Các polyphenol và tannin đặc hiệu liên quan đến khả năng phòng vệ chống lại côn trùng ăn lá ở cây sồi nhiệt đới Quercus oleoides

Journal of Chemical Ecology - Tập 40 - Trang 458-467 - 2014
Coral Moctezuma1, Almuth Hammerbacher2, Martin Heil3, Jonathan Gershenzon2, Rodrigo Méndez-Alonzo4, Ken Oyama1,5
1Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México (UNAM), Morelia, Mexico
2Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
3Departamento de Ingeniería Genética, CINVESTAV - Irapuato, Irapuato, Mexico
4Department of Ecology and Evolutionary Biology, University of California, Los Angeles, USA
5Escuela Nacional de Estudios Superiores Unidad Morelia, UNAM, Morelia, Mexico

Tóm tắt

Vai trò của các polyphenol thực vật như một cơ chế phòng ngừa chống lại côn trùng ăn lá vẫn còn gây tranh cãi. Chúng tôi đã kết hợp các nghiên cứu hiện trường tương quan trên ba khu vực địa lý (Bắc Mexico, Nam Mexico và Costa Rica) với các thí nghiệm cảm ứng trong điều kiện kiểm soát để tìm kiếm các hợp chất ứng cử viên có thể đóng vai trò phòng vệ trong lá của cây sồi nhiệt đới, Quercus oleoides. Chúng tôi đã định lượng mức độ hư hại của lá do bốn nhóm côn trùng ăn lá (côn trùng cắn, côn trùng ăn lõi, côn trùng đào hầm và côn trùng tạo u) và phân tích nội dung của 18 polyphenol (bao gồm tannin thủy phân, flavan-3-ol và flavonol glycoside) trong cùng một tập hợp lá bằng phương pháp sắc ký lỏng hiệu năng cao và sắc ký khối. Mức độ hư hại lá dao động từ hai đến tám phần trăm theo từng khu vực, và gần 90% tổng mức hư hại là do côn trùng cắn. Hư hại do côn trùng cắn có mối tương quan dương với acutissimin B, catechin, và dimer catechin, trong khi hư hại do côn trùng đào hầm có mối tương quan dương với mongolinin A. Ngược lại, sự hiện diện của u lại có mối tương quan âm với vescalagin và acutissimin B. Bằng cách sử dụng phân tích thừa, chúng tôi tìm kiếm các tổ hợp polyphenol liên quan đến sự ăn lá tự nhiên: tổ hợp mongolinin A và acutissimin B có sự liên quan cao nhất đến ăn lá. Trong một thí nghiệm vườn chung với cây sồi non, hư hại nhân tạo làm tăng nội dung của acutissimin B, mongolinin A và vescalagin, trong khi nội dung của catechin giảm. Các polyphenol đặc hiệu, ​​có thể là riêng lẻ hoặc trong tổ hợp, thay vì tổng lượng polyphenol, đã được liên kết với mức độ hư hại lá hiện hữu ở cây sồi nhiệt đới này. Các nghiên cứu trong tương lai nhằm hiểu vai trò sinh thái của polyphenol có thể sử dụng các nghiên cứu tương quan tương tự để xác định các hợp chất ứng cử viên có thể được sử dụng độc lập và trong các tổ hợp có ý nghĩa sinh học trong các thử nghiệm với côn trùng ăn lá và các tác nhân gây bệnh.

Từ khóa

#polyphenol #tannin #Quercus oleoides #côn trùng ăn lá #sinh học thực vật #sinh thái học

Tài liệu tham khảo

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 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 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 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 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 Ayres MP, Clausen TP, Maclean SFJ, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712 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 Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565 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 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 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 Barrett LG, Heil M (2012) Unifying concepts and mechanisms in the specificity of plant–enemy interactions. Trends Plant Sci 17:282–292 Bernays EA (1981) Plant tannins and insect herbivores: an appraisal. Ecol Entomol 6:353–360 Bernays EA, Chamberlain DJ (1980) A study of tolerance of ingested tannin in Schistocerca gregaria. J Insect Physiol 26:415–420 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 Bernays EA, Howard JJ, Champagne D, Estesen BJ (1991) Rutin: a phagostimulant for the polyphagous acridid Schistocerca americana. Entomol Exp Appl 60:19–28 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 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 Close DC, Mcarthur C (2002) Rethinking the role of many plant phenolics - protection from photodamage not herbivores? Oikos 99:166–172 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 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 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 Cranshaw W (2004) Garden Insects of North America: The ultimate guide to backyard bugs. Princeton Press, WA Daglia M (2012) Polyphenols as antimicrobials agents. Curr Opin Biotechnol 23:174–181 Duffey SS (1980) Sequestration of natural products by insects. Annu Rev Entomol 25:447–477 Faeth SH (1985) Quantitative defense theory and patterns of feeding by oak insects. Oecologia 68:34–40 Feeny PP (1969) Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin. Phytochemistry 8:2119–2126 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 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 Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nature Chemical Biology 3:408–414 Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504 Haslam E (1998) Practical Polyphenolics: from structure to molecular recognition and physiological action. UK, Cambridge Haslam E (2007) Vegetable tannins – Lessons of a phytochemical lifetime. Phytochemistry 68:2713–2721 Heil M (2009) Damaged-self recognition in plant herbivore defence. Trends Plant Sci 14:356–363 Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144 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 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 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 Karban R, Shiojiri K (2009) Self-recognition affects plant communication and defense. Ecol Lett 12:502–506 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 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 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 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 Makarenkov V, Legendre P (2002) Non linear redundancy analysis and canonical correspondence analysis based on polynomial regression. Ecology 83:1146–1161 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 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 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 Mueller-Harvey I (2001) Analysis of hydrolyzable tannins. Anim Feed Sci Technol 91:3–20 Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92 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 <http://cran.r-project.org/web/packages/vegan> 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 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 Quideau S, Deffieux D, Douat-Casassus C, Pouységu L (2011) Plant polyphenols: Chemical properties, biological activities, and synthesis. Angew Chem Int 50:586–621 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/ 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 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 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 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 Salminen J-P, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338 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 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 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 Valencia S (2004) Diversidad del género Quercus (Fagaceae) en México. B Soc Bot Mex 75:33–53 Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, UK 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 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