. Cespedes CL, Muñoz E, Salazar JR, Yamaguchi L, Werner E, Alarcón J, Kubo I (2013b) Inhibition of cholinesterase activity by extracts, fractions and compounds from Calceolaria talcana and C. integrifolia (Calceolariaceae: Scrophulariaceae). Food Chem Toxicol 62:919–926PubMedGoogle Scholar
  23. Cespedes CL, Salazar JR, Alarcón J (2013c) Chemistry and biological activities of Calceolaria spp. (Calceolariaceae: Scrophulariaceae). Phytochem Rev 12:733–749Google Scholar
  24. Cespedes CL, Salazar JR, Ariza-Castolo A, Yamaguchi L, Avila JG, Aqueveque P, Kubo I, Alarcon J (2014) Biopesticides from plants: calceolaria integrifolia s.l. Environ Res 132:391–406PubMedGoogle Scholar
  25. Colombo PS, Flamini G, Christodoulou MS, Rodondi G, Vitalini S, Passarella D, Fico G (2014) Farinose alpine primula species: phytochemical and morphological investigations. Phytochemistry 98:151–159PubMedGoogle Scholar
  26. Conner WE, Boada R, Schroeder, FC, Gonzalez A, Meinwald J, Eisner T (2000) Chemical defense: bestowal of a nuptial alkaloidal garment by a male moth on its mate. Proc Nat Acad Sci 97(26):14406–14411Google Scholar
  27. Cosacov A, Sérsic AN, Sosa V, De-Nova JA, Nylinder S, Cocucci AA (2009) New insights into the phylogenetic relationships, character evolution, and phytogeographic patterns of Calceolaria (Calceolariaceae). Am J Bot 96(12):2240–2255PubMedGoogle Scholar
  28. Crombie L (1999) Natural product chemistry and its part in the defense against insects and fungi in agriculture. Pestic Sci 55:761–774Google Scholar
  29. De la Cruz H, Vilcapoma G, Zevallos PA (2007) Ethnobotanical study of medicinal plants used by the Andean people of Canta, Lima. Peru J Ethnopharmacol 111(2):284–294Google Scholar
  30. De la Cruz MG, Malpartida SB, Santiago HB, Jullian V, Bourdy G (2014) Hot and cold: Medicinal plant uses in Quechua speaking communities in the high Andes (Callejón de Huaylas, Ancash, Perú). J Ethnopharmacol 155(2):1093–1117PubMedGoogle Scholar
  31. Di Fabio A, Bruni A, Poli F, Garbarino JA, Chamy MC, Piovano M, Nicoletti M (1995) The distribution of phenylpropanoid glycosides in Chilean Calceolaria spp. Biochem Syst Ecol 23(2):179–182Google Scholar
  32. Domínguez M, Nieto A, Marín JC, Keck A-S, Jeffery E, Cespedes CL (2005) Antioxidant activities of extracts from Barkleyanthus salicifolius (Asteraceae) and Penstemon gentianoides (Scrophulariaceae). J Agric Food Chem 53:5889–5895PubMedGoogle Scholar
  33. Domínguez M, Marín JC, Esquivel B, Cespedes CL (2007) Pensteminoside, an unusual catalpol-type iridoid from Penstemon gentianoides HBK (Plantaginaceae). Phytochemistry 68:1762–1766PubMedGoogle Scholar
  34. Domínguez M, Keck AS, Jeffery EH, Cespedes CL (2010) Effects of extracts, flavonoids and iridoids from Penstemon gentianoides (Plantaginaceae) on inhibition of inducible nitric oxide synthase (iNOS), cyclooxygenase-2 (COX-2) in LPS-Activated RAW 264.7 macrophage cells and their antioxidant activity. Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas 9(5):397–413Google Scholar
  35. Ehrhart Ch (2000) Die gattung Calceolaria (Scrophulariaceae) in Chile. Biblioth Bot H 153:1–283Google Scholar
  36. Ehrhart Ch (2005) The Chilean Calceolaria integrifolia s.l. species complex (Scrophulariaceae). Syst Bot 30:383–411Google Scholar
  37. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608Google Scholar
  38. Eisner T, Eisner M, Aneshansley DJ, Wu CL, Meinwald J (2000) Chemical defense of the mint plant, Teucrium marum (Labiatae). Chemoecology 10(4):211–216Google Scholar
  39. Engler A (1964) Sillabus der Pflanzenfamilien. Melchio H (ed) Berlin, Borntrager, vol II, p 451Google Scholar
  40. Falcão DQ, Costa ER, Alviano DS, Alviano CS, Kuster RM, Menezes FS (2006) Atividade antioxidante e antimicrobiana de Calceolaria chelidonioides Humb. Bonpl Kunth Braz J Pharmacog 16(1):73–76Google Scholar
  41. Falcão DQ, Costa ER, Kuster RM, Nielloud F, Vian L, Menezes FS (2007) Evaluation of cytotoxicity, phototoxicity and genotoxicity from Calceolaria chelidonioides (Scrophulariaceae) flowers ethanol extract. Plant Med pp 73–77Google Scholar
  42. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci 87:7713–7716PubMedCentralPubMedGoogle Scholar
  43. Feeny PP (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical Interactions between Plants and Insects. Plenum Press, New York, pp 1–40Google Scholar
  44. Feijo de Souza J, Carvalho M, Trevisan D, Schmitz W, Saridakis H (2004) Phenolic compounds and hydroxymethylfurfural from the flowers of Caesalpinia peltophoroides and their antibacterial activity. Rev Latinoamer Quim 32:25–29Google Scholar
  45. Feng RY, Chen WK, Isman MB (1995) Synergism of malathion and inhibition of midgut esterase activities by an extract from Melia toosendan (Meliaceae). Pestic Biochem Physiol 53:34–41Google Scholar
  46. Feyereisen R (1995) Molecular biology of insecticide resistance. Toxicol Lett 82(83):83–90PubMedGoogle Scholar
  47. Fournier D, Mutero A (1994) Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 108(1):19–31Google Scholar
  48. Garbarino JA, Chamy MC, Piovano M (2000) Chemistry of the Calceolaria genus. Structural and biological aspects. Molecules 5(3):302–303Google Scholar
  49. Garbarino JA, Chamy MC, Piovano M, Espinoza L, Belmonte E (2004) Diterpenoids from Calceolaria inamoena. Phytochemistry 65(7):903–908PubMedGoogle Scholar
  50. Garbarino JA, Cardile V, Lombardo L, Chamy MC, Piovano M, Russo A (2007) Demalonyl thyrsiflorin A, a semisynthetic labdane-derived diterpenoid, induces apoptosis and necrosis in human epithelial cancer cells. Chem Biol Interact 169(3):198–206PubMedGoogle Scholar
  51. González JA, Estevez-Braun A (1998) Effect of E-chalcone on potato-cyst nematodes (Globodera pallida and G. rostochiensis). J Agric Food Chem 46:1163–1165Google Scholar
  52. Gonzalez-Coloma A, Gutierrez C, Cabrera R, Reina M (1997) Silphinene derivatives: their effects and modes of action on Colorado potato Beetle. J Agric Food Chem 45:946–950Google Scholar
  53. Green BT, Welch KD, Panter KE, Lee ST (2013) Plant toxins that affect nicotinic acetylcholine receptors: a review. Chem Res Toxicol 26(8):1129–1138 PubMedGoogle Scholar
  54. Guerrero A, Rosell G (2005) Biorational approaches for insect control by enzymatic inhibition. Curr Med Chem 12:461–469Google Scholar
  55. Harborne J, Baxter H (2001) Chemical dictionary of economic plants. Wiley, ChichesterGoogle Scholar
  56. Heath JJ, Kessler A, Woebbe E, Cipollini D, Stireman JO (2014) Exploring plant defense theory in tall goldenrod, Solidago altissima. New Phytol 202:1357–1370PubMedGoogle Scholar
  57. Hutcheson SW (1998) Current concepts of active defense in plants. Annu Rev Phytopathol 36:59–80PubMedGoogle Scholar
  58. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66PubMedGoogle Scholar
  59. Isman MB, Akthar Y (2007) Plant natural products as a source for developing environmentally acceptable insecticides. In: Ishaaya I, Nauen R, Horowitz AR (eds) Insecticides design using advanced technologies. Springer, Berlin, pp 235–248Google Scholar
  60. Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19(3):140–145PubMedGoogle Scholar
  61. Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43(10):885–895PubMedGoogle Scholar
  62. Kakuta H, Seki T, Hashidoko Y, Mizutani J (1992) Ent-kaurenic acid and its related compounds from glandular trichome exudate and leaf extracts of Polymnia sonchifolia. Bioscience Biotechnol Biochem 56:1562–1564Google Scholar
  63. Kantzanou M, Tassios PT, Tseleni-Kotsovili A, Legakis LJ, Vatopoulos AC (1999) Reduced susceptibility to vancomycin of nosocomial isolates of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 43(5):729–731PubMedGoogle Scholar
  64. Keane S, Ryan MF (1999) Purification, characterization, and inhibition by monoterpenes of acetylcholinesterase from the waxmoth, Galleria mellonella (L.). Insect Biochem Mol Biol 29:1097–1104Google Scholar
  65. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Ann Rev Plant Biol 53:299–328Google Scholar
  66. Khambay BPS, Jewess PJ (2000) The potential of natural naphthoquinones as the basis for a new class of pest control agents: an overview of research at IACR-Rothamsted. Crop Prot. 19(8/10):597–601Google Scholar
  67. Khambay BPS, Batty D, Cahill M, Denholm I, Mead-Briggs M, Vinall S, Niemeyer HM, Simmonds MSJ (1999) Isolation, characterization, and biological activity of naphthoquinones from Calceolaria andina L. J Agric Food Chem 47(2):770–775PubMedGoogle Scholar
  68. Khambay BPS, Batty D, Jewess PJ, Bateman GL, Holloman DW (2003) Mode of action and pesticidal activity of the natural product dunnione and of some analogues. Pest Manag Sci 59(2):174–182PubMedGoogle Scholar
  69. Kubo I (1997) Tyrosinase inhibitors from plants. In: Hedin P, Hollingworth R, Masler E, Miyamoto J, Thompson D (eds) Phytochemicals for pest control. ACS symposium series 658, American Chemical Society, Washington, pp 310–326Google Scholar
  70. Kubo I, Klocke A, Asano S (1981) Insect ecdysis inhibitors from the east African medicinal plant Ajuga remota (Labiatae). Agric Biol Chem 45:1925–1927Google Scholar
  71. Kubo I, Muroi H, Himejima M (1993) Combination effects of antifungal nagilactones against Candida albicans and two other fungi with phenylpropanoids. J Nat Prod 56:220–226PubMedGoogle Scholar
  72. Kubo I, Kinst-Hori I, Chauduri SK, Kubo Y, Sánchez Y, Ogura T (2000) Flavonols from Heterotheca inuloides: tyrosinase inhibitory activity and structural criteria. Bioorg Med Chem 8:1749–1755PubMedGoogle Scholar
  73. Kubo I, Chen Q-X, Nihei KI, Calderón JS, Cespedes CL (2003a) Tyrosinase inhibition kinetics of anisic acid. Z Naturforsch C 58c:713–718Google Scholar
  74. Kubo I, Kinst-Hori I, Nihei KI, Soria F, Takasaki M, Calderón JS, Cespedes CL (2003b) Tyrosinase inhibitors from galls of Rhus javanica leaves and their effects on insects. Z Naturforsch C 58c:719–725Google Scholar
  75. Leon E, Guillen Z, Felix LM, Chavez J, Martinez R (2009) Parasitemy of Trypanosoma cruzi in Mus musculus and preliminary in vitro study of the trypanocidal action of two species of Calceolaria in Peru. Revista de Investigacion de la Universidad Norbert Wiener, year 2009:81–88Google Scholar
  76. Li Sh, Shao M-W, Lu Y-H, Kong L-Ch, Jiang D-H, Zhang Y-L (2014) Phytotoxic and antibacterial metabolites from Fusarium proliferatum ZS07 isolated from the gut of long-horned grasshoppers. J Agric Food Chem 62:8997–9001PubMedGoogle Scholar
  77. Macía MJ, García E, Vidaurre PJ (2005) An ethnobotanical survey of medicinal plants commercialized in the markets of La Paz and El Alto, Bolivia. J Ethnopharmacol 97(2):337–350PubMedGoogle Scholar
  78. Marin JC, Cespedes CL (2007) Compuestos volatiles de plantas. Origen, emisión, efectos, análisis y aplicaciones al agro [Volatile compounds from plant. Origin, emissions, effects, analysis and agro applications]. Rev Fitotec Mex 30(4):327–351Google Scholar
  79. Mayhuasca O, Bonilla P, Ballon M, Ferreira M, Carrasco E (2007) Efecto antiinflamatorio en ratones de extractos de Calceolaria tripartita R&P, comparación fitoquimica con el extracto hidroalcoholico de Calceolaria melissifolia Bentham [Antiinflammatory effect in mice of extracts of Calceolaria tripartita R&P, compared phytochemical with the hydroalcoholic extract of Calceolaria melissifolia Bentham. Ciencia e Investigacion [Facultad de Farmacia y Bioquimica, UNMSM] 10(2): 71–80Google Scholar
  80. Meinwald J (2001) Sex, violence and drugs in the world of insects: a chemist’s view. Science 5:80–92Google Scholar
  81. Marticorena C, Quezada M (1985) Catalogo de la flora vascular de Chile. Gayana Bot 42:1–157Google Scholar
  82. Mercado MI, Coll MV, Grau A, Catalan CAN (2010) New acyclic diterpenic acids from Yacon (Smallanthus sonchifolius) leaves. Nat Prod Commun 5:1721–1726 Google Scholar
  83. Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant-herbivore chemical interactions. Trends Plant Sci 19(1):29–35PubMedGoogle Scholar
  84. Mithofer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450PubMedGoogle Scholar
  85. Molau U (1988) Scrophulariaceae: part I. Calceolarieae. Flora Neotropica 47:1–326Google Scholar
  86. Molau U (2003) Two new species of Calceolaria (Scrophulariaceae) from the tropical Andes. Novon 13:101–103Google Scholar
  87. Montes M (1987) Aspectos de la medicación popular en la región del Bío Bío. Acta Bonaerense 6:115–124Google Scholar
  88. Montes M, Wilkomirsky T (1978) Plantas chilenas en medicina popular: Ciencia y Folklore. Universidad de Concepción, Concepción, Chile, Escuela de Química y Farmacia y BioquímicaGoogle Scholar
  89. Moreira X, Lundborg L, Zas R, Carrillo-Gavilan A, Borg-Karlson AK, Sampedro L (2013) Inducibility of chemical defenses by two chewing insect herbivores in pine trees is specific to targeted plant tissue, particular herbivore and defensive trait. Phytochemistry 94:113–122PubMedGoogle Scholar
  90. Morello A, Pavani M, Garbarino JA, Chamy MC, Frey C, Mancilla J, Guerrero A, Repetto Y, Ferreira J (1995) Effects and mode of action of 1,4-naphthoquinones isolated from Calceolaria sessilis on tumoral cells and Trypanosoma parasites. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 112C(2):119–128Google Scholar
  91. Mullin ChA, Gonzalez-Coloma A, Gutierrez C, Reina M, Eichenseer H, Hollister B, Chyb S (1997) Antifeedant effects of some novel terpenoids on chrysomelidae Beetles: comparisons with alkaloids on an alkaloid-adapted and nonadapted species. J Chem Ecol 23:1851–1866Google Scholar
  92. Muñoz O, Montes M, Wilkomirsky T (2001) Plantas medicinales de uso en Chile, química y farmacología. Editorial Universitaria. Universidad de Chile. Vicerrectoría de Asuntos Académicos. Santiago, ChileGoogle Scholar
  93. Muñoz E, Lamilla C, Marin JC, Alarcon J, Cespedes CL (2013a) Antifeedant, insect growth regulatory and insecticidal effects of Calceolaria talcana (Calceolariaceae) on Drosophila melanogaster and Spodoptera frugiperda. Ind Crop Prod 42:137–144Google Scholar
  94. Muñoz E, Escalona D, Salazar JR, Alarcon J, Cespedes CL (2013b) Insect growth regulatory effects by diterpenes from Calceolaria talcana Grau & Ehrhart (Calceolariaceae: Scrophulariaceae) against Spodoptera frugiperda and Drosophila melanogaster. Ind Crop Prod 45:283–292Google Scholar
  95. Muñoz E, Avila JG, Alarcón J, Kubo I, Cespedes CL (2013c) Tyrosinase inhibitors from Calceolaria integrifolia s.l.: Calceolaria talcana aerial parts. J Agric Food Chem 61:4336–4343PubMedGoogle Scholar
  96. Muñoz MA, Chamy C, Bucio MA, Hernandez-Barragan A, Joseph-Nathan P (2014) Absolute configuration of scopadulane diterpenes from Calceolaria species. Tetrahed Lett 55:4274–4277Google Scholar
  97. Nicoletti M, Galeffi C, Messana I, Garbarino JA, Gambaro V, Nyandat E, Marini-Bettolo GB (1986) New phenylpropanoid glucosides from Calceolaria hypericina. Gazz Chim Ital 116(8):431–433Google Scholar
  98. Nicoletti M, Galeffi C, Messana I, Marini-Bettolo GB, Garbarino JA, Gambaro V (1988a) Studies in Calceolaria genus. Part 2. Phenylpropanoid glycosides from Calceolaria hypericina. Phytochemistry 27(2):639–641Google Scholar
  99. Nicoletti M, Galeffi C, Multari G, Garbarino JA, Gambaro V (1988b) Studies on the genus Calceolaria. Part 3. Polar constituents of Calceolaria ascendens. Planta Med 54(4):347–348PubMedGoogle Scholar
  100. Ortego F, Rodriguez B, Castañera P (1995) Effects of neo-clerodane diterpenes from Teucrium on feeding behavior of Colorado potato beetle larvae. J Chem Ecol 21:1375–1386PubMedGoogle Scholar
  101. Ortego F, López-Olguín J, Ruíz M, Castanera P (1999) Effects of toxic and deterrent terpenoids on digestive protease and detoxication enzyme activities of Colorado potato beetle larvae. Pestic Biochem Physiol 63:76–84Google Scholar
  102. Pang YP, Brimijoin S, Ragsdale DW, Zhu KY, Suranyi R (2012) Novel and viable acetyl- cholinesterase target site for developing effective and environmentally safe insecticides. Curr Drug Targets 13:471–482PubMedCentralPubMedGoogle Scholar
  103. Passi S, Nazzaro-Porro M (1981) Molecular basis of substrate and inhibitory specificity of tyrosinase: phenolic compounds. Brit J Dermatol 104(6):659–665Google Scholar
  104. Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochemistry 10:168–213Google Scholar
  105. Rhodes SHL, Fitzmaurice AG, Cockburn M, Bronstein JM, Sinsheimer JS, Ritz B (2013) Pesticides that inhibit the ubiquitin-proteasome system: effect measure modification by genetic variation in SKP1 in Parkinson’s disease. Environ Res 126:1–8PubMedGoogle Scholar
  106. Rosner D, Markowitz G (2013) Persistent pollutants: a brief history of the discovery of the widespread toxicity of chlorinated hydrocarbons. Environ Res 120:126–133PubMedGoogle Scholar
  107. Ryan JD (1979) Proteinase inhibitors. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 599–618Google Scholar
  108. Sachetti G, Romagnoli C, Nicoletti M, Di Fabio A, Bruni A, Poli F (1999) Glandular trichomes of Calceolaria adscendens Lidl. (Scrophulariaceae): histochemistry, development and ultrastructure. Ann Bot 83:87–92Google Scholar
  109. Serrano A, Palacios C, Roy G, Cespon C, Villar ML, Nocito M, Gonzalez-Porque P (1998) Derivatives of gallic acid induce apoptosis in tumoral cell lines and inhibit lymphocyte proliferation. Arch Biochem Biophys 350:49–54PubMedGoogle Scholar
  110. Simmonds MSJ, Blaney WM, Esquivel B, Rodriguez-Hahn L (1996) Effect of clerodane-type diterpenoids isolated from Salvia spp on the feeding behaviour of Spodoptera littoralis. Pestic Sci 47:17–23Google Scholar
  111. Simmonds MSJ, Manlove JD, Blaney WM, Khambay BPS (2002) Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporariorum and the parasitoid Encarsia formosa. Entomol Exp Appl 102:39–47Google Scholar
  112. Singh ShB, Graham PL, Reamer RA, Cordingley MG (2001) Discovery, total synthesis, HRV 3C-protease inhibitory activity, and structure-activity relationships of 2-methoxystypandrone and its analogues. Bioorg Med Chem Lett 11:3143–3146PubMedGoogle Scholar
  113. Singh-Ratan R (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920Google Scholar
  114. Swain T (1979) Tannins and lignins. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 657–682Google Scholar
  115. Takemoto K, Kamisuki Sh, Chia PTh, Kuriyama I, Mizushina Y, Sugawara F (2014) Bioactive Dihydronaphthoquinone Derivatives from Fusarium solani. J Nat Prod. doi: 10.1021/np500175j Google Scholar
  116. Tene V, Malagón O, Finzi PV, Vidari G, Armijos C, Zaragoza T (2007) An ethnobotanical survey of medicinal plants used in Loja and Zamora-Chinchipe, Ecuador. J Ethnopharmacol 111(1):63–81PubMedGoogle Scholar
  117. Thomas E, Vandebroek I, Sanca S, Van Damme P (2009) Cultural significance of medicinal plant families and species among Quechua farmers in Apillapampa, Bolivia. J Ethnopharmacol 122(1):60–67PubMedGoogle Scholar
  118. Torres P, Ávila JG, Romo de Vivar A, García AM, Marín JC, Aranda E, Cespedes CL (2003) Antioxidant and insect growth regulatory activities of stilbenes and extracts from Yucca periculosa. Phytochemistry 64:463–473PubMedGoogle Scholar
  119. Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of the metamorphosis in insects. Annual Rev Entomol 47:467–500Google Scholar
  120. Valladares G, Defago MT, Palacios SM, Carpinella MC (1997) Laboratory evaluationof Melia azedarach (Meliaceae) extracts against the elm leaf beetle (Coleoptera:Chrysomelidae). J Econ Entomol 90:747–750Google Scholar
  121. Woldemichael GM, Waechter G, Singh MP, Maiese WM, Timmermann BN (2003) Antibacterial diterpenes from Calceolaria pinifolia. J Nat Prod 66(2):242–246PubMedGoogle Scholar
  122. Wollenweber E, Mann K, Roitman JN (1989) Flavonoid aglycons excreted by three Calceolaria species. Phytochemistry 28(8):2213–2214Google Scholar
  123. Xie Y, Isman MB, Feng Y, Wong A (1993) Diterpene resin acids: major active principles in tall oil against variegated cutworm, Peridroma saucia (Lepidoptera: Noctuidae). J Chem Ecol 19:1075–1084PubMedGoogle Scholar
  124. Yamane H, Konno K, Sabelis M, Takabayashi J, Sassa T, Oikawa H (2010) Chemical defence and toxins of plants. In: Mander L, Lui H-W (eds) Comprehensive natural products ii chemistry and biology, vol 4. Elsevier, Oxford, pp 339–385Google Scholar
  125. Zhu F, Poelman EH, Dicke M (2014) Insect herbivore-associated organisms affect plant responses to herbivory. New Phytol. doi: 10.1111/nph.12886 PubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Carlos L. Cespedes
    • 1
  • Pedro M. Aqueveque
    • 2
  • José G. Avila
    • 3
  • Julio Alarcon
    • 4
  • Isao Kubo
    • 5
  1. 1.Laboratorio de Bioquimica Vegetal y Fitoquimica-Ecologica, Grupo de Investigación: Química y Biotecnología de Productos Naturales Bioactivos, Departamento de Ciencias Básicas, Facultad de CienciasUniversidad del Bio BioChillanChile
  2. 2.Laboratorio de Micología Aplicada, Departamento de Agroindustrias, Facultad de Ingeniería AgrícolaUniversidad de ConcepciónChillanChile
  3. 3.Laboratorio de FitoquímicaUBIPRO, FES-Iztacala UNAMTlalnepantlaMexico
  4. 4.Laboratorio de Sintesis y Biotransformación de Productos Naturales, Grupo de Investigación: Química y Biotecnología de Productos Naturales Bioactivos. Departamento de Ciencias Básicas, Facultad de CienciasUniversidad del Bio BioChillanChile
  5. 5.Chemical Ecology Lab., ESPM DepartmentUniversity of California at BerkeleyBerkeleyUSA

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