Diverse Ecological Roles of Plant Tannins: Plant Defense and Beyond

Recent Advances in Polyphenol Research

Volumn 4, Issue , 2014, Pages 115-142

  Constabel, C Peter ^a   Yoshida, Kazuko ^a   Walker, Vincent ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Antimicrobial; Antioxidant; Plant defense; Plant stress; Polyphenols; Pro oxidant; Proanthocyanidin

Indexed keywords

ANTIOXIDANTS; ECOLOGY; FORESTRY; NETWORK SECURITY; PLANT CELL CULTURE; TANNINS;

ANTIMICROBIAL; PLANT DEFENSE; PLANT STRESS; POLYPHENOLS; PRO-OXIDANTS; PROANTHOCYANIDINS;

FLAVONOIDS;

EID: 84976370879     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118329634.ch5     Document Type: Chapter

References (174)

1. Aastrup, S., Outtrup, H. & Erdal, K. (1984) Location of the proanthocyanidins in the barley grain. Carlsberg Research Communications, 49, 105-109.
2. Adamczyk, B., Kitunen, V. & Smolander, A. (2008) Protein precipitation by tannins in soil organic horizon and vegetation in relation to tree species. Biology and Fertility of Soils, 45, 55-64.
3. Aerts, R.J., Barry, T.N. & Mcnabb, W.C. (1999) Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agriculture Ecosystems & Environment, 75, 1-12.
4. Akagi, T., Ikegami, A., Suzuki, Y., et al. (2009) Expression balances of structural genes in shikimate and flavonoid biosynthesis cause a difference in proanthocyanidin accumulation in persimmon (Diospyros kaki) fruit. Planta, 230, 899-915.
5. Akagi, T., Ikegami, A. & Yonemori, K. (2010) DkMyb2 wound-induced transcription factor of persimmon (Diospyros kaki), contributes to proanthocyanidin regulation. Planta, 232, 1045-1059.
6. Amatangelo, K.L. & Vitousek, P.M. (2009) Contrasting predictors of fern versus angiosperm decomposition in a common garden. Biotropica, 41, 154-161.
7. Anuraga, M., Duarsa, P., Hill, M. & Lovett, J. (1993) Soil moisture and temperature affect condensed tannin concentrations and growth in Lotus corniculatus and Lotus pedunculatus. Australian Journal of Agricultural Research, 44, 1667-1681.
8. Anderson, R.C., Vodovnik, M., Min, B.R., et al. (2012) Bactericidal effect of hydrolysable and condensed tannin extracts on Campylobacter jejuni in vitro. Folia Microbiologica, 57, 253-258.
9. Appel, H.M. (1993) Phenolics in ecological interactions-the importance of oxidation. Journal of Chemical Ecology, 19, 1521-1552.
10. Arnold, T.A., Tanner, C.E., Rothen, M. & Bullington, J. (2008) Wound-induced accumulations of condensed tannins in turtlegrass, Thalassia testudinum. Aquatic Botany, 89, 27-33.
11. Ascacio-Valdés, J.A., Buenrostro, J.J., De la Cruz, R., et al. (2014) Fungal biodegradation of pomegranate ellagitannins. Journal of Basic Microbiology, 54, 28-34.
12. Ayres, M.P., Clausen, T.P., Maclean, S.F., et al. (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology, 78, 1696-1712.
13. Bailey, J.K., Deckert, R., Schweitzer, J.A., et al. (2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection. Canadian Journal of Botany, 83, 356-361.
14. Baldwin, I.T., Olson, R.K. & Reiners, W.A. (1983) Protein binding phenolics and the inhibition of nitrification in subalpine balsam fir soils. Soil Biology and Biochemistry, 15, 419-423.
15. Barbehenn, R.V. & Constabel, C.P. (2011) Tannins in plant-herbivore interactions. Phytochemistry, 72, 1551-1565.
16. Barbehenn, R.V., Jones, C.P., Hagerman, A.E., et al. (2006) Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. Journal of Chemical Ecology, 32, 2253-2267.
17. Barbehenn, R.V., Jaros, A., Lee, G., et al. (2009a) Hydrolyzable tannins as "quantitative defenses": limited impact against Lymantria dispar caterpillars on hybrid poplar. Journal of Insect Physiology, 55, 297-304.
18. Barbehenn, R.V., Jaros, A., Lee, G., et al. (2009b) Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition. Oecologia, 159, 777-788.
19. Bate-Smith, E.C. & Metcalfe, C.R. (1957) Leuco-anthocyanins. 3. The nature and systematic distribution of tannins in dicotyledonous plants. Journal of the Linnean Society of London, Botany, 55, 669-705.
20. Batista, E.F., Costa, D.M., Guilhon, G. M., et al. (2011) Chemical constituents and allelopathic and antioxidant activities of Alchorneopsis floribunda Müll. Arg. (Euphorbiaceae). Natural Product Research, 25, 1-8.
21. Bending, G.D. & Read, D.J. (1996) Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biology and Biochemistry, 28, 1595-1602.
22. Berard, N.C., Wang, Y., Wittenberg, K.M., et al. (2011) Condensed tannin concentrations found in vegetative and mature forage legumes grown in western Canada. Canadian Journal of Plant Science, 91, 669-675.
23. Bernays, E.A., Chamberlain, D.J.Leather, E.M. (1981) Tolerance of acridids to ingested condensed tannin. Journal of Chemical Ecology, 7, 247-256.
24. Bindon, K.A. & Kennedy, J.A. (2011) Ripening-induced changes in grape skin proanthocyanidins modify their interaction with cell walls. Journal of Agricultural and Food Chemistry 59, 2696-2707.
25. Bindon, K.A., Smith, P.A., Holt, H.Kennedy, J.A. (2010) Interaction between grape-derived proanthocyanidins and cell wall material. 2. Implications for vinification. Journal of Agricultural and Food Chemistry 58, 10736-10746.
26. Boeckler, G.A., Towns,M., Unsicker S.B., et al. (2014) Transgenic upregulation of the condensed tannin pathway in poplar leads to dramatic shift in leaf palatability for two tree-feeding Lepidoptera. Journal of Chemical Ecology, 40, 150-158.
27. Bogs, J., Downey, M.O., Harvey, J.S., et al. (2005) Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiology, 139, 652-663.
28. Boyer, M., Bally, R., Perrotto, S., et al. (2008) A quorum-quenching approach to identify quorum-sensing-regulated functions in Azospirillum lipoferum. Research in Microbiology, 159, 699-708.
29. Bradley, R.L., Titus, B.D. & Preston, C.P. (2000) Changes to mineral N cycling and microbial communities in black spruce humus after additions of (NH4)2SO4 and condensed tannins extracted from Kalmia angustifolia and balsam fir. Soil Biology and Biochemistry, 32, 1227-1240.
30. Brandon, M.J., Foo, L.Y., Porter, L.J.Meredith, P. (1980) Proanthocyanidins of barley and sorghum; composition as a function of maturity of barley ears. Phytochemistry, 21, 2953-2957.
31. Butler, L.G. (1982) Relative degree of polymerization of sorghum tannin during seed development and maturation. Journal of Agricultural and Food Chemistry, 30, 1090-1094.
32. Cazetta, E., Schaefer, H. & Galetti, M. (2008) Does attraction to frugivores or defense against pathogens shape fruit pulp composition? Oecologia, 155, 277-286.
33. Chin, L., Leung, D.W.M. & Taylor, H.H. (2009) Lead chelation to immobilised Symphytum officinale L. (comfrey) root tannins. Chemosphere, 76, 711-715.
34. Cipollini, M.L. & Stiles, E.W. (1992) Relative risks of fungal rot for temperate ericadeous fruits-effects of seasonal variation on selection for chemical defense. Canadian Journal of Botany, 70, 1868-1877.
35. Cipollini, M.L. & Stiles, E.W. (1993) Fruit rot, antifungal defense, and palatability of fleshy fruits for frugivorous birds. Ecology, 74, 751-762.
36. Close, D.C. & McArthur, C. (2002) Rethinking the role of many plant phenolics-protection from photodamage not herbivores? Oikos, 99, 166-172.
37. Coq, S., Souquet, J.-M., Meudec, E., et al. (2010) Interspecific variation in leaf litter tannins drives decomposition in a tropical rain forest of French Guiana. Ecology, 91, 2080-2091.
38. Debeaujon, I., Peeters, A.J.M., Léon-Kloosterziel, K.M. & Koornneef, M. (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell, 13, 853-872.
39. DeGabriel, J.L.,Wallis, I.R., Moore, B.D.Foley,W.J. (2008)Asimple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia, 156, 107-116.
40. DeGabriel, J.L., Moore, B.D., Foley, W.J. & Johnson, C.N. (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology, 90, 711-719.
41. Dixon, R.A., Xie, D.-Y. & Sharma, S.B. (2005) Proanthocyanidins-a final frontier in flavonoid research? New Phytologist, 165, 9-28.
42. Donaldson, J.R., Stevens, M.T., Barnhill, H.R. & Lindroth, R.L. (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). Journal of Chemical Ecology, 32, 1415-1429.
43. Eberl, L.Riedel, K. (2011) Mining quorum sensing regulated proteins-role of bacterial cell-to-cell communication in global gene regulation as assessed by proteomics. Proteomics, 11, 3070-3085.
44. Engels, C., Knoedler, M., Zhao, Y.-Y., et al. (2009) Antimicrobial activity of gallotannins isolated from mango (Mangifera indica L.) kernels. Journal of Agricultural and Food Chemistry, 57, 7712-7718.
45. Feeny, P.P. (1968) Effect of oak leaf tannins on larval growth of winter moth Operophthera brumata. Journal of Insect Physiology, 14, 805-817.
46. Feeny, P. (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology, 51, 565-581.
47. Feucht, W., Schmid, P.P.S. & Christ E. (1986) Distribution of flavanols in meristematic and mature tissues of Prunus avium shoots. Journal of Plant Physiology, 125, 1-8.
48. Ferreira, D., Slade D. & Marais, J.P.J (2006) Flavans and pranthocyanididns. In: The Flavonoids-Chemistry, Biochemistry and Applications (eds O. M. Andersen & K. R.Markham), pp. 553-616. CRC Taylor & Francis, Boca Raton, FL.
49. Fierer, N., Schimel, J.P., Cates, R.G. & Zou, J. (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biology and Biochemistry, 33, 1827-1839.
50. Fuchs, C.T. & Spiteller, G. (1998) Accumulation of caffeoyl-D-quinic acids and catechins in plums affected by the fungus Taphrina pruni. Zeitschrift für Naturforschung, 53c, 799-805.
51. Gallet-Budynek, A., Brzostek, E., Rodgers, V.L., et al. (2009) Intact amino acid uptake by northern hardwood and conifer trees. Oecologia, 160, 129-138.
52. Grimplet, J., Deluc, L.G., Tillett, R.L., et al. (2007) Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics, 8, 187.
53. Gu, L.,Kelm,M.A., Hammerstone, J.F., et al. (2004) Concentrations of proanthocyanidins in common foods and estimations of normal consumption. The Journal of Nutrition, 134, 613-617.
54. Guyot, S., Marnet, N., Sanoner, P., et al. (2001) Direct thiolysis on crude apple materials for high-performance liquid chromatography characterization and quantification of polyphenols in cider apple tissues and juices. Methods in Enzymology, 335, 57-70.
55. Haddock E.A., Gupta, R.K., Alshafi, S.M. K., et al. (1982) The metabolism of gallic acid and hexahydroxydiphenic acid in plants. 4. Biogenic and molecular taxonomic considerations. Phytochemistry 21, 1049-1062.
56. Hagerman, A.E., Riedl, K.M., Jones, G.A., et al. (1998) High molecular weight plant polyphenolics (tannins) as biological antioxidants. Journal of Agricultural and Food Chemistry, 46, 1887-1892.
57. Halvorson, J.J., Gonzalez, J.M., Hagerman, A.E. & Smith, J.L. (2009) Sorption of tannin and related phenolic compounds and effects on soluble-N in soil. Soil Biology and Biochemistry, 41, 2002-2010.
58. Haslam, E. (1975) Natural proanthocyanidins. In: The Flavonoids (eds J. B. Harborne, T. J.Mabry & H. Mabry), pp. 505-559. Chapman and Hall, London.
59. Hatano, T., Kira, R., Yoshizaki, M. & Okuda, T. (1986) Seasonal changes in the tannins of Liquidambar formosana reflecting their biogenesis. Phytochemistry, 25, 2787-2789.
60. Hättenschwiler, S., Hagerman, A.E. & Vitousek, P. M. (2003) Polyphenols in litter from tropical montane forests across a wide range in soil fertility. Biogeochemistry, 64, 129-148.
61. Hellström, J.K., Törrönen, A.R. & Mattila, P.H. (2009) Proanthocyanidins in common food products of plant origin. Journal of Agricultural and Food Chemistry, 57, 7899-7906.
62. Holeski, L.M., Vogelzang, A., Stanosz, G. & Lindroth, R.L. (2009) Incidence of Venturia shoot blight in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochemical Systematics and Ecology, 37, 139-145.
63. Huber, B., Eberl, L., Feucht, W. & Polster, J. (2003) Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift für Naturforschung, 58c, 879-884.
64. Hwang, S.Y. & Lindroth, R.L. (1997) Clonal variation in foliar chemistry of aspen: Effects on gypsy moths and forest tent caterpillars. Oecologia, 111, 99-108.
65. Inoue, K.H. & Hagerman A.E. (1998) Determination of gallotannin with rhodanine. Analytical Biochemistry, 169, 363-369.
66. Inselsbacher, E. & Näsholm, T. (2012) The below-ground perspective of forest plants: soil provides mainly organic nitrogen for plants and mycorrhizal fungi. New Phytologist, 195, 329-334.
67. Iwashina, T. (2000) The structure and distribution of the flavonoids in plants. Journal of Plant Research, 113, 287-299.
68. Jansman, A.J.M., Verstegen, M.W. A., Huisman, J. & Vandenberg, J.W.O. (1995) Effects of hulls of faba beans (Vicia faba L.) with a low or high content of condensed tannins on the apparent ileal and fecal digestibility of nutrients and the excretion of endogenous protein in ileal digesta and feces of pigs. Journal of Animal Science, 73, 118-127.
69. Janzen, D.H. (1983) Seed and pollen dispersal by animals: convergence in the ecology of contamination and sloppy harvest. Biological Journal of the Linnean Society, 20, 103-113.
70. Jin, A., Ozga, J.A., Lopes-Lutz, D., Schieber, A. & Reinecke, D.M. (2012) Characterization of proanthocyanidins in pea (Pisum sativum L.), lentil (Lens culinaris L.), and faba bean (Vicia faba L.) seeds. Food Research International, 46, 528-535.
71. Johnson, K.S. (2005) Plant phenolics behave as radical scavengers in the context of insect (Manduca sexta) hemolymph and midgut fluid. Journal of Agricultural and Food Chemistry, 53, 10120-10126.
72. Kaal, J., Nierop, K.G. J. & Verstraten, J.M. (2005) Retention of tannic acid and condensed tannin by Fe-oxide-coated quartz sand. Journal of Colloid and Interface Science, 287, 72-79.
73. Kamachi, H., Komori, I., Tamura, H., et al. (2005) Lead tolerance and accumulation in the gametophytes of the fern Athyrium yokoscense. Journal of Plant Research, 118, 137-145.
74. Kanerva, S., Kitunen, V., Kiikkilä, O., et al. (2006) Response of soil C and N transformations to tannin fractions originating from Scots pine and Norway spruce needles. Soil Biology and Biochemistry, 38, 1364-1374.
75. Kanerva, S., Kitunen, V., Loponen, J. & Smolander, A. (2008) Phenolic compounds and terpenes in soil organic horizon layers under silver birch, Norway spruce and Scots pine. Biology and Fertility of Soils, 44, 547-556.
76. Kao, Y.Y., Harding, S.A. & Tsai, C.J. (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiology, 130, 796-807.
77. Karowe, D.N. (1989) Differential effect of tannic acid on two tree-feeding Lepidoptera-implications for theories of plant anti-herbivore chemistry. Oecologia, 80, 507-512.
78. Kennedy, J.A., Matthews, M.A. & Waterhouse, A.L. (2002) Effect of maturity and vine water status on grape skin and sine flavonoids. American Journal of Enology and Viticulture, 53, 268-274.
79. Kinraide, T.B. & Hagermann, A.E. (2010) Interactive intoxicating and ameliorating effects of tannic acid, aluminum (Al3+), copper (Cu2+), and selenate (SeO4 2-) in wheat roots: a descriptive and mathematical assessment. Physiologia Plantarum, 139, 68-79.
80. Koponen, J.M., Happonen, A.M.,Mattila, P.H.Törrönen, A.R. (2007) Contents of anthocyanins and ellagitannins in selected foods consumed in Finland. Journal of Agricultural and Food Chemistry, 55, 1612-1619.
81. Kraus, T.E.C., Dahlgren, R.A. & Zasoski, R.J. (2003) Tannins in nutrient dynamics of forest ecosystems - a review. Plant and Soil, 256, 41-66.
82. Kraus, T.E.C., Zasoski, R.J. & Dahlgren, R.A. (2004a) Fertility and pH effects on polyphenol and condensed tannin concentrations in foliage and roots. Plant and Soil, 262, 95-109.
83. Kraus, T.E.C., Zasoski, R.J., Dahlgren, R.A., et al. (2004b) Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biology and Biochemistry, 36, 309-321.
84. Kurokawa, H., Peltzer, D.A. & Wardle, D.A. (2010) Plant traits, leaf palatability and litter decomposability for co-occurring woody species differing in invasion status and nitrogen fixation ability. Functional Ecology, 24, 513-523.
85. Laitinen, M.-L., Julkunen-Tiitto, R. & Rousi, M. (2002) Foliar phenolic composition of European white birch during bud unfolding and leaf development. Physiologia Plantarum, 114, 450-460.
86. Landete, J.M. (2011) Ellagitannins, ellagic acid and their derived metabolites: A review about source, metabolism, functions and health. Food Research International, 44, 1150-1160.
87. Lattanzio, V., Terzano, R., Cicco, N., et al. (2005) Seed coat tannins and bruchid resistance in stored cowpea seeds. Journal of the Science of Food and Agriculture, 85, 839-846.
88. Lavola, A. (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiology, 18, 53-58.
89. Lees, G.L., Suttill, N.H. & Gruber, M.Y. (1993) Condensed tannins in sainfoin.1. A histological and cytological survey of plant tissues. Canadian Journal of Botany, 71, 1147-1152.
90. Lees, G.L., Suttill, N.H., Wall, K.M. & Beveridge, T.H. (1995) Localization of condensed tannins in apple fruit peel, pulp, and seeds. Canadian Journal of Botany, 73, 1897-1904.
91. Lepiniec, L., Debeaujon, I., Routaboul, J.-M., et al. (2006) Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology, 57, 405-430.
92. Lim, C.K., Penesyan, A., Hassan, K.A., et al. (2013) Effect of tannic acid on the transcriptome of the soil bacterium Pseudomonas protegens Pf-5. Applied and Environmental Microbiology, 79, 3141-3145.
93. Lin, B., Johnson, B.J., Rubin, R.A., et al. (2011) Iron chelation by cranberry juice and its impact on Escherichia coli growth. Biofactors, 37, 121-130.
94. Lindroth, R.L., Osier, T.L., Barnhill, H.R.H. & Wood, S.A. (2002) Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochemical Systematics and Ecology, 30, 297-307.
95. Lorenz, K., Preston, C.M., Raspe, S., et al. (2000) Litter decomposition and humus characteristics in Canadian and German spruce ecosystems: information from tannin analysis and 13C CPMAS NMR. Soil Biology and Biochemistry, 32, 779-792.
96. Ma, Y. & Bliss, F.A. (1978) Tannin content and inheritance in common bean. Crop Science, 18, 201-204.
97. Madritch, M.D. & Lindroth, R.L. (2011) Soil microbial communities adapt to genetic variation in leaf litter inputs. Oikos, 120, 1696-1704.
98. Madritch, M., Donaldson, J.R. & Lindroth, R.L. (2006) Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems, 9, 528-537.
99. Maie, N., Behrens, A., Knicker, H. & Kögel-Knabner, I. (2003) Changes in the structure and protein binding ability of condensed tannins during decomposition of fresh needles and leaves. Soil Biology and Biochemistry, 35, 577-589.
100. Martin, J.S., Martin, M.M. & Bernays, E.A., (1987) Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. Journal of Chemical Ecology, 13, 605-621.
101. McArt, S.H., Spalinger, D.E., Collins, W.B., et al. (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology, 90, 1400-1411.
102. McDonald, M., Mila, I. & Scalbert, A. (1996) Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation. Journal of Agricultural and Food Chemistry, 44, 599-606.
103. McKenzie, B.E. & Peterson, C.A. (1995) Root browning in Pinus banksiana and Eucalyptus pilularis Sm.1. Anatomy and permeability of the white and tannin zones. Botanica Acta, 108, 127-137.
104. McSweeney, C.S., Palmer, B., McNeill, D.M. & Krause, D.O. (2001) Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology, 91, 83-93.
105. Mellway, R.D., Tran, L.T., Prouse, M.B., et al. (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiology, 150, 924-941.
106. Mila, I., Scalbert, A. & Expert, D. (1996) Iron withholding by plant polyphenols and resistance to pathogens and rots. Phytochemistry, 42, 1551-1555.
107. Min, B.R., Attwood, G.T., Reilly, K., et al. (2002) Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep. Canadian Journal of Microbiology, 48, 911-921.
108. Min, B.R., Barry, T.N., Attwood, G.T. & McNabb, W.C. (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology, 106, 3-19.
109. Mingshu, L., Kai, Y., Qiang, H., & Dongying, J. (2006) Biodegradation of gallotannins and ellagitannins. Journal of Basic Microbiology, 46, 68-84.
110. Miranda, M., Ralph, S.G., Mellway, R., et al. (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Molecular Plant-Microbe Interactions, 20, 816-831.
111. Mueller-Harvey, I. (2001) Analysis of hydrolysable tannins. Animal Feed Science and Technology, 91, 3-20.
112. Mole, S. (1993) The systematic distribution of tannins in the leaves of angiosperms: A tool for ecological studies. Biochemical Systematics and Ecology, 21, 833-846.
113. Näsholm, T., Ekblad, A., Nordin, A., et al. (1998) Boreal forest plants take up organic nitrogen. Nature, 392, 914-916.
114. Nelson, K.E., Pell, A.N., Doane, P.H., et al. (1997) Chemical and biological assays to evaluate bacterial inhibition by tannins. Journal of Chemical Ecology, 23, 1175-1194.
115. Nierop, K., Verstraten, J., Tietema, A., et al. (2006a) Short- and long-term tannin induced carbon, nitrogen and phosphorus dynamics in Corsican pine litter. Biogeochemistry, 79, 275-296.
116. Nierop, K.G.J., Preston, C.M. & Verstraten, J.M. (2006b) Linking the B ring hydroxylation pattern of condensed tannins to C, N and P mineralization. A case study using four tannins. Soil Biology and Biochemistry, 38, 2794-2802.
117. Norris, C.E., Preston, C.M., Hogg, K.E. & Titus, B.D. (2011) The influence of condensed tannin structure on rate ofmicrobial mineralization and reactivity to chemical assays. Journal of Chemical Ecology, 37, 311-319.
118. Northup, R.R., Yu, Z.S., Dahlgren, R.A. & Vogt, K.A. (1995) Polyphenol control of nitrogen release from pine litter. Nature, 377, 227-229.
119. O'May, C. & Tufenkji, N. (2011) The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials. Applied EnvironmentalMicrobiology, 77, 3061-3067.
120. Oates, J.F., Swain, T. & Zantovska, J. (1977) Secondary compounds and food selection by colobus monkeys. Biochemical Systematics and Ecology, 5, 317-321.
121. Okuda, T., Yoshida, T., Hatano, T. & Ito, H. (2009) Ellagitannins renewed the concept of tannins. In: Chemistry and Biology of Ellagitannins (ed. S. Quideau), pp. 1-54. World Scientific, Singapore.
122. Osawa, H., Endo, I., Hara, Y., et al. (2011) Transient proliferation of proanthocyanidin-accumulating cells on the epidermal apex contributes to highly aluminum-resistant root elongation in camphor tree. Plant Physiology, 155, 433-46.
123. Osier, T.L.Lindroth, R.L. (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. Journal of Chemical Ecology, 27, 1289-1313.
124. Osier, T.L. & Lindroth, R.L. (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia, 148, 293-303.
125. Peng, S., Scalbert, A. & Monties, B. (1991) Insoluble ellagitannins in Castanea sativa and Quercus petraea woods. Phytochemistry, 30, 775-778.
126. Peters, D.J. & Constabel, C.P. (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant Journal, 32, 701-712.
127. Peterson, C.A., Enstone, D.E. & Taylor, J.H. (1999) Pine root structure and its potential significance for root function. Plant and Soil, 217, 205-213.
128. Porter, L.J. (1988). Flavans and proanthocyanidins. In: The Flavonoids-Recent Advances in Research Since 1980 (ed. J.B. Harborne), pp. 21-62. Chapman & Hall, London.
129. Porter, L.J., Hrstich, L.N. & Chan, B.G. (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphidin. Phytochemistry, 25, 223-230.
130. Pourcel, L., Routaboul, J.-M., Kerhoas, L., et al. (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell, 17, 2966-2980.
131. Prior, R.L.Gu, L. (2005) Occurrence and biological significance of proanthocyanidins in the American diet. Phytochemistry, 66, 2264-80.
132. Prior, R.L., Lazarus, S.A., Cao, G., et al. (2001) Identification of procyanidins and anthocyanins in blueberries and cranberries (Vaccinium spp.) using high-performance liquid chromatography/mass spectrometry. Journal of Agricultural and Food Chemistry, 49, 1270-1276.
133. Puupponen-Pimiä, R.,Nohynek, L., Hartmann-Schmidlin, S., et al. (2005) Berry phenolics selectively inhibit the growth of intestinal pathogens. Journal of Applied Microbiology, 98, 991-1000.
134. Quideau, S., Deffieux, D., Douat-Casassus, C. & Pouysegu, L. (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angewandte Chemie International Edition, 50, 586-621.
135. Rasmussen, S.E., Frederiksen, H., Krogholm, K.S. & Poulsen, L. (2005) Dietary proanthocyanidins: occurrence, dietary intake, bioavailability, and protection against cardiovascular disease. Molecular Nutrition & Food Research, 49, 159-174.
136. Rawat, M.S.M., Pant, G., Prasad, D., et al. (1998) Plant growth inhibitors (Proanthocyanidins) from Prunus armeniaca. Biochemical Systematics and Ecology, 26, 13-23.
137. Rehill, B.J.,Whitham, T.G., Martinsen, G.D., et al. (2006) Developmental trajectories in cottonwood phytochemistry. Journal of Chemical Ecology, 32, 2269-2285.
138. Sakaguchi, T. & Nakajima, A. (1994) Accumulation of uranium by immobilized persimmon tannin. Separation Science and Technology, 29, 205-221.
139. Salminen, J.-P., Karonen, M. & Sinkkonen, J. (2011) Chemical ecology of tannins: recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chemistry-A European Journal, 17, 2806-2816.
140. Santos-Buelga, C. & Scalbert, A. (2000) Proanthocyanidins and tannin-like compounds-nature, occurrence, dietary intake and effects on nutrition and health. Journal of the Science of Food and Agriculture, 80, 1094-1117.
141. Scalbert, A. (1991) Antimicrobial properties of tannins. Phytochemistry, 30, 3875-3883.
142. Schaefer, H.M., Schmidt, V. & Winkler, H. (2003) Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos, 102, 318-328.
143. Schimel, J.P., Cleve, K.V., Cates, R.G., et al. (1996) Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: implications for changes in N cycling during succession. Canadian Journal of Botany, 74, 84-90.
144. Schimel, J.P., Cates, R.G. & Ruess, R. (1998) The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga. Biogeochemistry, 42, 221-234.
145. Schmidt, M.A., Kreinberg, A.J., Gonzalez, J.M., et al. (2013) Soil microbial communities respond differently to three chemically defined polyphenols. Plant Physiology and Biochemistry, 72, 190-197.
146. Schofield, P., Mbugua, D.M. & Pell, A.N. (2001) Analysis of condensed tannins: a review. Animal Feed Science and Technology, 91, 21-40.
147. Schweitzer, J.A., Bailey, J.K., Rehill, B.J., et al. (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecology Letters, 7, 127-134.
148. Schweitzer, J.A., Madritch, M.D., Bailey, J.K., et al. (2008) From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems, 11, 1005-1020.
149. Schweitzer, J.A., Fischer, D.G., Rehill, B.J., et al. (2011) Forest gene diversity is correlated with the composition and function of soil microbial communities. Population Ecology, 53, 35-46.
150. Scioneaux, A.N., Schmidt,M.A., Moore, M.A., et al. (2011) Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key. Journal of Chemical Ecology, 37, 57-70.
151. Shimada, T. (2006) Salivary proteins as a defense against dietary tannins. Journal of Chemical Ecology, 32, 1149-1163.
152. Shimada, T., Saitoh, T., Sasaki, E., et al. (2006) Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. Journal of Chemical Ecology, 32, 1165-1180.
153. Sivakumaran, S.,Molan, A.L., Meagher, L.P., et al. (2004) Variation in antimicrobial action of proanthocyanidins from Dorycnium rectum against rumen bacteria. Phytochemistry, 65, 2485-2497.
154. Smith, A.H., Zoetendal, E. & Mackie, R.I. (2005) Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microbial Ecology, 50, 197-205.
155. Smolander, A., Loponen, J., Suominen, K. & Kitunen, V. (2005) Organic matter characteristics and C and N transformations in the humus layer under two tree species, Betula pendula and Picea abies. Soil Biology & Biochemistry, 37, 1309-1318.
156. Souquet, J.-M., Cheynier, V., Brossaud, F. & Moutounet, M. (1996) Polymeric proanthocyanidins from grape skins. Phytochemistry, 43, 509-512.
157. Souquet, J.-M., Labarbe, B., Le Guernevé, C., et al. (2000) Phenolic composition of grape stems. Journal of Agricultural and Food Chemistry, 48, 1076-1080.
158. Stark, S., Julkunen-Tiitto, R. & Kumpula, J. (2007) Ecological role of reindeer summer browsing in the mountain birch (Betula pubescens ssp. czerepanovii) forests: effects on plant defense, litter decomposition, and soil nutrient cycling. Oecologia, 151, 486-498.
159. Stoutjesdijk, P.A., Sale, P.W. & Larkin, P.J. (2001) Possible involvement of condensed tannins in aluminium tolerance of Lotus pedunculatus. Australian Journal of Plant Physiology, 28, 1063-1074.
160. Strumeyer, D.H. & Malin, M.J. (1975) Condensed tannins in grain sorghum. Isolation, fractionation, and characterization. Journal of Agricultural and Food Chemistry, 23, 909-914.
161. Taganna, J.C., Quanico, J.P., Perono, R.M., et al. (2011) Tannin-rich fraction from Terminalia catappa inhibits quorum sensing (QS) in Chromobacterium violaceum and the QS-controlled biofilm maturation and LasA staphylolytic activity in Pseudomonas aeruginosa. J Ethnopharmacology, 134, 865-871.
162. Takahashi, A., Ichihara, Y., Isagi, Y.Shimada, T. (2010) Effects of acorn tannin content on infection by the fungus Ciboria batschiana. Forest Pathology, 40, 96-99.
163. Takos, A.M., Ubi, B.E., Robinson, S.P. Walker, A.R. (2006) Condensed tannin biosynthesis genes are regulated separately from other flavonoid biosynthesis genes in apple fruit skin. Plant Science, 170, 487-499.
164. Tarascou, I., Souquet, J.M.,Mazauric, J.P., et al. (2010) The hidden face of food phenolic composition. Archives of Biochemistry and Biophysics, 501, 16-22.
165. Thibault, J.R., Fortin, J.A. & Smirnoff,W.A. (1982) in vitro allelopathic inhibition of nitrification by balsam poplar and balsam fir. American Journal of Botany, 69, 676-679.
166. Vander Wall, S.B. (2001) The evolutionary ecology of nut dispersal. Botanical Review, 67, 74-117.
167. Wallis, I.R., Edwards, M.J., Windley, H., et al. (2012) Food for folivores: nutritional explanations linking diets to population density. Oecologia, 169, 281-291.
168. Whitham, T.G., Bailey, J.K., Schweitzer, J.A., et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics, 7, 510-523.
169. Wrangham, R.W. Waterman, P.G. (1983) Condensed tannins fruits eaten by chimpanzees. Biotropica, 15, 217-222.
170. Yoneda, S. & Nakatsubo, F. (1998) Effects of the hydroxylation patterns and degrees of polymerization of condensed tannins on their metal-chelating capacity. Journal of Wood Chemistry and Technology, 18, 193-205.
171. Yoshida, T., Hatano, T., Ito, H. & Okuda, T. (2009) Structural diversity and antimicrobial activities of ellagitannins. In: Chemistry and Biology of Ellagitannins (ed. S. Quideau), pp. 55-93. World Scientific, Singapore.
172. Zhou, H.-C., Lin, Y.-M.,Wei, S.-D.Tam, N.F.Y. (2011) Structural diversity and antioxidant activity of condensed tannins fractionated from mangosteen pericarp. Food Chemistry, 129, 1710-1720.
173. Zhou, H.C., Tam, N.F.Y., Lin, Y.M., et al. (2012) Changes of condensed tannins during decomposition of leaves of Kandelia obovata in a subtropical mangrove swamp in China. Soil Biology & Biochemistry, 44, 113-121.
174. Zifkin, M., Jin, A., Ozga, J.A., et al. (2012) Gene expression and metabolite profiling of developing highbush blueberry (Vaccinium corymbosum L.) fruit indicates transcriptional regulation of flavonoidmetabolism and activation of abscisic acidmetabolism. Plant Physiology, 158, 200-224.