Specific Polyphenols and Tannins are Associated with Defense Against Insect Herbivores in the Tropical Oak Quercus oleoides

Journal of Chemical Ecology

Volumn 40, Issue 5, 2014, Pages 458-467

  Moctezuma, Coral ^a   Hammerbacher, Almuth ^b   Heil, Martin ^c   Gershenzon, Jonathan ^b   Méndez Alonzo, Rodrigo ^d   Oyama, Ken ^a,e  

^a INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS Y SUSTENTABILIDAD   (Mexico)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSTITUTO DE MATEMÁTICAS   (Mexico)

Author keywords

Flavan 3 ols; Flavonol glycosides; Herbivory; Hydrolyzable tannins; Plant insect interactions; Polyphenols

Indexed keywords

ALCOHOL; ANTIHERBIVORE DEFENSE; CHEMICAL DEFENSE; DAMAGE; DECIDUOUS TREE; GALL; INSECT; PHENOLIC COMPOUND; PLANT-HERBIVORE INTERACTION; TANNIN;

COSTA RICA; MEXICO [NORTH AMERICA];

AGROMYZIDAE; HEXAPODA; QUERCUS OLEOIDES;

POLYPHENOL; TANNIN DERIVATIVE;

ANIMAL; CHEMISTRY; HERBIVORY; HOST PARASITE INTERACTION; INSECT; METABOLISM; OAK; PARASITOLOGY; PHYSIOLOGY; PLANT LEAF;

ANIMALS; HERBIVORY; HOST-PARASITE INTERACTIONS; INSECTS; PLANT LEAVES; POLYPHENOLS; QUERCUS; TANNINS;

EID: 84902197909     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-014-0431-3     Document Type: Article

References (66)

1. Adams JM, Zhang Y (2009) Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America. J Ecol 97: 933-940.
2. Adams JM, Rehill B, Zhang Y, Gower J (2008) A test of the latitudinal defense hypothesis: herbivory, tannins and total phenolics in four North American tree species. Ecol Res 24: 697-704.
3. Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen JP (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338: 113-116.
4. Appel HM, Govenor HL, D'Ascenzo M, Siska E, Schultz JC (2001) Limitations of Folin assays of foliar phenolics in ecological studies. J Chem Ecol 27: 761-778.
5. Arámbula-Salazar JA, Ibarra-Salinas BI, González-Laredo RF, Muñoz-Galindo OD, Hernández-Vela H (2010) Seasonal variation in the phenolic content of oak leaves (Quercus sideroxyla) in different soil textures. Madera y Bosques 16: 49-59.
6. Ayres MP, Clausen TP, Maclean SFJ, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78: 1696-1712.
7. Baptist F, Zinger L, Clement JC, Gallet C, Guillemin R, Martins JM, Sage L, Shahnavaz B, Choler P, Geremia R (2008) Tannin impacts on microbial diversity and the functioning of alpine soils: a multidisciplinary approach. Environ Microbiol 10: 799-809.
8. Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72: 1551-1565.
9. Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen JP (2006) Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. J Chem Ecol 32: 2253-2267.
10. Barbehenn RV, Weir Q, Salminen J-P (2008a) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34: 748-56.
11. Barbehenn RV, Maben RE, Knoester JJ (2008b) Linking phenolic oxidation in the midgut lumen with oxidative stress in the midgut tissues of a tree-feeding caterpillar Malacosoma disstria (Lepidoptera: Lasiocampideae). Environ Entomol 37: 1113-1118.
12. Barrett LG, Heil M (2012) Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci 17: 282-292.
13. Bernays EA (1981) Plant tannins and insect herbivores: an appraisal. Ecol Entomol 6: 353-360.
14. Bernays EA, Chamberlain DJ (1980) A study of tolerance of ingested tannin in Schistocerca gregaria. J Insect Physiol 26: 415-420.
15. Bernays EA, Chamberlain D, Mccarthy P (1980) The differential effects of ingested tannic acid on different species of Acridoidea. Entomol Exp Appl 28: 158-166.
16. Bernays EA, Howard JJ, Champagne D, Estesen BJ (1991) Rutin: a phagostimulant for the polyphagous acridid Schistocerca americana. Entomol Exp Appl 60: 19-28.
17. Bricchi I, Leitner M, Foti M, Mithöfer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232: 719-729.
18. Cavender-Bares JM, González-Rodríguez A, Pahlich A, Koehler K, Deacon N (2011) Phylogeography and climatic niche evolution in live oaks (Quercus series Virentes) from the tropics to the temperate zone. J Biogeogr 38: 962-981.
19. Close DC, Mcarthur C (2002) Rethinking the role of many plant phenolics - protection from photodamage not herbivores? Oikos 99: 166-172.
20. Close DC, Mcarthur C, Paterson S, Fitzgerald H, Walsh A (2003) Photoinhibition: a link between the effects of the environment of Eucalyptus leaf chemistry and herbivory. Ecology 84: 2952-2966.
21. Close DC, Mcarthur C, Hagerman AE, Fitzgerald H (2005) Differential distribution of leaf chemistry in eucalypt seedlings due to variation in whole-plant nutrient availability. Phytochemistry 66: 215-221.
22. Courtois EA, Baraloto C, Paine CET, Petronelli P, Blandinieres PA, Stien D, Höuel E, Bessière JM, Chave J (2012) Differences in volatile terpene composition between the bark and leaves of tropical tree species. Phytochemistry 82: 81-88.
23. Cranshaw W (2004) Garden Insects of North America: The ultimate guide to backyard bugs. Princeton Press, WA.
24. Daglia M (2012) Polyphenols as antimicrobials agents. Curr Opin Biotechnol 23: 174-181.
25. Duffey SS (1980) Sequestration of natural products by insects. Annu Rev Entomol 25: 447-477.
26. Faeth SH (1985) Quantitative defense theory and patterns of feeding by oak insects. Oecologia 68: 34-40.
27. Feeny PP (1969) Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin. Phytochemistry 8: 2119-2126.
28. Feeny PP (1970) Seasonal changes in oak leave tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51: 565-581.
29. Forkner RE, Marquis RJ, Lill JT (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29: 174-187.
30. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nature Chemical Biology 3: 408-414.
31. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55: 481-504.
32. Haslam E (1998) Practical Polyphenolics: from structure to molecular recognition and physiological action. UK, Cambridge.
33. Haslam E (2007) Vegetable tannins - Lessons of a phytochemical lifetime. Phytochemistry 68: 2713-2721.
34. Heil M (2009) Damaged-self recognition in plant herbivore defence. Trends Plant Sci 14: 356-363.
35. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25: 137-144.
36. Heil M, Baumann B, Andary C, Linsenmair KE, Mckey D (2002) Extraction and quantification of "condensed tannins" as a measure of plant anti-herbivore defence? Revisiting an old problem. Naturwissenschaften 89: 519-524.
37. Heil M, Ibarra-Laclette E, Adame-Álvarez RM, Martínez O, Ramírez-Chavez E, Molina-Torres J, Herrera-Estrella L (2012) How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces Octadecanoid signaling. PLoS ONE 7: e30537. doi: 10. 1371/journal. pone. 0030537.
38. Johnson MTJ, Agrawal AA, Maron JL, Salminen J-P (2009) Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. J Evol Biol 22: 1295-1307.
39. Karban R, Shiojiri K (2009) Self-recognition affects plant communication and defense. Ecol Lett 12: 502-506.
40. Kashiwada Y, Nonaka GI, Nishioka I, Chang JJ, Lee KH (1992) Tannins and related compounds as selective cytotoxic agents. J Nat Prod 55: 1033-1043.
41. Kelm MA, Johnson JC, Robbins RJ, Hammerstone JF, Schmitz HH (2006) High-performance liquid chromatography separation and purification of cacao (Theobroma cacao L.) procyanidins according to degree of polymerization using a diol stationary phase. J Agric Food Chem 54: 1571-1576.
42. Khennouf S, Amira S, Arrar L, Baghiani A (2010) Effect of some phenolic compounds and Quercus tannins on lipid peroxidation. World Appl Sci J 8: 1144-1149.
43. König M, Scholz E, Hartmann R, Lehmann W, Rimpler H (1994) Ellagitannins and complex tannins from Quercus petraea bark. J Nat Prod 57: 1411-1415.
44. Makarenkov V, Legendre P (2002) Non linear redundancy analysis and canonical correspondence analysis based on polynomial regression. Ecology 83: 1146-1161.
45. Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and UV-B -responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150: 924-941.
46. Moles AT, Wallis IR, Foley WJ et al (2011a) Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytol 191: 777-788.
47. Moles AT, Bonser S, Poorel AGB, Wallis IR, Foley W (2011b) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25: 380-388.
48. Mueller-Harvey I (2001) Analysis of hydrolyzable tannins. Anim Feed Sci Technol 91: 3-20.
49. Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47: 57-92.
50. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: Community Ecology Package. R package version 1. 17-4 .
51. Pearce G, Yamaguchi Y, Barona G, Ryan CA (2010) A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107: 14921-14925.
52. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32: 701-712.
53. Quideau S, Deffieux D, Douat-Casassus C, Pouységu L (2011) Plant polyphenols: Chemical properties, biological activities, and synthesis. Angew Chem Int 50: 586-621.
54. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www. R-project. org/.
55. Rey D, Pautou M-P, Meyran J-C (1999) Histopathological effects of tannic acid on the midgut epithelium of some aquatic Diptera larvae. J Invertebr Pathol 73: 173-181.
56. Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68: 98-107.
57. Roslin T, Salminen J-P (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117: 1560-1568.
58. Ryan KG, Swinny EE, Markham KR, Winefield C (2002) Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry 59: 23-32.
59. Salminen J-P, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25: 325-338.
60. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14: 17781-17811.
61. Scioneaux AN, Schmidt MA, Moore MA, Lindroth RA, Wooley SC, Hagerman AE (2011) Qualitative variation in proanthocyanidin composition of Populus species and hybrids: Genetics is the key. J Chem Ecol 37: 57-50.
62. Thelen GC, Vivanco JM, Newingham B, Good W, Bais HP, Landres P, Caesar A, Callaway RM (2005) Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol Lett 8: 209-217.
63. Valencia S (2004) Diversidad del género Quercus (Fagaceae) en México. B Soc Bot Mex 75: 33-53.
64. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, UK.
65. Yarnes CT, Boecklen WJ, Salminen J-P (2008a) No simple sum: seasonal variation in tannin phenotypes and leaf-miners in hybrid oaks. Chemoecology 18: 39-51.
66. Yarnes CT, Boecklen WJ, Touminen K, Salminen J-P (2008b) Hybridization affects seasonal variation of phytochemical phenotypes in an oak hybrid complex (Quercus gambelii x Quercus grisea). Int J Plant Sci 169: 567-578.