Geographical and within-population variation of constitutive chemical defences in a Mediterranean oak (Quercus ilex)
Abstract
Aim of study: to assess whether constitutive levels of total phenols and condensed tannins acting as chemical defences in Quercus ilex vary across regions, populations and genotypes.
Area of study: acorns from six Spanish regions with natural presence of Q. ilex were collected for later sowing in the greenhouse of the University of Extremadura at Plasencia, western Spain.
Materials and methods: 1176 acorns from 12 populations (2 per region) were sown according to a nested design (6 regions x 2 populations/region x 7 genotypes/population). After five months, 588 emerged seedlings were harvested for phenol extraction from their leaves. Quantification of total phenols through the Folin-Ciocalteu method and condensed tannins by Porter's reagent method was carried out.
Main results: total phenolics and condensed tannins correlated positively. Significant differences were found for the concentration of total phenolics and condensed tannins among regions and among genotypes, but not among populations within regions. The lowest levels of constitutive defences were found in the northern Iberian Peninsula. Also, the defensive phenolic content was significantly higher in regions with acidic soils. Heritability values (total phenols 0.37±0.08 and condensed tannins 0.48±0.36) were lower than those obtained of total tannins in a previous study.
Research highlights: constitutive levels of heritable chemical defences in holm oak significantly depend on their geographical origin and genotype.
Keywords: condensed tannins, genetic and latitudinal variability, heritability, total phenolics.
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References
Abdala-Roberts L, Moreira X, Rasmann S, Parra-Tabla V, Mooney KA, 2016. Test of biotic and abiotic correlates of latitudinal variation in defenses in the perennial herb Ruellia nudiflora. J Ecol 104 (2): 580-590. https://doi.org/10.1111/1365-2745.12512
Abdala-Roberts L, Galmán A, Petry W, Covelo F, De la Fuente M, Glauser G, Moreira X, 2018. Interspecific variation in leaf functional and defensive traits in oak species and its underlying climatic drivers. PloS One 13(8) e0202548. https://doi.org/10.1371/journal.pone.0202548
Agrawal AA, Heil M, 2012. Synthesizing specificity: multiple approaches to understanding the attack and defense of plants. Trends Plant Sci 17 (5): 239-242. https://doi.org/10.1016/j.tplants.2012.03.011
Alcaide F, Solla A, Cherubini M, Mattioni C, Cuenca B, Camisón Á, Martín MA, 2019a. Adaptive evolution of chestnut forests to the impact of ink disease in Spain. J Syst Evol 58 (4): 504-516. https://doi.org/10.1111/jse.12551
Alcaide F, Solla A, Mattioni C, Castellana S, Martín MA, 2019b. Adaptive diversity and drought tolerance in Castanea sativa assessed through EST-SSR genic markers. Forestry 92 (3): 287-296. https://doi.org/10.1093/forestry/cpz007
Alía R, García del Barrio JM, Iglesias S, Mancha JA, De Miguel J, Nicolás JL, Pérez F, Sánchez de Ron D, 2009. Regiones de Procedencia de especies forestales en España. Ministerio de Medio Ambiente y Medio Rural y marino. Organismo Autónomo Parques nacionales. 363 pp. Madrid.
Anstett DN, Nunes KA, Baskett C, Kotanen PM, 2016. Sources of controversy surrounding latitudinal patterns in herbivory and defense. Trends Ecol Evol 31(10): 789-802. https://doi.org/10.1016/j.tree.2016.07.011
Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen JP, 2009. Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition. Oecologia. 159(4): 777-788. https://doi.org/10.1007/s00442-008-1268-7
Becerra JX, Noge K, Venable DL, 2009. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proc Natl Acad Sci USA 106(43):18062-18066. https://doi.org/10.1073/pnas.0904456106
Benton JJ, 2003. Agronomic handbook: Management of crops, soils and their fertility. CRC press LLC. USA.
Blaker NS, MacDonald JD, 1983. Influence of container médium pH on sporangium formation, zoospore reléase and infection of rhododendron by Phytophthora cinnamomi. Plant Disease 67: 259-263. https://doi.org/10.1094/PD-67-259
Bogdziewicz M, Espelta JM, Bonal R, 2019. Tolerance to seed predation mediated by seed size increases at lower latitudes in a Mediterranean oak. Ann Bot 123(4): 707-714. https://doi.org/10.1093/aob/mcy203
Brasier CM, 1992. Oak tree mortality in Iberia. Nature 360(6404), 539. https://doi.org/10.1038/360539a0
Brasier CM, 1996. Phytophthora cinnamomi and oak decline in Southern Europe. Environmental constraints, including climate change. Ann For Sci 53(2-3): 347-358. https://doi.org/10.1051/forest:19960217
Cadahía E, Conde E, Cañellas I, García-Vallejo MC, 1993. Variación del contenido de taninos en las bellotas de Quercus suber L. y Quercus ilex L. durante el proceso de maduración. Congreso Forestal Español, Lourizán. Tomo 11. 485.
Campos P, 2004. Towards a sustainable global economics approach for Mediterranean agroforestry systems. In: Schnabel, S., Ferreira, A. (eds.) Sustainability of agrosilvopastoral systems. Advances in GeoEcology, vol 37. Catena Verlag, Reiskirchen, Germany, pp 13-28.
Conrad AO, McPherson BA, Wood DL, Madden LV, Bonello P, 2017. Constitutive phenolic biomarkers identify naïve Quercus agrifolia resistant to Phytophthora ramorum, the causal agent of sudden oak death. Tree Physiol 37(12): 1686-1696-. https://doi.org/10.1093/treephys/tpx116
Corcobado T, Solla A, Madeira MA, Moreno G, 2013. Combined effects of soil properties and Phytophthora cinnamomi infections on Quercus ilex decline. Plant Soil 373(1-2): 403-413. https://doi.org/10.1007/s11104-013-1804-z
Corcobado T, Cubera E, Juarez E, Moreno G, Solla A, 2014. Drought events determine performance of Quercus ilex seedlings and increase their susceptibility to Phytophthora cinnamomi. Agric For Meteorol 192-193:1-8. https://doi.org/10.1016/j.agrformet.2014.02.007
Dawra RK, Makkar HPS, Singh B, 1988. Total phenolics, condensed tannins and protein-precipitable phenolics in young and mature leaves of oak species. J Agric Food Chem 36(5): 951-953. https://doi.org/10.1021/jf00083a013
Delgado-Baquerizo M, Guerra CA, Cano-Díaz C, Egidi E, Wang JT, Eisenhauer N, Singh BK, Maestre FT, 2020. The proportion of soil-borne pathogens increases with warming at the global scale. Nat Clim Change 10: 550-554. https://doi.org/10.1038/s41558-020-0759-3
Díaz M, Pulido FJ, 2009. 6310 Dehesas perennifolias de Quercus spp. En: VV.AA., Bases ecológicas preliminares para la conservación de los tipos de hábitat de interés comunitario en España. Madrid: Ministerio de Medio Ambiente, y Medio Rural y Marino. 69 p.
Dicke M, Hilker M, 2003. Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl Ecol 4(1): 3-14. https://doi.org/10.1078/1439-1791-00129
Dixon G, 1984. Plan pathogens and their control in horticulture. Science in Horticulture Series, Aberdeen, UK. https://doi.org/10.1007/978-1-349-06923-1
Duque-Lazo J, Navarro-Cerrillo RM, Van Gils H, Groen TA, 2018. Forecasting oak decline caused by Phytophthora cinnamomi in Andalusia: Identification of priority areas for intervention. For EcolManag 417, pp. 122-136. https://doi.org/10.1016/j.foreco.2018.02.045
Duvenhage JA, Kotzé JM, 1991. The influence of calcium on saprophytic growth and pathogenicity of Phytophthora cinnamomi and on resistance of avocado to root rot. South African Avocado Growers′Association Yearbook 14: 13-14.
Eckert CG, Samis KE, Lougheed SC, 2008. Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17(5):1170-1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x
Eriksson G, Ekberg I, Clapham D, 2013. Genetics applied to forestry. Department of Plant Biology and Forest Genetics, SLU. Uppsala, Sweden.
Escribano M, Pulido FJ, 1998. La dehesa en Extremadura. Estructura económica y recursos naturales. SIDT Junta de Extremadura, Mérida (Spain).
Faeth SH,1986. Indirect interactions between temporally separated hervibores mediated by the host plant. Ecology 67: 479-454. https://doi.org/10.2307/1938591
Freeman BC, Beattie GA, 2008. An overview of plant defenses against pathogens and herbivores. The Plant Health Instructor. https://doi.org/10.1094/PHI-I-2008-0226-01
Gallardo A, Morcuende D, Solla A, Moreno G, Pulido FJ, Quesada A, 2019. Regulation by biotic stress of tannins biosynthesis in Quercus ilex: crosstalk between defoliation and Phytophthora cinnamomi infection. Physiol Plant 165(2): 319-329. https://doi.org/10.1111/ppl.12848
Gilbert KJ, Whitlock MC, 2015. QST-FST comparisons with unbalanced half-sib designs. Mol Ecol Resour 15(2): 262-267. https://doi.org/10.1111/1755-0998.12303
Hahn PG, Maron JL, 2016. A framework for predicting intraspecific variation in plant defense. Trends Ecol Evol 31(8): 646-656. https://doi.org/10.1016/j.tree.2016.05.007
Haslam E, 2007. Vegetable tannins-lessons of a pythochemical lifetime. Phytochemistry 68: 2713-2721. https://doi.org/10.1016/j.phytochem.2007.09.009
IGME, Geochemistry Database of the Geological and Mining Institute of Spain: http://info.igme.es/Geoquimica/.
Isabel N, Holliday JA, Aitken SN, 2020. Forest genomics: advancing climate adaptation, forest health, productivity and conservation. Evol Appl 13(1): 3-10. https://doi.org/10.1111/eva.12902
Ivetić V, Devetaković J, Nonić M, Stanković D, Šijačić-Nikolić M, 2016. Genetic diversity and forest reproductive material - from seed source selection to planting. iForest 9(5): 801-812. https://doi.org/10.3832/ifor1577-009
Ivetić V, Devetaković J, 2017. Concerns and evidence on genetic diversity in planted forests. Reforesta 3:196-207. https://doi.org/10.21750/REFOR.3.15.39
Jayaraman K, 1999. A statistical manual for forestry research. FORSPA-FAO Publication, Bangkok.
Jensen EL, Barr GR, 1971. Standard errors of heritability estimates calculated from variance component analysis of a two-way classification. J Anim Sci 32 (6): 1069-1077. https://doi.org/10.2527/jas1971.3261069x
Kraus TEC, Dahlgren EC, Zasoski RJ, 2003. Tannins in nutrient dynamics of forest ecosystems - a review. Plant and Soil 256(1): 41-66. https://doi.org/10.1023/A:1026206511084
Kraus TEC, Zasoski RJ, Dahlgren RA, 2004. Fertility and pH effects on polyphenol and condensed tannin concentrations in foliage and roots. Plant Soil 262: 95-109.López-Goldar X, Villari C, Bonello P, Borg-Karlson AK, Grivet D, Sampedro L, Zas R, 2019. Genetic variation in the constitutive defensive metabolome and its inducibility are geographically structured and largely determined by demographic processes in maritime pine. J Ecol 107(5), 2464-2477. https://doi.org/10.1111/1365-2745.13159
Makkar HPS, 2003. Measurement of total phenolics and tannins using Folin-Ciocalteu method. In: Quantification of tannins in tree and shrub foliage. Springer, Dordrecht, the Netherlands, pp 49-51. https://doi.org/10.1007/978-94-017-0273-7_3
Martín JA, Sobrino-Plata J, Rodríguez-Calcerrada J, Collada C, Gil L, 2019. Breeding and scientific advances in the fight against Dutch elm disease: Will they allow the use of elms in forest restoration? New For (Dordr) 50: 183-215. https://doi.org/10.1007/s11056-018-9640-x
McKown AD, Guy RD, Quamme L, Klapste J, La Mantia J, Constabel CP, El-Kassaby YA, Hamelin RC, Zifkin M, Azam MS, 2014. Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs. Mol Ecol 23: 5771-5790. https://doi.org/10.1111/mec.12969
Merilä J, Crnokrak P, 2001. Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14: 892-903. https://doi.org/10.1046/j.1420-9101.2001.00348.x
Moore BD, Andrew RL, Kulheim C, Foley WJ, 2014. Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201(3): 733-750. https://doi.org/10.1111/nph.12526
Moreira X, Mooney KA, Rasmann S, Petry WK, Carrillo-Gavilan A, Zas R, Sampedro L, 2014. Trade‐offs between constitutive and induced defences drive geographical and climatic clines in pine chemical defences. Ecol Lett 17(5): 537-546. https://doi.org/10.1111/ele.12253
Moreira X, Glauser G, Abdala-Roberts L, 2017. Interactive effects of plant neighbourhood and ontogeny on insect herbivory and plant defensive traits. Sci Rep 7(1): 4047. https://doi.org/10.1038/s41598-017-04314-3
Moreira X, Castagneyrol B, Abdala-Roberts L, Berny-Mier y Teran JC, Timmermans BGH, Bruun HH, Covelo F, Glauser G, Rasmann S, Tack AJM, 2018. Latitudinal variation in plant chemical defences drives latitudinal patterns of leaf herbivory. Ecography 41(7): 1124-1134. https://doi.org/10.1111/ecog.03326
Moreira X, Abdala-Roberts L, Henrik-Bruun H, Covelo F, De Frenne P, Galmán A, Gaytán A, Jaatinen R, Ten Hoopen JPJG, Pulkkinen P et al., 2020. Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species. Ann Bot 125(6): 881-890. https://doi.org/10.1093/aob/mcz207
Oliva A, Lahoz E, Contillo R, Aliota G, 1999. Fungistatic activity of Ruta graveolens extract and its allelochemicals. Chem Ecol 25(3): 519-526. https://doi.org/10.1023/A:1020949703205
Ortego J, Bonal R, Muñoz A, Aparicio JM, 2014. Extensive pollen immigration and no evidence of disrupted mating patterns or reproduction in a highly fragmented holm oak stand. J Plant Ecol 7(4):384-395. https://doi.org/10.1093/jpe/rtt049
Pearse IS, Hipp AL, 2012. Global patterns of leaf defences in oak species. Evolution 66(7): 2272-2286. https://doi.org/10.1111/j.1558-5646.2012.01591.x
Pereira HM, Domingos T, Vicente L (Eds.), 2004. Portugal Millennium Ecosystem Assessment: State of the Assessment Report. Centro de Biologia Ambiental de la Faculdade de Ciências, Universidade de Lisboa, Portugal.
Plieninger T, Hartel T, Martín-López B, Beaufoy G, Bergmeier E, Kirby K, Montero MJ, Moreno G, Otero-Rozas E, Van Uytyanck J, 2015. Wood-pastures of Europe: Geographic coverage, social-ecological values, conservation management and policy implications. Biol Conserv 190: 70-79. https://doi.org/10.1016/j.biocon.2015.05.014
Porter LJ, Hirstich LN, Chan BG, 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochem 25(1): 223-230. https://doi.org/10.1016/S0031-9422(00)94533-3
Pulido F, Díaz M, Hidalgo de Trucios S, 2001. Size structure and regeneration of Spanish holm oak Quercus ilex forests and dehesas: effects of agroforestry use on their long-term sustainability. Forest Ecol Manag 146(1-3): 1-13. https://doi.org/10.1016/S0378-1127(00)00443-6
Rasmann S, Agrawal AA, 2011. Latitudinal patterns in plant defence: evolution of cardenolides, their toxicity, and induction following herbivory. Ecol Lett 14(5): 476- 483. https://doi.org/10.1111/j.1461-0248.2011.01609.x
Roda F, Vayreda J, Ninyerola M, 2009. 9340 Encinares de Quercus ilex y Quercus rotundifolia. En: VV.AA., Bases ecológicas preliminares para la conservación de los tipos de hábitat de interés comunitario en España. Madrid: Ministerio de Medio Ambiente, y Medio Rural y Marino. 94 p.
Rodríguez-Martín JA, López-Arias M, Grau-Corbí JM, 2009. Metales pesados, materia orgánica y otros parámetros de los suelos agrícolas y pastos de España. Ministerio de Medio Ambiente y Medio Rural y Marino/Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) - Ministerio de Ciencia e Innovación, Madrid.
Salminen JP, Karonen M, 2011. Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol. 25(2):325-338. https://doi.org/10.1111/j.1365-2435.2010.01826.x
Sánchez ME, Caetano P, Romero MA, Navarro RM, Trapero A, 2006. Phytophthora root rot as the main factor of oak decline in southern Spain. In: Brasier C, Jung T, Oßwald W, eds. Progress in Research on Phytophthora Diseases of Forest Trees. Farnham, Surrey, UK: Forest Research, 149-54.
Scalbert A, 1991. Antimicrobial properties of tannins. Phytochemistry 30(12): 3875-3883. https://doi.org/10.1016/0031-9422(91)83426-L
Schultz J, 1988. Plant responses to herbivores. Trends Ecol Evol 3(2): 45:49. https://doi.org/10.1016/0169-5347(88)90047-X
Serrano MS, Fernández-Rebollo P, De Vita P, Sánchez ME, 2013. Calcium mineral nutrition increases the tolerance of Quercus ilex to Phytophthora root disease affecting oak rangeland ecosystems in Spain. Agrofor Syst 87(1): 173-179. https://doi.org/10.1007/s10457-012-9533-5
Solla A, López JC, Martín JA, Gil LA, 2015. Genetic variation and heritability estimates of Ulmus minor and Ulmus pumila hybrids for budburst, growth and tolerance to Ophiostoma novo-ulmi. iForest 8: 422-430. https://doi.org/10.3832/ifor1227-007
Solla A, Slobodan M, Gallardo A, Bueno A, Corcobado T, Cáceres Y, Morcuende D, Quesada A, Moreno G, Pulido FJ, 2016. Genetic determination of tannins and herbivore resistance in Quercus ilex. Tree Genet Genom 12(6): 117. https://doi.org/10.1007/s11295-016-1069-9
Stevens MT, Brown SC, Bothwell HM, Bryant JP, 2016. Biogeography of Alaska paper birch (Betula neoalaskana): latitudinal patterns in chemical defense and plant architecture. Ecology 97(2): 494-502. https://doi.org/10.1890/15-0968
Stong RA, Kolodny E, Kelsey RG, González-Hernández MP, Vivanco JM, Manter DK, 2013. Effect of plant sterols and tannins on Phytophthora ramorum growth and sporulation. J Chem Ecol 39(6): 733-743. https://doi.org/10.1007/s10886-013-0295-y
Thompson JN, 2005. The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press, USA. https://doi.org/10.7208/chicago/9780226118697.001.0001
Urli M, 2013. Réponse des rabres forestiers aux changements globaux: approches biogéographique et écophysiologique. Biologie végétale. Thèse Doctorale. Université Sciences et Technologies - Bordeaux I, France.
Visscher PM, Goddard ME, 2015. A general unified framework to assess the sampling variance of heritability estimates using pedigree or marker-based relationships. Genetics 199(1): 223-232. https://doi.org/10.1534/genetics.114.171017
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