Subscribe to RSS
DOI: 10.1055/s-2006-924662
Georg Thieme Verlag Stuttgart KG · New York
Morphology and Biochemistry of Non-Glandular Trichomes in Cistus salvifolius L. Leaves Growing in Extreme Habitats of the Mediterranean Basin
Publication History
Received: July 17, 2006
Accepted: September 11, 2006
Publication Date:
04 December 2006 (online)

Abstract
Here the functional roles of stellate and dendritic trichomes in Cistus salvifolius L leaves were studied by analysing i) both leaf surface and trichome morphology using scanning electron and light microscopy; and ii) the composition and localisation of polyphenols by coupling liquid chromatography with fluorescence spectroscopy and fluorescence microimaging. Red-coloured compounds were detected in the stalk cells and the channel in the trichome arm, and appeared to be released at the tip end of the trichome branch. We identified such metabolites as ellagitannins, namely punicalagin and two galloyl derivatives of punicalagin. These ellagitannins accounted for 4.3 % of leaf dry weight and their concentration in the leaf leachate averaged 289.4 mg L-1. The trichome arms exhibited an appreciable orange-red autofluorescence (centred at 620 nm) when excited with UV light (at 365 nm) or emitted in the yellow waveband (peak centred at 566 nm) when stained with the Naturstoff reagent, and excited at 488 nm. The fluorescence signatures of the trichome arms were consistent with the presence of mono-hydroxy B-ring substituted flavonoids, which were identified as the mono- and di-coumaroyl derivative of a kaempferol 3-O-glycoside. Our data may provide some insights on the functional roles of stellate and dendritic trichomes in the response mechanisms of C. salvifolius to Mediterranean-type climate, based upon (i) the potential effect of released ellagitannins on the soil nitrogen dynamic and (ii) the ability of acylated kaempferol 3-O-glycosides to effectively absorb both the UV‐B and UV‐A wavelengths.
Key words
Cistus salvifolius - coumaroyl derivatives of kaempferol 3-O-glycoside - dendritic and stellate trichomes - ellagitannins - environmental scanning electron microscopy (ESEM) - fluorescence spectroscopy and microimaging - Mediterranean-type ecosystems.
References
- 1 Agati G., Galardi C., Gravano E., Romani A., Tattini M.. Flavonoid distribution in tissues of Phillyrea latifolia L. leaves as estimated by microspectrofluorometry and multispectral fluorescence microimaging. Photochemistry and Photobiology. (2002); 76 350-360
- 2 Aloni R., Schwalm K., Langhans M., Ullrich C. I.. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta. (2003); 216 841-853
- 3 Aronne G., De Micco V.. Seasonal dimorphism in the Mediterranean Cistus incanus L. subsp. incanus. Annals of Botany. (2001); 87 789-794
-
4 Behnke H. D..
Plant trichome-structure and ultrastructure: general terminology, taxonomic applications, and aspects of trichome bacterial interactions in leaf tips of Dioscorea. Rodriguez, E., Healey, P. L., and Mehta, I., eds. Biology and Chemistry of Plant Trichomes. New York; Plenum Press (1984): 1-21 - 5 Bruschi P., Vendramin G. G., Bussotti F., Grassoni P.. Morphological and molecular diversity among Italian populations of Quercus petraea (Fagaceae). Annals of Botany. (2003); 91 707-716
- 6 Castells E., Peñuelas J.. Is there a feedback between N availability in siliceous and calcareous soils and Cistus albidus leaf chemical composition?. Oecologia. (2003); 136 183-192
- 7 Castells E., Peñuelas J., Valentine D. W.. Are phenolic compounds released from the Mediterranean shrub Cistus albidus responsible for changes in N cycling in siliceous and calcareous soils?. New Phytologist. (2004); 162 187-195
- 8 Chaves N., Rios J. J., Gutierrez C., Escudero J. C., Olias J. M.. Analysis of secreted flavonoids of Cistus ladanifer L. by high-performance liquid chromatography-particle beam mass spectrometry. Journal of Chromatography A. (1998); 799 111-115
- 9 Chu C. C., Freeman T. P., Buckner J. S., Henneberry T. J., Nelson D. R., Natwick E. T.. Susceptibility of upland cotton cultivars to Bemisia tabaci biotype B (Homoptera: Aleyrodidae) in relation to leaf age and trichome density. Annals of the Entomological Society of America. (2001); 94 743-749
- 10 Coley P. D., Bryant J. P., Chapin III. F. S.. Resource availability and plant antiherbivore defense. Science. (1985); 230 895-899
- 11 Day T. A., Martin G., Vogelmann T. C.. Penetration of UV‐B radiation in foliage: evidence that the epidermis behaves as a non-uniform filter. Plant, Cell and Environment. (1993); 16 735-741
- 12 Demmig-Adams B., Adams III. W. W.. Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology. (1992); 43 599-626
- 13 Ehleringer J., Björkman O., Mooney H. A.. Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science. (1976); 192 376-377
-
14 Ehleringer J., Comstock J..
Leaf absorptance and leaf angle: mechanisms of stress avoidance. Tenhunen, J. D., Catarino, F. M., Lange, O. L., and Oechel, W. L., eds. Plant Response to Stress. Berlin; Springer-Verlag (1987): 55-76 - 15 El-Toumy S. A. A., Rauwald H. W.. Two ellagitannins from Punica granatum heartwood. Phytochemistry. (2002); 61 971-974
- 16 Fahn A.. Structural and functional properties of trichomes of xeromorphic leaves. Annals of Botany. (1986); 57 631-637
- 17 Fahn A.. Secretory tissues in vascular plants. New Phytologist. (1988); 108 229-257
- 18 Fahn A.. Structure and function of secretory cells. Advances in Botanical Research. (2000); 31 219-238
- 19 Farley R. A., McNeilly T.. Diversity and divergence in Cistus salvifolius (L.) populations from contrasting habitats. Hereditas. (2000); 132 183-192
- 20 Feild T. S., Sage T. L., Czerniak C., Iles W. J. D.. Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation-induced flooding of the mesophyll. Plant, Cell and Environment. (2005); 28 1179-1190
- 21 Fordyce J. A., Agrawal A. A.. The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. Journal of Animal Ecology. (2001); 70 997-1005
- 22 Gitz D. C., Liu-Gitz L.. How do UV photomorphogenic responses confer water stress tolerance?. Photochemistry and Photobiology. (2003); 78 529-534
- 23 Grant O. G., Incoll L. D.. Photochemical efficiency is an important component of ecophysiological variation of Cistus albidus between habitats in south-east Spain. Functional Plant Biology. (2005); 32 107-115
- 24 Gülz P.-G., Herrmann T., Hanqst K.. Leaf trichomes in the genus Cistus. Flora. (1996); 191 85-104
- 25 Gutschick V. P.. Biotic and abiotic consequences of differences in leaf structure. New Phytologist. (1999); 143 3-18
- 26 Johnson H. B.. Plant pubescence: an ecological perspective. The Botanical Review. (1975); 41 233-258
- 27 Harley P. C., Tenhunen J. D., Beyschlag W., Lange O. L.. Seasonal changes in net photosynthetic capacity in leaves of Cistus salvifolius, a European Mediterranean semi-deciduous shrub. Oecologia. (1987); 74 380-388
- 28 Hättenschwiler S., Vitousek P. M.. The role of polyphenols in terrestrial ecosystems nutrient cycling. Trends in Ecology and Evolution. (2000); 15 238-243
- 29 Ishida T. A., Hattori K., Sato H., Rimura M. T.. Differentiation and hybridization between Quercus crispula and Quercus dentata (Fagaceae): insights from morphological traits, amplified fragment length polymorphism markers, and leafminer composition. American Journal of Botany. (2003); 90 769-776
- 30 Karabourniotis G., Papadopoulos K., Papamarkou M., Manetas Y.. Ultraviolet-B radiation absorbing capacity of leaf hairs. Physiologia Plantarum. (1992); 86 414-418
- 31 Karabourniotis G., Kotsabassidis D., Manetas Y.. Trichome density and its protective potential against ultraviolet-B radiation damage during leaf development. Canadian Journal of Botany. (1994); 73 376-383
- 32 Karabourniotis G., Kofidis G., Fasseas C., Liakoura V., Drossopoulos M.. Polyphenol deposition in leaf hairs of Olea europaea (Oleaceae) and Quercux ilex (Fagaceae). American Journal of Botany. (1998); 85 1007-1012
- 33 Karabourniotis G., Bornman J. F.. Penetration of UV‐A, UV‐B and blue light through the leaf trichome layers of two xeromorphic plants, olive and oak, measured by optical fibre microprobes. Physiologia Plantarum. (1999); 105 655-661
- 34 Lee K. D. W., Graham R.. Leaf optical properties of rainforest sun and extreme shade plants. American Journal of Botany. (1986); 73 1100-1108
- 35 Levin D. A.. The role of trichomes in plant defense. Quarterly Review of Plant Biology. (1973); 48 3-15
- 36 Liakopoulos G., Stavrianakou S., Karabourniotis G.. Analysis of epicuticular phenolics of Prunus persica and Olea europaea leaves: evidence for the chemical origin of the UV-induced fluorescence of stomata. Annals of Botany. (2001); 87 641-648
- 37 Liakopoulos G., Karabourniotis G.. Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. Tree Physiology. (2005); 25 307-315
- 38 Ludlow M. M., Björkman O.. Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions: damage by excessive light and heat. Planta. (1984); 161 505-518
- 39 Machado T. B., Leal I. C. R., Amaral A. C. F., dos Santos K. R. N., da Silva M. G., Kuster R. M.. Antimicrobial ellagitannin of Punica granatum fruits. Journal of the Brazilian Chemical Society. (2002); 13 606-610
- 40 Manetas Y.. The importance of being hairy: the adverse effects of hair removal on stem photosynthesis of Verbascum speciosum are due to solar UV‐B radiation. New Phytologist. (2003); 158 503-508
-
41 Margaris N. S..
Adaptive strategies in plants dominating Mediterranean-type ecosystems. di Castri, F., Goodall, D. W., and Specht, R. I., eds. Ecosystems of the World, Vol. 11. Mediterranean-Type Shrublands. New York; Elsevier Scientific (1981): 309-315 - 42 Markham K. R., Webby R. F., Whitehouse L. A., Molloy B. P. J., Vilain C., Mues R.. Support from flavonoid glycoside distribution for the division of Podocarpus in New Zealand. New Zealand Journal of Botany. (1985); 23 1-13
- 43 Martin C. E., von Willert D. J.. Leaf epidermal hydathodes and the ecophysiological consequences of foliar water uptake in species of Crassula from Namib Desert in Southern Africa. Plant Biology. (2000); 2 229-242
- 44 Matsuki S., Sano Y., Koike T.. Chemical and physical defence in early and late leaves in three heterophyllous birch species native to Northern Japan. Annals of Botany. (2004); 93 141-147
- 45 McNally D. J., Wurms K. V., Labbé C., Bélanger R. R.. Synthesis of C-glycosyl phytoalexins as a site-specific response to fungal penetration in cucumber. Physiological and Molecular Plant Pathology. (2003); 63 293-303
- 46 Morrison L. W.. The geographical distribution of pubescence in the sea daisy, Borrichia aborescens, on Bahamian Islands. Global Ecology and Biogeography. (2002); 11 247-252
- 47 Nobel P. S.. Physicochemical and Environmental Plant Physiology, 2nd ed. San Diego; Academic Press (1999): 293-349
- 48 Northup R. R., Dahlgren R. A., McColl J. G.. Polyphenols as regulators of plant-litter-soil interactions in northern California's pygmy forest: a positive feedback?. Biogeochemistry. (1998); 42 189-220
- 49 Oliveira G., Peñuelas J.. Comparative protective strategies of Cistus albidus and Quercus ilex facing photoinhibitory winter conditions. Environmental and Experimental Botany. (2002); 47 281-289
- 50 Onyilagha J. C., Grotewold E.. The biology and structural distribution of surface flavonoids. Recent Research Development in Plant Science. (2004); 2 1-19
- 51 Pérez-Estrada L. B., Cano-Santana Z., Oyama K.. Variation in leaf trichomes of Wigandia urens: environmental factors and physiological consequences. Tree Physiology. (2002); 20 629-632
- 52 Pignatti S.. Flora d'Italia, Vol. III. Bologna, Italy; Edagricole (1982): 451-620
- 53 Sandquist D. R., Ehleringer J.. Population- and family-level variation of brittlebush (Encelia farinosa, Asteraceae) pubescence: its relation to drought and implications for selection in variable environments. American Journal of Botany. (2003); 90 1481-1486
- 54 Saracini E., Tattini M., Traversi M. L., Vincieri F. F., Pinelli P.. Simultaneous LC‐DAD and LC‐MS determination of ellagitannins, flavonoid glycosides, and acyl-glycosyl flavonoids in Cistus salvifolius leaves. Chromatographia. (2005); 62 245-249
- 55 Schnitzler H.-P., Junglubt T. P., Heller W., Kofferlein K., Hutzler P., Heinzmann U., Schmelzer E., Ernst D., Langebartels C., Sandermann Jr. H.. Tissue localization of UV‐B screening pigments and chalcone synthase mRNA in needles of Scots pine seedlings. New Phytologist. (1996); 132 247-258
- 56 Skaltsa H., Verykokidou E., Harvala C., Karabourniotis G., Manetas Y.. UV‐B protective potential and flavonoid content of leaf hairs of Quercus ilex. Phytochemistry. (1994); 37 987-990
-
57 Southwood T. R. E..
Plant surfaces and insects - an overwiew. Juniper, B. and Southwood, T. R. E., eds. Insects and the Plant Surface. London; Edward Arnold (1986): 1-22 - 58 Stephanou M., Manetas Y.. The effect of season, exposure, enhanced UV‐B radiation, and water stress on leaf epicuticular and internal UV‐B absorbing capacity of Cistus creticus: a Mediterranean field study. Journal of Experimental Botany. (1997); 48 1977-1985
- 59 Strack D., Heilemann J., Mömken M., Wray V.. Cell wall-conjugated phenolics from Coniferae leaves. Phytochemistry. (1988); 27 3517-3521
- 60 Tattini M., Gravano E., Pinelli P., Mulinacci N., Romani A.. Flavonoids accumulate in leaves and glandular trichomes of Phillyrea latifolia exposed to excess solar radiation. New Phytologist. (2000); 148 69-77
- 61 Tattini M., Guidi L., Morassi-Bonzi L., Pinelli P., Remorini D., Degl'Innocenti E., Giordano C., Massai R., Agati G.. On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytologist. (2005); 167 457-470
- 62 Tattini M., Remorini D., Pinelli P., Agati G., Saracini E., Traversi M. L., Massai R.. Morpho-anatomical, physiological and biochemical adjustemnts in response to root zone salinity stress and high solar radiation in two Mediterranean sclerophyll shrubs, Myrtus communis and Pistacia lentiscus. New Phytologist. (2006); 170 779-794
-
63 Theobald N. L., Khaulik J. I., Rollins R. C..
Trichome description and classification. Metcalfe, C. R. and Chalk, L., eds. Anatomy of the Dicotyledons, 2nd ed., Vol. I. Oxford; Clarendon Press (1983): 40-53 - 64 Treutter D.. Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology. (2005); 7 581-591
- 65 Valkama E., Salminen J.-P., Koricheva J., Pihlaja K.. Comparative analysis of leaf trichome structures and composition of epicuticular flavonoids in Finnish birch species. Annals of Botany. (2003); 91 643-655
- 66 Vogt T., Proksch P., Gülz P.-G.. Epicuticular flavonoid aglycones in the genus Cistus (Cistaceae). Journal of Plant Physiology. (1987); 131 25-36
- 67 Vogt T., Gülz P.-G.. Accumulation of flavonoids during leaf development in Cistus laurifolius. Phytochemistry. (1994); 36 591-597
- 68 Wagner G. J., Wang E., Shepherd R. W.. New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany. (2004); 93 3-11
- 69 Wiegand K. M.. The relation of hairy and cutinized coverings to transpiration. Botanical Gazette. (1910); 4 430-444
- 70 Wollenweber E., Dietz V. H.. Occurrence and distribution of free flavonoid aglycones in plants. Phytochemistry. (1981); 20 869-932
M. Tattini
Istituto per la Valorizzazione del Legno e delle Specie Arboree (IVALSA)
Consiglio Nazionale delle Ricerche
Via Madonna del Piano
50019, Sesto F.no, Firenze
Italy
Email: m.tattini@ivalsa.cnr.it
Editor: J. T. M. Elzenga