Chemical Composition of Cuticular Waxes and Pigments and Morphology of Leaves of Quercus suber Trees of Different Provenance
Abstract
:1. Introduction
2. Results
3. Discussion
4. Material and Methods
4.1. Sampling
4.2. Morphological Variables
4.3. Determination of Leaf Pigment Contents
4.4. Cuticle Permeability Assay
4.5. Extraction of Cuticular Waxes
4.6. Cuticular Wax Composition
4.7. Structural and Anatomical Observations
4.8. Statistical Analyses
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Pollard, M.; Beisson, F.; Li, Y.; Ohlrogge, J.B. Building lipid barriers: Biosynthesis of cutin and suberin. Trends Plant Sci. 2008, 13, 236–246. [Google Scholar] [CrossRef] [PubMed]
- Domínguez, E.; Heredia-Guerrero, J.A.; Heredia, A. The biophysical design of plant cuticles: An overview. New Phytol. 2011, 189, 938–949. [Google Scholar] [CrossRef] [PubMed]
- Ingram, G.; Nawrath, C. The Roles of the Cuticle in Plant Development: Organ Adhesions and Beyond. J. Exp. Bot. 2017, 68, 5307–5321. [Google Scholar] [CrossRef] [PubMed]
- Samuels, L.; Kunst, L.; Jetter, R. Sealing Plant Surfaces: Cuticular Wax Formation by Epidermal Cells. Annu. Rev. Plant Biol. 2008, 59, 683–707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kunst, L.; Samuels, L. Plant cuticles shine: Advances in wax biosynthesis and export. Curr. Opin. Plant Biol. 2009, 12, 721–727. [Google Scholar] [CrossRef]
- Jetter, R.; Kunst, L.; Samuels, A.L. Composition of plant cuticular waxes. In Biology of the Plant Cuticle, Annual Plant Reviews; Riederer, M., Müller, C., Eds.; Blackwell: Oxford, UK, 2006; Volume 23, pp. 145–181. [Google Scholar]
- Reynhardt, E.C.; Riederer, M. Structures and molecular dynamics of plant waxes. II. Cuticular waxes from leaves of Fagus sylvatica L. and Hordeum vulgare L. Eur. Biophys. J. 1994, 23, 59–70. [Google Scholar]
- Zeisler-Diehl, V.; Müller, Y.; Schreiber, L. Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. J. Plant Physiol. 2018, 227, 66–74. [Google Scholar] [CrossRef]
- Sharma, P.; Kothari, S.L.; Rathore, M.S.; Gour, V.S. Properties, variations, roles and potential applications of epicuticular wax: A review. Turk. J. Bot. 2018, 42, 135–149. [Google Scholar] [CrossRef]
- Shepherd, T.; Griffiths, D.W. The effects of stress on plant cuticular waxes. New Phytol. 2006, 171, 469–499. [Google Scholar] [CrossRef]
- Kosma, D.K.; Jenks, M. Eco-physiological and molecular-genetic determinants of plant cuticle function in drought and salt stress tolerance. In Advances in Molecular Breeding toward Drought and Salt Tolerant Crops; Jenks, M.A., Hasegawa, P.M., Jain, S.M., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 91–120. [Google Scholar]
- Serrano, M.; Coluccia, F.; Torres, M.; L’Haridon, F.; Métraux, J.-P. The cuticle and plant defense to pathogens. Front. Plant Sci. 2014, 5, 274. [Google Scholar] [CrossRef] [Green Version]
- Domínguez, E.; Heredia-Gerrero, J.A.; Heredia, A. The plant cuticle: Old challenges, new perspectives. J. Exp. Bot. 2017, 68, 5251–5255. [Google Scholar] [CrossRef] [PubMed]
- Schuster, A.C.; Burghardt, M.; Riederer, M. The ecophysiology of leaf cuticular transpiration: Are cuticular water permeabilities adapted to ecological conditions? J. Exp. Bot. 2017, 68, 5271–5279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pereira, H. Cork: Biology, Production and Uses; Elsevier: Amsterdam, The Netherlands, 2007. [Google Scholar]
- Leite, C.; Oliveira, V.; Lauw, A.; Pereira, H. Cork rings suggest how to manage Quercus suber to mitigate the effects of climate changes. Agric. For. Meteorol. 2019, 266, 12–19. [Google Scholar] [CrossRef]
- Pérez-Harguindeguy, N.; Díaz, S.; Garnier, E.; Lavorel, S.; Poorter, H.; Jaureguiberry, P.; Bret-Harte, M.S.; Cornwell, W.K.; Craine, J.M.; Gurvich, D.E.; et al. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 2013, 61, 167–234. [Google Scholar] [CrossRef]
- Oliveira, G.; Correia, O.; Martins Loução, M.; Catarino, F.M. Phenological and growth-patterns of the Mediterranean oak Quercus suber L. Trees Struct. Funct. 1994, 9, 41–46. [Google Scholar] [CrossRef] [Green Version]
- Vaz, M.; Pereira, J.S.; Gazarini, L.C.; David, T.S.; David, J.S.; Rodrigues, A.; Moroco, J.; Chaves, M.M. Drought-induced photosynthetic inhibition and autumn recovery in two Mediterranean oak species (Quercus ilex and Quercus suber). Tree Physiol. 2010, 30, 946–956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prats, K.A.; Brodersen, C.R.; Ashton, M.S. Influence of dry season on Quercus suber L. leaf traits in the Iberian Peninsula. Am. J. Bot. 2019, 106, 656–666. [Google Scholar] [CrossRef]
- Costa-e-Silva, F.; Correia, A.C.; Piayda, A.; Dubbert, M.; Rebmenn, C.; Cuntz, M.; Werner, C.; David, J.S.; Pereira, J.S. Effects of an extremely dry winter on net ecosystem carbon exchange and tree phenology at a cork oak woodland. Agric. For. Meteorol. 2015, 204, 48–57. [Google Scholar] [CrossRef] [Green Version]
- Martins, C.M.C.; Mesquita, S.M.M.; Vaz, W.L.C. Cuticular Waxes of the Holm (Quercus ilex L. subsp. ballota (Desf.) Samp.) and Cork (Q. suber L.) Oaks. Phytochem. Anal. 1999, 10, 1–5. [Google Scholar] [CrossRef]
- Varela, M.C. European Network for the Evaluation of Genetic Resources of Cork Oak for Appropriate Use in Breeding and Gene Conservation Strategies; Handbook; INIA: Lisbon, Portugal, 2000. [Google Scholar]
- Eriksson, G. Quercus suber—Recent Genetic Research; European Forest Genetic Resources Programme (EUFORGEN), Bioversity International: Rome, Italy, 2017; 30p, Available online: http://www.euforgen.org/fileadmin/templates/euforgen.org/upload/Publications/Thematic_publications/Quercus_suber_OpenSourceCR_web.pdf (accessed on 25 June 2020).
- Sampaio, T.; Branco, M.; Guichoux, E.; Petit, R.J.; Pereira, J.S.; Varela, M.C.; Almeida, M.H. Does the geography of cork oak origin influence budburst and leaf pest damage? For. Ecol. Manag. 2016, 373, 33–43. [Google Scholar] [CrossRef]
- Sampaio, T.; Gonçalves, E.; Patrício, M.S.; Cota, T.M.; Almeida, M.H. Seed origin drives differences in survival and growth traits of cork oak (Quercus suber L.) populations. For. Ecol. Manag. 2019, 448, 267–277. [Google Scholar] [CrossRef] [Green Version]
- Varela, M.C.; Tessier, C.; Ladier, J.; Dettori, S.; Filigheddu, M.; Bellarosa, R.; Vessella, F.; Almeida, M.H.; Sampaio, T.; Patrício, M.S. Characterization of the International Network Fair 202 of provenance and progeny trials of cork oak on multiple sites for further use on forest sustainable management and conservation of genetic resources. In Proceedings of the Second International Congress of Silviculture, Designing the Future of the Forestry Sector, Florence, Italy, 26–29 November 2014. [Google Scholar]
- Mediavilla, S.; Martín, I.; Babiano, J.; Escudero, A. Foliar plasticity related to gradients of heat and drought stress across crown orientations in three Mediterranean Quercus species. PLoS ONE 2019, 14, e0224462. [Google Scholar] [CrossRef] [PubMed]
- Vaz, M.; Moroco, J.; Ribeiro, N.; Gazarini, L.C.; Pereira, J.S.; Chaves, M.M. Leaf-level responses to light in two co-occurring Quercus (Quercus ilex and Quercus suber): Leaf structure, chemical composition and photosynthesis. Agrofor. Syst. 2011, 82, 173–181. [Google Scholar] [CrossRef]
- Ramírez-Valiente, J.A.; Valladares, F.; Delgado, A.; Granados, S.; Aranda, I. Factors affecting cork oak growth under dry conditions: Local adaptation and contrasting additive genetic variance within populations. Tree Genet. Genomes 2011, 7, 285–295. [Google Scholar] [CrossRef]
- Rzigui, T.; Jazzar, L.; Ben Baaziz, K.; Fkiri, S.; Nasr, Z. Drought tolerance in cork oak is associated with low leaf stomatal and hydraulic conductances. iForest 2018, 11, 728–733. [Google Scholar] [CrossRef]
- Lobo-do-Val, R.; Besson, C.K.; Caldeira, M.C.; Chaves, M.M.; Pereira, J.S. Drought reduces tree growing season length but increases nitrogen resorption efficiency in a Mediterranean ecosystem. Biogeosciences 2019, 16, 1265–1279. [Google Scholar] [CrossRef] [Green Version]
- Daoudi, H.; Derridj, A.; Hannachi, L.; Mévy, J.P. Comparative drought responses of Quercus suber seedlings of three algerian provenances under greenhouse conditions. Revue d’Ecologie (Terre et Vie) 2018, 73, 57–70. [Google Scholar]
- Aranda, I.; Pardos, M.; Puértolas, J.; Jiménez, M.D.; Pardos, J.A. Water use efficiency in cork oak (Quercus suber L.) is modified by the interaction of water and light availabilities. Tree Physiol. 2007, 27, 671–677. [Google Scholar] [CrossRef]
- Gunn, S.; Farrar, J.F.; Collis, B.E.; Nason, M. Specific leaf area in barley: Individual leaves versus whole plants. New Phytol. 1999, 143, 45–51. [Google Scholar] [CrossRef]
- Pierce, L.L.; Running, S.W.; Walker, J. Regional-scale relationships of leaf-area index to specific leaf-area and leaf nitrogen-content. Ecol. Appl. 1999, 4, 313–321. [Google Scholar] [CrossRef] [Green Version]
- Reich, P.B.; Wright, I.J.; Lusk, C. Predicting leaf physiology from simple plant and climate attributes: A global glopnet analysis. Ecol. Appl. 2007, 17, 1982–1988. [Google Scholar] [CrossRef] [PubMed]
- Han, Q.; Kabeya, D.; Günter, H. Leaf traits, shoot growth and seed production in mature Fagus sylvatica trees after 8 years of CO2 enrichment. Ann. Bot. 2011, 107, 1405–1411. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Li, Y.; Li, X.; Chen, Z.; He, N. Variation in leaf morphological, stomatal, and anatomical traits and their relationships in temperate and subtropical forests. Sci. Rep. 2019, 9, 5803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Faria, T.; García-Plazaola, J.I.; Abadía, A.; Cerasoli, S.; Pereira, J.S.; Chaves, M.M. Diurnal changes in photoprotective mechanisms in leaves of cork oak (Quercus suber L.) during summer. Tree Physiol. 1996, 16, 115–123. [Google Scholar] [CrossRef] [Green Version]
- Prasad, R.B.N.; Gülz, P.G. Surface structure and chemical composition of leaf waxes from Quercus robur L., Acer pseudoplatanus L. and JugIans regia L. Z. Naturforsch. C 1990, 45, 813–817. [Google Scholar] [CrossRef]
- Bahamonde, H.A.; Gil, L.; Fernández, V. Surface properties and permeability to calcium chloride of Fagus sylvatica and Quercus petraea leaves of different canopy heights. Front. Plant Sci. 2018, 9, 494. [Google Scholar] [CrossRef]
- Maiti, R.; Rodriguez, H.G.; Sarkar, N.C.; Kumari, A. Biodiversity in leaf chemistry (Pigments, epicuticular wax and leaf nutrients) in woody plant species in north-eastern Mexico, a synthesis. Forest Res. 2016, 5, 170. [Google Scholar]
- Sánchez, F.J.; Manzanares, M.; de Andrés, E.F.; Tenorio, J.L.; Ayerbe, L. Residual transpiration rate, epicuticular wax load and leaf colour of pea plants in drought conditions. Influence on harvest index and canopy temperature. Eur. J. Agron. 2001, 15, 57–70. [Google Scholar] [CrossRef]
- Xue, D.; Zhang, X.; Lu, X.; Chen, G.; Chen, Z.-H. Molecular and Evolutionary Mechanisms of Cuticular Wax for Plant Drought Tolerance. Front. Plant Sci. 2017, 8, 621. [Google Scholar] [CrossRef]
- Riederer, M.; Schreiber, L. Protecting against water loss: Analysis of the barrier properties of plant cuticles. J. Exp. Bot. 2001, 52, 2023–2032. [Google Scholar] [CrossRef]
- Kerstiens, G. Cuticular water permeability and its physiological significance. J. Exp. Bot. 1996, 47, 1813–1832. [Google Scholar] [CrossRef] [Green Version]
- Burghardt, M.; Riederer, M. Ecophysiological relevance of cuticular transpiration of deciduous and evergreen plants in relation to stomatal closure and leaf water potential. J. Exp. Bot. 2003, 54, 1941–1949. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jetter, R.; Schäffer, S. Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant. Physiol. 2001, 126, 1725–1737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buschhaus, C.; Jetter, R. Composition differences between epicuticular and intracuticular wax substructures: How do plants seal their epidermal surfaces? J. Exp. Bot. 2011, 62, 841–853. [Google Scholar] [CrossRef] [Green Version]
- Gülz, P.G.; Müller, E. Seasonal variation in the composition of epicuticular waxes of Quercus robur leaves. Z. Naturforsch. C 1992, 47, 800–806. [Google Scholar] [CrossRef]
- Gülz, P.G.; Müller, E.; Herrmann, T. Chemical composition and surface structures of epicuticular leaf waxes from Castanea sativa and Aesculus hippocastanum. Z. Naturforsch. C 1992, 47, 661–666. [Google Scholar] [CrossRef]
- Gülz, P.G.; Prasad, R.B.N.; Müller, E. Surface structures and chemical composition of epicuticular waxes during leaf development of Fagus sylvatica L. Z. Naturforsch. C 1992, 47, 190–196. [Google Scholar] [CrossRef]
- Fernández, M.A.; de las Heras, B.; García, M.D.; Sáenz, M.T.; Villar, A. New insights into the mechanism of action of the anti-inflammatory triterpene lupeol. J. Pharm. Pharmacol. 2001, 53, 1533–1539. [Google Scholar] [CrossRef]
- Zhang, L.; Zhang, Y.; Zhang, L.; Yang, X.; Lv, Z. Lupeol, a dietary triterpene, inhibited growth and induced apoptosis through down-regulation of DR3 in SMMC7721 cells. Cancer Investig. 2009, 27, 163–170. [Google Scholar] [CrossRef]
- Beserra, F.P.; Xue, M.; Maia, G.L.A.; Leite Rozza, A.L.; Pellizzon, C.H.; Jackson, C.J. Lupeol, a Pentacyclic Triterpene, Promotes Migration, Wound Closure and Contractile Effect In Vitro: Possible Involvement of PI3K/Akt and p38/ERK/MAPK Pathways. Molecules 2018, 23, 2819. [Google Scholar] [CrossRef] [Green Version]
- Paulo, J.A.; Crous-Duran, J.; Firmino, P.N.; Faias, S.P.; Palma, J.H.N. System Report: Cork Oak Silvopastoral Systems in Portugal; The AGFORWARD Research Project WP 2; AGFORWARD: Bedfordshire, UK, 2006. [Google Scholar]
- Rizzini, C.T. Tratado de Fitogeografia do Brasil; HUCITEC, USP: São Paulo, Brazil, 1976. [Google Scholar]
- Lichtenthaler, H.K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Meth. Enzymol. 1987, 148, 350–382. [Google Scholar]
- Wellburn, A.R. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994, 144, 307–313. [Google Scholar] [CrossRef]
- Nobel, P.S. Physicochemical and Environmental Plant Physiology; Academic Press: Oxford, UK, 2009. [Google Scholar]
- Bueno, A.; Alfarhan, A.; Arand, K.; Burghardt, M.; Deininger, A.-C.; Hedrich, R.; Leide, J.; Seufert, P.; Staiger, S.; Riederer, M. Temperature effects on the cuticular transpiration barrier of two desert plants with water-spender and water-saver life strategies. J. Exp. Bot. 2019, 70, 1613–1625. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kolattukudy, P.E.; Agrawal, V.P. Structure and composition of aliphatic constituents of potato tuber skin (suberin). Lipids 1974, 9, 682–691. [Google Scholar] [CrossRef]
- Ferreira, J.P.; Miranda, I.; Sen, A.; Pereira, H. Chemical and cellular features of virgin and reproduction cork from Quercus variabilis. Ind. Crops Prod. 2016, 94, 638–648. [Google Scholar] [CrossRef]
- Alvin, C.R. Methods of Multivariate Analysis; Wiley: New York, NY, USA, 2002. [Google Scholar]
Leaf Features/Provenance Code | PT35 | ES11 | IT3 | FR3 | MA27 | TU32 |
---|---|---|---|---|---|---|
Leaf size (LS; cm2) | 6.2 ± 2.1a | 5.1 ± 2.1b | 6.8 ± 2.7a | 4.6 ± 1.9b | 6.4± 2.8a | 5.6 ± 2.1b |
Specific leaf area (SLA; cm2/g) | 61.5 ± 18.5a | 55.6 ± 17.6a | 67.8 ± 22.7a | 63.1 ± 19.4 a | 64.7 ± 27.9a | 63.7 ± 28.9a |
Sclerophylly index (g/dm2) | 0.9 ± 0.3a | 1.0 ± 0.4a | 0.8 ± 0.3a | 0.9 ± 0.4a | 0.9 ± 0.4a | 0.9 ± 0.4a |
Cuticular wax content (µg/cm2) | 212.5 ± 40.3a | 182.2 ± 60.2a | 201.0 ± 60.4a | 231.5 ± 64.4a | 173.0 ± 80.6a | 136.4 ± 45.9b |
Cuticular wax content (mg/g) | 25.9 ± 0.5a | 20.7 ± 0.5a | 25.7 ± 0.6a | 29.7 ± 0.7a | 24.2 ± 0.4a | 21.6 ± 0.4a |
Photosynthetic Pigments | ||||||
Chlorophyll a (µg/cm2) | 26.6 ± 1.6a | 23.9 ± 3.2b | 24.1 ± 2.0b | 21.1 ± 1.4b | 26.4 ± 2.9a | 24.8 ± 0.7b |
Chlorophyll b (µg/cm2) | 13.3 ± 2.1a | 12.0 ± 1.9a | 12.1 ± 1.4a | 10.7 ± 1.4b | 14.0 ± 1.8a | 12.7 ± 0.5a |
Chlorophyll a/b ratio | 2.0 ± 0.3a | 2.0 ± 0.1a | 2.0 ± 0.1a | 2.0 ± 0.1a | 1.9 ± 0.1a | 2.0 ± 0.1a |
Total chlorophyll (µg/cm2) | 40.0 ± 3.4a | 35.9 ± 5.0b | 36.3 ± 3.4b | 31.8 ± 1.8b | 40.4 ± 4.5 a | 37.5 ± 1.0a |
Total chlorophyll (mg/g) | 2.5 ± 0.2a | 2.1 ± 0.3a | 2.3 ±0.2a | 2.1 ± 0.1a | 2.5 ±0.3a | 2.7 ± 0.1a |
Total carotenoids (µg/cm2) | 8.4 ± 0.4 a | 7.9 ± 0.7b | 7.5 ± 0.8b | 7.2 ± 0.1b | 8.7 ± 0.1a | 8.3 ± 0.2a |
Chlorophyll/carotenoids ratio | 0.2 ± 0.03a | 0.3 ± 0.03a | 0.3 ± 0.04a | 0.3 ± 0.01a | 0.2 ± 0.03a | 0.2 ± 0.01a |
Cuticular Water Permeability | ||||||
Tcut × 10−4 (g/m2s) | 5.5 | 2.7 | 4.9 | 3.3 | 4.8 | 4.0 |
P × 10−5 (m/s) | 2.4 | 1.2 | 2.1 | 1.4 | 2.1 | 1.7 |
Family | Percent of Total Compounds |
---|---|
n-Alkanols | 1.10 ± 0.56 |
n-Alkanes | 6.07 ± 0.72 |
Fatty acids | 12.73 ± 2.41 |
Aromatic compounds | 1.94 ± 0.44 |
Sterols | 5.32 ± 1.23 |
Terpenes | 60.05 ± 3.65 |
Others | 3.76 ± 1.98 |
Total identified compounds | 91.15 ± 3.95 |
Compound/Provenance Code | PT35 | ES11 | IT3 | FR3 | MA27 | TU32 | Whole Leaves |
---|---|---|---|---|---|---|---|
n-Alkanols | 2.03 | 1.33 | 0.90 | 0.93 | 0.35 | 1.05 | 1.10 ± 0.56 |
hexadecan-1-ol (C16OH) | 0.21 | 0.17 | 0.08 | 0.00 | 0.05 | 0.08 | 0.10 ± 0.08 |
octadecan-1-ol (C18OH) | 0.00 | 0.17 | 0.03 | 0.00 | 0.00 | 0.00 | 0.03 ± 0.07 |
tretracosan-1-ol (C24OH) | 1.43 | 0.75 | 0.53 | 0.66 | 0.15 | 0.60 | 0.69 ± 0.42 |
octacosan-1-ol (C28OH) | 0.39 | 0.24 | 0.27 | 0.27 | 0.15 | 0.37 | 0.28 ± 0.09 |
n-Alkanes | 5.78 | 5.92 | 5.57 | 6.09 | 5.55 | 7.46 | 6.06 ± 0.72 |
n-pentadecane (C15) | 0.10 | 0.06 | 0.04 | 0.04 | 0.08 | 0.15 | 0.08 ± 0.04 |
n-Pentacosane (C25) | 0.38 | 0.33 | 0.36 | 0.42 | 0.42 | 0.44 | 0.39 ± 0.04 |
n-heptacosane (C27) | 0.20 | 0.28 | 0.28 | 0.21 | 0.10 | 0.27 | 0.22 ± 0.07 |
n-octacosane (C28) | 3.65 | 3.73 | 3.07 | 3.96 | 3.56 | 4.38 | 3.73 ± 0.44 |
1-nonacosene (C29(2)) | 0.06 | 0.39 | 0.00 | 0.10 | 0.19 | 0.25 | 0.17 ± 0.14 |
n-nonacosane (C29) | 0.47 | 0.10 | 0.33 | 0.49 | 0.29 | 0.40 | 0.35 ± 0.14 |
n-hentriacontane (C31) | 0.93 | 1.04 | 1.49 | 0.87 | 0.92 | 1.57 | 1.14 ± 0.31 |
Fatty Acids | 15.22 | 11.70 | 14.19 | 14.93 | 11.12 | 9.24 | 12.73 ± 2.41 |
Saturated | 14.57 | 11.50 | 13.50 | 13.48 | 9.93 | 8.59 | 11.93 ± 2.33 |
octanoic acid (C8:0) | 0.13 | 0.17 | 0.13 | 0.04 | 0.08 | 0.13 | 0.11 ± 0.05 |
nonanoic acid (C9:0) | 0.05 | 0.21 | 0.28 | 0.17 | 0.03 | 0.06 | 0.13 ± 0.10 |
nonadioc acid (C9(2)) | 0.04 | 0.11 | 0.05 | 0.40 | 0.33 | 1.07 | 0.33 ± 0.39 |
decanoic acid (C10:0) | 0.11 | 0.09 | 0.22 | 0.00 | 0.05 | 0.09 | 0.09 ± 0.07 |
dodecanoic acid (C12:0) | 0.13 | 0.16 | 0.21 | 0.12 | 0.10 | 0.12 | 0.14 ± 0.04 |
tetradecanoic acid (C14:0) | 0.25 | 0.15 | 0.35 | 0.27 | 0.28 | 0.31 | 0.27 ± 0.07 |
hexadecanoic acid (C16:0) | 1.04 | 1.37 | 1.01 | 1.66 | 1.95 | 1.62 | 1.44 ± 0.37 |
octadecanoic acid (C18:0) | 0.21 | 0.23 | 0.17 | 0.31 | 0.27 | 0.29 | 0.25 ± 0.05 |
eicosanoic acid (C20:0) | 0.35 | 0.23 | 0.26 | 0.43 | 0.28 | 0.29 | 0.31 ± 0.07 |
docosanoic acid (C22:0) | 0.67 | 0.44 | 0.39 | 0.69 | 0.38 | 0.45 | 0.50 ± 0.14 |
tetracoscanoic acid (C24:0) | 0.55 | 0.32 | 0.40 | 0.82 | 0.20 | 0.23 | 0.42 ± 0.23 |
hexacosanoic acid (C26:0) | 0.88 | 0.53 | 0.71 | 0.87 | 0.64 | 0.27 | 0.65 ± 0.23 |
octacosanoic acid (C28:0) | 4.03 | 2.51 | 3.19 | 3.39 | 2.38 | 1.22 | 2.79 ± 0.98 |
triacontanoic acid (C30:0) | 6.13 | 4.98 | 6.13 | 4.31 | 2.96 | 2.44 | 4.49 ± 1.56 |
unsaturated | 0.65 | 0.20 | 0.69 | 1.45 | 1.19 | 0.65 | 0.81 ± 0.45 |
9,12-octadecadienoic acid (C18:2) | 0.12 | 0.06 | 0.20 | 0.39 | 0.37 | 0.17 | 0.22 ± 0.13 |
9,12,15-octadecatrienoic acid (C18:3) | 0.53 | 0.14 | 0.49 | 1.06 | 0.82 | 0.48 | 0.59 ± 0.32 |
Aromatic Compounds | 1.39 | 2.57 | 1.77 | 1.77 | 1.41 | 1.74 | 1.78 ± 0.43 |
benzoic acid | 0.06 | 0.13 | 0.11 | 0.06 | 0.03 | 0.08 | 0.08 ± 0.04 |
4-hydroxybenzaldehyde | 0.11 | 0.23 | 0.07 | 0.17 | 0.14 | 0.12 | 0.14 ± 0.06 |
vanillin | 0.01 | 0.06 | 0.06 | 0.00 | 0.11 | 0.03 | 0.05 ± 0.04 |
4-(2-hydroxyethy) phenol | 0.13 | 0.20 | 0.16 | 0.48 | 0.35 | 0.07 | 0.23 ± 0.15 |
methyl p-coumarate, trans | 0.06 | 0.16 | 0.00 | 0.16 | 0.12 | 0.12 | 0.10 ± 0.06 |
quercetin/myricetin | 0.19 | 0.05 | 0.27 | 0.05 | 0.21 | 0.08 | 0.14 ± 0.09 |
kaempferol | 0.13 | 0.30 | 0.55 | 0.00 | 0.09 | 0.49 | 0.26 ± 0.22 |
pinoresinol | 0.33 | 0.46 | 0.32 | 0.62 | 0.04 | 0.50 | 0.38 ± 0.20 |
2,3-dihydrobenzofuran | 0.26 | 0.17 | 0.12 | 0.17 | 0.07 | 0.18 | 0.16 ± 0.06 |
hexadecy-(E)-p-coumarate | 0.38 | 0.99 | 0.23 | 0.24 | 0.32 | 0.25 | 0.40 ± 0.29 |
Sterols | 5.11 | 3.16 | 5.14 | 6.36 | 6.62 | 5.54 | 5.32 ± 1.23 |
β-tocopherol/γ-tocopherol | 0.34 | 0.42 | 1.07 | 0.22 | 0.29 | 0.62 | 0.49 ± 0.31 |
α-tocopherol | 0.58 | 0.22 | 0.41 | 0.66 | 0.69 | 0.16 | 0.45 ± 0.23 |
β-sitosterol | 4.19 | 2.52 | 3.66 | 5.48 | 5.64 | 4.76 | 4.38 ± 1.18 |
Terpenes | 55.64 | 57.53 | 62.56 | 58.24 | 64.61 | 60.70 | 59.88 ± 3.36 |
diterpenes | 1.00 | 0.29 | 1.21 | 1.59 | 1.30 | 0.55 | 0.99 ± 0.49 |
phytol | 0.46 | 0.21 | 1.00 | 1.18 | 0.86 | 0.38 | 0.68 ± 0.39 |
α-tocopherolquinone | 0.54 | 0.08 | 0.21 | 0.41 | 0.44 | 0.17 | 0.31 ± 0.18 |
pentacyclic triterpenes | 54.64 | 57.24 | 61.35 | 56.65 | 64.31 | 60.15 | 59.06 ± 3.54 |
α-amyrin | 1.01 | 0.92 | 0.97 | 1.00 | 1.09 | 0.73 | 0.95 ± 0.12 |
β-amyrin | 5.14 | 4.82 | 4.63 | 5.68 | 8.26 | 5.30 | 5.64 ± 1.34 |
lupeol | 37.76 | 34.37 | 38.59 | 32.91 | 37.22 | 40.49 | 36.89 ± 2.79 |
friedooleanan-3-ol | 3.95 | 7.59 | 8.25 | 7.29 | 7.85 | 5.82 | 6.79 ± 1.62 |
friedelin | 2.94 | 5.39 | 3.79 | 4.60 | 4.86 | 3.12 | 4.12 ± 0.99 |
betulin | 1.42 | 1.40 | 1.44 | 2.02 | 2.25 | 1.75 | 1.71 ± 0.36 |
oleanolic acid | 0.43 | 0.63 | 0.61 | 0.92 | 0.42 | 0.76 | 0.63 ± 0.19 |
betulinic acid | 1.27 | 1.31 | 1.78 | 1.73 | 1.94 | 1.83 | 1.64 ± 0.28 |
ursolic acid | 0.72 | 0.81 | 1.29 | 0.50 | 0.42 | 0.35 | 0.68 ± 0.35 |
Others | 3.48 | 3.59 | 2.66 | 8.21 | 3.29 | 3.48 | 4.12 ± 2.03 |
myo-inositol/ Scyllo-inositol | 1.55 | 1.30 | 1.60 | 3.46 | 1.06 | 1.01 | 1.66 ± 0.91 |
D (-) fructofuranose | 0.39 | 0.33 | 0.00 | 0.79 | 0.39 | 0.38 | 0.38 ± 0.25 |
D (-) fructopyranose | 0.43 | 0.36 | 0.00 | 0.79 | 0.28 | 0.51 | 0.40 ± 0.26 |
glycerol | 0.46 | 0.75 | 0.45 | 0.56 | 0.59 | 0.29 | 0.52 ± 0.16 |
6,10,14 trimethtylpentadecan-2-one | 0.09 | 0.52 | 0.23 | 1.91 | 0.40 | 0.82 | 0.66 ± 0.66 |
1-Linoleylglycerol | 0.08 | 0.01 | 0.14 | 0.25 | 0.27 | 0.11 | 0.14 ± 0.10 |
Total identified compounds | 88.65 | 85.80 | 92.77 | 96.52 | 93.94 | 89.21 | 91.15 ± 3.95 |
Provenance Code | Country of Seed Collection | Latitude | Longitude | Altitude (m) | Tm (°C) | PPT (mm) |
---|---|---|---|---|---|---|
PT35 | Portugal, Ermidas do Sado | 38° 00′ N | 8° 70′ W | 79 | 15.8 | 557 |
ES11 | Spain, Alpujarras | 36° 50′ N | 3° 18′ W | 1300 | 13.0 | 742 |
IT13 | Italy, Puglia | 40° 34′ N | 17° 40′ E | 45 | 16.6 | 588 |
FR3 | France, Landes | 43° 45′ N | 1° 20′ W | 20 | 12.3 | 870 |
MA27 | Morocco, Rif Occidental I.2 | 35° 07′ N | 5° 16′ W | 300 | n.a. | 1280 |
TU32 | Tunisia, Mekna | 36° 57′ N | 8° 51′ W | 12 | 17.9 | 948 |
Monte da Fava | Portugal, Santiago do Cacém | 38° 00’ N | 8° 07’ W | 79 | 15.8 | 557 |
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Simões, R.; Rodrigues, A.; Ferreira-Dias, S.; Miranda, I.; Pereira, H. Chemical Composition of Cuticular Waxes and Pigments and Morphology of Leaves of Quercus suber Trees of Different Provenance. Plants 2020, 9, 1165. https://doi.org/10.3390/plants9091165
Simões R, Rodrigues A, Ferreira-Dias S, Miranda I, Pereira H. Chemical Composition of Cuticular Waxes and Pigments and Morphology of Leaves of Quercus suber Trees of Different Provenance. Plants. 2020; 9(9):1165. https://doi.org/10.3390/plants9091165
Chicago/Turabian StyleSimões, Rita, Ana Rodrigues, Suzana Ferreira-Dias, Isabel Miranda, and Helena Pereira. 2020. "Chemical Composition of Cuticular Waxes and Pigments and Morphology of Leaves of Quercus suber Trees of Different Provenance" Plants 9, no. 9: 1165. https://doi.org/10.3390/plants9091165