Protective and defensive roles of non-glandular trichomes against multiple stresses: structure–function coordination

Abstract

As superficial structures, non-glandular trichomes, protect plant organs against multiple biotic and abiotic stresses. The protective and defensive roles of these epidermal appendages are crucial to developing organs and can be attributed to the excellent combination of suitable structural traits and chemical reinforcement in the form of phenolic compounds, primarily flavonoids. Both the formation of trichomes and the accumulation of phenolics are interrelated at the molecular level. During the early stages of development, non-glandular trichomes show strong morphological similarities to glandular ones such as the balloon-like apical cells with numerous phenolics. At later developmental stages, and during secondary wall thickening, phenolics are transferred to the cell walls of the trichomes. Due to the diffuse deposition of phenolics in the cell walls, trichomes provide protection against UV-B radiation by behaving as optical filters, screening out wavelengths that could damage sensitive tissues. Protection from strong visible radiation is also afforded by increased surface light reflectance. Moreover, the mixtures of trichome phenolics represent a superficial chemical barrier that provides protection against biotic stress factors such as herbivores and pathogens. Although the cells of some trichomes die at maturity, they can modulate their quantitative and qualitative characteristics during development, depending on the prevailing conditions of the external biotic or abiotic environment. In fact, the structure and chemical constituents of trichomes may change due to the particular light regime, herbivore damage, wounding, water stress, salinity and the presence of heavy metals. Hence, trichomes represent dynamic protective structures that may greatly affect the outcome of many plant–environment interactions.

Keywords

Non-glandular trichomes / Phenolics / Flavonoids / Protection / Defence / Biotic stress / Abiotic stress

References

[1] Agati G, Tattini M. Multiple functional roles of flavonoids in photoprotection. New Phytol, 2010, 186(4): 786-793.

[2] Agati G, Azzarello E, Pollastri S, Tattini M. Flavonoids as antioxidants in plants: location and functional significance. Plant Sci, 2012, 196: 67-76.

[3] Ager FJ, Ynsa JR, Dominguez-Solis Lopez-Martin MC, Gotor C, Romero LC. Nuclear micro-probe analysis of Arabidopsis thaliana leaves. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater At, 2003, 210: 401-406.

[4] Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE, Sparks JP. Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol, 2009, 183: 848-867.

[5] Agrios G. Plant pathology, 2005 5 London: Academic Press 952

[6] Allen EA, Hoch HC, Steadman JR, Stavely RG. Andrews JH, Hirano SS. Influence of leaf surface on spore deposition and the epiphytic growth of phytopathogenic fungi. Microbial ecology of leaves, 1991, New York: Springer 87 110

[7] Amada G, Onoda Y, Ichie T, Kitayama K. Influence of leaf trichomes on boundary layer conductance and gas-exchange characteristics in Metrosideros polymorpha (Myrtaceae). Biotropica, 2017, 49: 482-492.

[8] Baur R, Binder S, Benz G. Non glandular leaf trichomes as short-term inducible defence of the grey alder, Alnus incana (L.), against the chrysomelid beetle Agelastica alni L.. Oecologia, 1991, 87: 219-226.

[9] Bickford CP. Ecophysiology of leaf trichomes. Funct Plant Biol, 2016, 43(9): 807-814.

[10] Bisba A, Petropoulou Y, Manetas Y. The transiently pubescent young leaves of plane (Platanus orientalis) are deficient in photodissipative capacity. Physiol Plant, 1997, 101: 373-378.

[11] Blamey FPC, Joyce DC, Edwards DG, Asher CJ. Role of trichomes in sunflower tolerance to manganese toxicity. Plant Soil, 1986, 91: 171-180.

[12] Boeger MRT, Alves LC, Negrelle RRB. Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Braz Arch Biol Technol, 2004, 47: 933-943.

[13] Bongers F, Popma J. Leaf characteristics of the tropical rain forest flora of Los Tuxtlas, Mexico. Bot Gaz, 1990, 151: 354-365.

[14] Boughalleb F, Hajlaoui H. Physiological and anatomical changes induced by drought in two olive cultivars (cv. Zalmati and Chemlali). Acta Physiol Plant, 2011, 33: 53-65.

[15] Bradley DJ, Gilbert GS, Parker IM. Susceptibility of clover species to fungal infection: the interaction of leaf surface traits and environment. Am J Bot, 2003, 90: 857-864.

[16] Broadhurst CL, Chaney RL, Angle JS, Maugel TK, Erbe EF, Murphy CA. Simultaneous hyperaccumulation of nickel, manganese, and calcium in Alyssum leaf trichomes. Environ Sci Technol, 2004, 38: 5797-5802.

[17] Calixto ES, Lange D, Del-Claro K. Foliar anti-herbivore defences in Qualea multiflora Mart. (Vochysiaceae): changing strategy according to leaf development. Flora, 2015, 212: 19-23.

[18] Carletti G, Nervo G, Cattivelli L. Flavonoids and melanins: a common strategy across two kingdoms. Int J Biol Sci, 2014, 10: 1159-1170.

[19] Çelik Ö, Atak Ç, Suludere Z. Comparative transcriptional profiling of soybean orthologs of Arabidopsis trichome developmental genes under salt stress. Plant Mol Biol Report, 2018, 36: 82-93.

[20] Dalin P, Ågren J, Bjorkman C, Huttunen P, Kärkkäinen K. Schaller A. Leaf trichome formation and plant resistance to herbivory. Induced plant resistance to herbivory, 2008, Berlin: Springer 89 105

[21] De Nicola F, Maisto G, Prati MV, Alfani A. Leaf accumulation of trace elements and polycyclic hydrocarbons (PAHs) in Quercus ilex L. Environ Pollut, 2008, 153: 376-383.

[22] De Silva LD, Mansfield TA, McAinsh MR. Changes in stomatal behaviour in the calcicole Leontodon hispidus due to the disruption by ozone of the regulation of apoplastic Ca²⁺ by trichomes. Planta, 2001, 214: 158-162.

[23] Demmig-Adams B, Adams WW. An integrative approach to photoinhibition and photoprotection of photosynthesis. Environ Exp Bot, 2018, 154: 1-3.

[24] Domínguez-Solís JR, López-Martín MC, Ager FJ, Ynsa MD, Romero LC, Gotor C. Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotech J, 2004, 2(6): 469-476.

[25] Ehleringer JR. Healy PL, Mehta I, Rodriguez E. Ecology and ecophysiology of leaf pubescence in North America desert plants. Biology and chemistry of plant trichomes, 1984, New York: Plenum Publishing Corporation 113 132

[26] El-Negoumy SI, Abdalla MF, Saleh NAM. Flavonoids of Phlomis aurea and P. floccosa. Phytochemistry, 1986, 25: 772-774.

[27] Fahn A. Structural and functional properties of trichomes of xeromorphic leaves. Ann Bot, 1986, 57: 631-637.

[28] Fahn A, Cutler D. Xerophytes, 1992, Berlin: Gebruder Borntraeger 176

[29] Fernadez S, Osorio S, Heredia A. Monitoring and visualising plant cuticles by confocal laser scanning microscopy. Plant Physiol Biochem, 1999, 37: 789-794.

[30] Fernández V, Khayet M, Montero-Prado P, Heredia-Guerrero J, Liakopoulos G, Karabourniotis G, del Río V, Domínguez E, Tacchini I, Nerín C, Val J, Heredia A. New insights into the properties of pubescent surfaces: peach fruit as a model. Plant Phys, 2011, 156: 2098-2108.

[31] Fernández V, Sancho-Knapik D, Guzmán P, Peguero-Pina JJ, Gil L, Karabourniotis G, Khayet M, Fasseas C, Heredia-Guerrero JA, Heredia A, Gil-Pelegrín E. Wettability, polarity, and water absorption of holm oak leaves: effect of leaf side and age. Plant Phys, 2014, 166: 168-180.

[32] Fu QS, Yang RC, Wang HS, Zhao B, Zhou CL, Ren SX, Guo Y-D. Leaf morphological and ultrastructural performance of eggplant (Solanum melongena L.) in response to water stress. Photosynthetica, 2013, 51(1): 109-114.

[33] Galati BG. Ontogenia de los trichomes de Olea europaea L. (Oleaceae). Physis (B. Aires), 1982, 41: 65-71.

[34] Galdon-Armero J, Fullana-Pericas M, Mulet PA, Conesa MA, Martin C, Galmes J. The ratio of trichomes to stomata is associated with water use efficiency in Solanum lycopersicum (tomato). Plant J, 2018, 96: 607-619.

[35] Galmés J, Medrano H, Flexas J. Photosynthesis and photoinhibition in response to drought in a pubescent (var. minor) and a glabrous (var. palaui) variety of Digitalis minor. Environ Exp Bot, 2007, 60: 105-111.

[36] Goodwin RH. Fluorescence substances in plants. Bot Rev, 1952, 3: 283-304.

[37] Grace SC. Smirnoff N. Phenolics as antioxidants. Antioxidants and reactive oxygen species in plants, 2007, Hoboken: Blackwell 141 196

[38] Grammatiκopoulos G, Karabourniotis G, Kyparissis A, Petropoulou Y, Manetas Y. Leaf hairs of olive (Olea europaea L.) prevent stomatal closure by ultraviolet-B radiation. Aust J Plant Physiol, 1994, 21: 293-301.

[39] Grubb PJ, Grubb EAA, Miyata I. Leaf structure and function in evergreen trees and shrubs of Japanese warm temperate rain forest. I. The structure of the lamina. Bog Mag Tokyo, 1975, 88: 197-211.

[40] Hättenschwiler S, Vitousek PM. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol, 2000, 15: 238-243.

[41] Hauser M-T. Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci, 2014, 5: 320.

[42] Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q Rev Biol, 1992, 67: 283-335.

[43] Holmes M, Keiller D. Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant Cell Environ, 2002, 25: 85-93.

[44] Howsam M, Jones KC, Ineson P. PAHs associated with leaves of three deciduous tree species. I - Concentrations and profiles. Environ Pollut, 2000, 108: 413-424.

[45] Hu YB, Peuke AD, Zhao XY, Yan JX, Li CM. Effects of simulated atmospheric nitrogen deposition on foliar chemistry and physiology of hybrid poplar seedlings. Plant Physiol Biochem, 2019, 143: 94-108.

[46] Huchelmann A, Boutry M, Hachez C. Plant glandular trichomes: natural cell factories of high biotechnological interest. Plant Phys, 2017, 175(1): 6-22.

[47] Hützler P, Fieschbach R, Heller W, Jungblut TP, Reuber S, Schmitz M, Veit M, Weissenboeck G, Schnitzler J-P. Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J Exp Bot, 1998, 49: 953-965.

[48] Ichie T, Inoue Y, Takahashi N, Kamiya K, Kenzo T. Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. J Plant Res, 2016, 129: 625-635.

[49] Inderjit K, Cheng HH, Nishimura H. Inderjit K, Dakshini MM, Foy CL. Plant Phenolics and terpenoids: transformation, degradation and potential for allelopathic interactions. Principles and practices in plant ecology, 1999, Boca Raton: CRC Press 255 266

[50] Iwashina T. Flavonoid function and activity to plants and other organisms. Biol Sci Space, 2003, 17: 24-44.

[51] Jansen MA, Coffey AM, Prinsen E. UV-B induced morphogenesis: four players or a quartet?. Plant Signal Behav, 2012, 7: 1185-1187.

[52] Johnson HB. Plant pubescence: an ecological perspective. Bot Rev, 1975, 41: 233-258.

[53] Jordheim M, Calcott K, Gould KS, Davies KM, Schwinn KE, Andersen ØM. High concentrations of aromatic acylated anthocyanins found in cauline hairs in Plectranthus ciliates. Phytochemistry, 2016, 128: 27-34.

[54] Jud W, Fischer L, Canaval E, Wohlfahrt G, Tissier A, Hansel A. Plant surface reactions: an ozone defence mechanism impacting atmospheric chemistry. Atmos Chem Phys, 2016, 16: 277-292.

[55] Karabourniotis G, Bornman JF. 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. Phys Plant, 1999, 105: 655-661.

[56] Karabourniotis G, Fasseas C. The dense indumentum with its polyphenol content may replace the protective role of the epidermis in some young xeromorphic leaves. Can J Bot, 1996, 74: 347-351.

[57] Karabourniotis G, Liakopoulos G. Phenolic compounds in plant cuticles: physiological and ecological aspects. Adv Plant Phys, 2005, 8: 33-47.

[58] Karabourniotis G, Papadopoulos K, Papamarkou M, Manetas Y. Ultraviolet-B radiation absorbing capacity of leaf hairs. Phys Plant, 1992, 86: 414-418.

[59] Karabourniotis G, Kyparissis A, Manetas Y. Leaf hairs of Olea europaea L. protect underlying tissues against ultraviolet-B radiation damage. Environ Exp Bot, 1993, 33: 341-345.

[60] Karabourniotis G, Kotsabassidis D, Manetas Y. Trichome density and its protective potential against ultraviolet-B radiation damage during leaf development. Can J Bot, 1995, 73: 376-383.

[61] Karabourniotis G, Kofidis G, Fasseas C, Liakoura V, Drossopoulos I. Polyphenol deposition in leaf hairs of Olea europaea (Oleaceae) and Quercus ilex (Fagaceae). Am J Bot, 1998, 85: 1007-1012.

[62] Karabourniotis G, Bornman JF, Liakoura V. Different leaf surface characteristics of three grape cultivars affect leaf optical properties as measured with fibre optics. Possible implication in Stress tolerance. Aust J Plant Phys, 1999, 26: 47-53.

[63] Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P, Stavroulaki V, Sumbele S. Carbon gain vs. water saving, growth vs. defence: two dilemmas with soluble phenolics as a joker. Plant Sci, 2014, 227: 21-27.

[64] Karioti A, Tooulakou G, Bilia AR, Psaras GK, Karabourniotis G, Skaltsa H. Erinea formation on Quercus ilex leaves: anatomical, physiological and chemical responses of leaf hairs against mite attack. Phytochemistry, 2011, 72: 230-237.

[65] Konrad W, Burkhardt J, Ebner M, Roth-Nebelsick A. Leaf pubescence as a possibility to increase water use efficiency by promoting condensation. Ecohydrology, 2014, 8: 480-492.

[66] Körner C. Alpine plant life, 2003, Berlin: Springer, Berlin 338

[67] Kortekamp A, Zyprian E. Leaf hairs as a basic protective barrier against downy mildew of grape. J Phytopathol, 1999, 147: 453-459.

[68] Kortekamp A, Wind R, Zyprian E. The role of hairs on the wettability of grapevine (Vitis spp.) leaves. Vitis, 1999, 38: 101-105.

[69] Koudounas K, Manioudaki ME, Kourti A, Banilas G, Hatzopoulos P. Transcriptional profiling unravels potential metabolic activities of the olive leaf non-glandular trichome. Front Plant Sci, 2015, 6: 633.

[70] Koul M, Bhatnagar AK. Changes in the leaf epidermal features of Cyamopsis tetragonoloba (L.) Taub. in response to lead in soil. Phytomorphology, 2017, 67: 1-1.

[71] Krämer U, Grime GW, Smith JAC, Hawes CR, Baker AJM. Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nucl Instrum Methods Phys Res B, 1997, 130(1): 346-350.

[72] Krimmel BA. Why plant trichomes might be better than we think for predatory insects. Pest Manag Sci, 2014, 70(11): 1666-1667.

[73] Kulich I, Vojtíková Z, Glanc M, Ortmannová J, Rasmann S, Zárský V. Cell wall maturation of Arabidopsis trichomes is dependent on exocyst subunit EXO70H4 and involves callose deposition. Plant Phys, 2015, 168: 120-131.

[74] Küpper H, Lombi E, Zhao FJ, McGrath SP. Cellular compartmentation of cadmium and zinc in relation to other metals in the hyperaccumulator Arabidopsis halleri. Planta, 2000, 212: 75-84.

[75] Lang M, Schindler C. The effect of leaf-hairs on blue and red fluorescence emission and on zeaxanthin cycle performance of Senecio medley L. J Plant Phys, 1994, 144: 680-685.

[76] Lange BM, Srividya N. Enzymology of monoterpene functionalization in glandular trichomes. J Exp Bot, 2019, 70: 1095-1108.

[77] Larkin JC, Young N, Prigge M, Marks MD. The control of trichome spacing and number in Arabidopsis. Development, 1996, 122: 997-1005.

[78] Levin DA. The role of trichomes in plant defence. Q Rev Biol, 1973, 48: 3-14.

[79] Li S, Tosens T, Harley PC, Harley PC, Jiang Y, Kanagendran A, Grosberg M, Jaamets K, Niinemets Ü. Glandular trichomes as a barrier against atmospheric oxidative stress: relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species. Plant Cell Environ, 2018, 41: 1263-1277.

[80] Liakopoulos G, Nikolopoulos D, Klouvatou A, Vekkos KA, Manetas Y, Karabourniotis G. The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). Ann Bot, 2006, 98: 257-265.

[81] Liakopoulos G, Stavrianakou S, Karabourniotis G. Trichome layers versus dehaired lamina of Olea europaea leaves: differences in flavonoid distribution, UV-absorbing capacity, and wax yield. Environ Exp Bot, 2006, 55: 294-304.

[82] Liakoura V, Stefanou M, Manetas Y, Cholevas C, Karabourniotis G. Trichome density and iIts UV-B protective potential are affected by shading and leaf position on the canopy. Environ Exp Bot, 1997, 38: 223-229.

[83] Little P, Wiffen RD. Emissions and deposition of petrol engine exhaust Pb-I. Deposition of exhaust Pb to plant and soil surface. Atmos Environ, 1977, 11: 437-447.

[84] Liu X, Liu C. Effects of drought-stress on Fusarium crown rot development in barley. PLOS ONE, 2016, 11: e0167304.

[85] Liu H, Liu S, Jiao J, Lubc TJ, Xu F. Trichomes as a natural biophysical barrier for plants and their bioinspired applications. Soft Matter, 2017, 13: 5096-5106.

[86] Liu S, Jiao J, Lu TJ, Xu F, Pickard BG, Genin GM. Arabidopsis leaf trichomes as acoustic antennae. Biophys J, 2017, 113: 2068-2076.

[87] LoPresti EF. Chemicals on plant surfaces as a heretofore unrecognized, but ecologically informative, class for investigations into plant defence. Biol Rev, 2015, 91: 1102-1117.

[88] Mandal D, Chakrabotry S, Dey S. Phenolic acids act as signalling molecules in plant-microbe symbioses. Plant Signal Behav, 2010, 5: 359-368.

[89] 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 Phytol, 2003, 158: 503-508.

[90] Mateu BP, Hauser MT, Heredia A, Gierlinger N. Waterproofing in Arabidopsis: following phenolics and lipids in situ by confocal raman microscopy. Front Chem, 2016, 4: 10.

[91] Mershon JP, Becker M, Bickford CP. Linkage between trichome morphology and leaf optical properties in New Zealand alpine Pachycladon (Brassicaceae). New Zeal J Bot, 2015, 53: 175-182.

[92] Michalak A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Stud, 2006, 15(4): 523-530.

[93] Mierziak J, Kostyn K, Kulma A. Flavonoids as important molecules of plant interactions with the environment. Molecules, 2014, 19: 16240-16265.

[94] Mithöfer A, Maffei ME. Gopalakrishnakone P, Carlini CR, Ligabue-Braun R. General mechanisms of plant defense and plant toxins. plant toxins, 2016, Berlin: Springer 1 22

[95] Mmbaga MT, Steadman JR. Adult-plant resistance associated with leaf pubescence in common bean. Plant Dis, 1992, 76: 1230-1236.

[96] Mmbaga MT, Steadman JR, Roberts JJ. Interaction of bean leaf pubescence with rust urediniospore deposition and subsequent infection density. Ann Appl Biol, 1994, 125: 243-254.

[97] Morales F, Abadía A, Abadía J, Montserrat G, Gil-Pelegrín E. Trichomes and photosynthetic pigment composition changes: responses of Quercus ilex subsp. ballota (Desf.) Samp. and Quercus coccifera L. to Mediterranean stress conditions. Trees, 2002, 16: 504-510.

[98] Moreno L, Bertiller MB, Carrera AL. Changes in traits of shrub canopies across an aridity gradient in northern Patagonia, Argentina. Basic Appl Ecol, 2010, 11: 693-701.

[99] Muhammad S, Wuyts K, Samson R. Atmospheric net particle accumulation on 96 plant species with contrasting morphological and anatomical leaf characteristics in a common garden experiment. Atmos Env, 2019, 202: 328-344.

[100] Nobel PS. Biophysical plant physiology and ecology, 1983, San Francisco: WH Freeman and Co.

[101] Ntefidou M, Manetas Y. Optical properties of hairs during the early stages of leaf development in Platanus orientalis. Aust J Plant Physiol, 1996, 23: 535-538.

[102] Oksanen E. Trichomes form an important first line of defence against adverse environment—new evidence for ozone stress mitigation. Plant Cell Environ, 2018, 41: 1497-1499.

[103] Pourcel L, Routaboul J-M, Cheynier V, Lepiniec L, Debeaujon I. Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci, 2006, 12: 29-36.

[104] Pringle EG, Adams RI, Broadbent E, Busby PE, Donatti CI, Kurten EL, Renton K, Dirzo R. Distinct leaf-trait syndromes of evergreen and deciduous trees in a seasonally dry tropical forest. Biotropica, 2011, 43: 299-308.

[105] Prozherina N, Freiwald V, Rousi M, Oksanen E. Interactive effect of springtime frost and elevated ozone on early growth, foliar injuries and leaf structure of birch (Betula pendula). New Phytol, 2003, 159: 623-636.

[106] Psaras GK, Constantinidis TH, Cotsopoulos B, Manetas Y. Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Ann Bot, 2000, 86: 73-78.

[107] Pshenichnikova TA, Doroshkov AV, Osipova SV, Permyakov AV, Permyakova MD, Efimov VM, Afonnikov DA. Quantitative characteristics of pubescence in wheat (Triticum aestivum L.) are associated with photosynthetic parameters under conditions of normal and limited water supply. Planta, 2019, 249: 839-847.

[108] Pyykkö M. Morphology and anatomy of leaves from some woody plants in a humid tropical rainforest of Venezuelan Guayana. Acta Bot Fenn, 1979, 112: 1-41.

[109] Quideau SP, Deffieux D, Douat-Casassus CL, Pouységu L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem Int Ed, 2011, 50: 586-621.

[110] Ram SS, Majumder S, Chaudhuri P, Chanda S, Santra SC, Chakraborty A, Sudarshan M. A review on air pollution monitoring and management using plants with special reference to foliar dust adsorption and physiological stress responses. Crit Rev Environ Sci Technol, 2015, 45(23): 2489-2522.

[111] Reigosa MJ, Sánchez-Moreiras A, González L. Ecophysiological approach in allelopathy. Crit Rev Plant Sci, 1999, 18: 577-608.

[112] Rennberger G, Keinath AP, Hess M. Correlation of trichome density and length and polyphenol fluorescence with susceptibility of five cucurbits to Didymella bryoniae. J Plant Dis Prot, 2017, 124: 313.

[113] Riddick EW, Simmons AM. Do plant trichomes cause more harm than good to predatory insects?. Pest Manag Sci, 2014, 70: 1655-1665.

[114] Ripley BS, Pammenter NW, Smith VR. Function of leaf hairs revisited: the hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates. J Plant Phys, 1999, 155: 78-85.

[115] Roka L, Koudounas K, Daras G, Zoidakis J, Vlahou A, Kalaitzis P, Hatzopoulos P. Proteome of olive non-glandular trichomes reveals protective protein network against (a)biotic challenge. J Plant Phys, 2018, 231: 210-218.

[116] Romantschuk M, Roine E, Björklöf K, Ojanen T, Nurmiaho-Lassila E-L, Haahtela K. Morris CG, Nicot PC, Nguyen C. Microbial attachment to plant aerial surfaces. Aerial plant surface microbiology, 1996, New York: Plenum Press 43 58

[117] Rost FWD. Fluorescence microscopy, 1995, New York: Cambridge University Press.

[118] Roth I. Stratification of tropical forests as seen in leaf structure, 1984, Hague: Dr W Junk Publishers 246

[119] Sæbø A, Popek R, Nawrot B, Hanslin HM, Gawronska H, Gawronski SW. Plant species differences in particulate matter accumulation on leaf surfaces. Sci Total Environ, 2012, 427–428: 347-354.

[120] Savé R, Biel C, de Herralde F. Leaf pubescence, water relations and chlorophyll fluorescence in two subspecies of Lotus Creticus L.. Biol Plant, 2000, 43: 239-244.

[121] Schreiner M, Mewis I, Huyskens-Keil S, Jansen MAK, Zrenner R, Winkler JB, O’Brien N, Krumbein A. UV-B-induced secondary plant metabolites—potential benefits for plant and human health. Crit Rev Plant Sci, 2012, 31(3): 229-240.

[122] Schuepp PH. Leaf boundary layers. New Phytol, 1993, 125: 477-507.

[123] Shirai A, Yasutomo Y-K. Bactericidal action of ferulic acid with ultraviolet-A light irradiation. J Photochem Photobiol B Biol, 2019, 191: 52-58.

[124] Siipola SM, Kotilainen T, Sipari N, Morales LO, Lindfors AV, Robson TM, Aphalo PJ. Flavonoids in sunlight. Plant Cell Environ, 2015, 38: 941-952.

[125] Skaltsa E, 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.

[126] Stavrianakou S, Liakopoulos G, Miltiadou D, Markoglou AN, Ziogas BN, Karabourniotis G. Antifungal and antibacterial capacity of extracted material from non-glandular and glandular leaf hairs applied at physiological concentrations. Plant Stress, 2010, 4(1): 25-30.

[127] Strack D, Heilemann J, Mömken M, Wray V. Cell wall-conjugated phenolics from Coniferae leaves. Phytochemistry, 1988, 27: 3517-3521.

[128] Tattini M, Matteini P, Saracini E, Traversi ML, Giordano C, Agati G. Morphology and biochemistry of non-glandular trichomes in Cistus salvifolius L. leaves growing in extreme habitats of Mediterranean basin. Plant Biol, 2007, 9: 411-419.

[129] Tian N, Liu F, Wang P, Yan X, Gao H, Zeng X, Wu G. Overexpression of BraLTP2, a lipid transfer protein of Brassica napus, results in increased trichome density and altered concentration of secondary metabolites. Int J Mol Sci, 2018, 19: 1733.

[130] Tozin LRdS, de Melo Silva SC, Rodrigues TM. Non-glandular trichomes in Lamiaceae and Verbenaceae species: morphological and histochemical features indicate more than physical protection. New Zeal J Bot, 2016, 54(4): 446-457.

[131] Traw MB, Bergelson J. Interactive effects of jasmonic acid, salicylic acid, and gibberellins on induction of trichomes in Arabidopsis. Plant Physiol, 2003, 133: 1367-1375.

[132] Uphof JCT. Plant hairs. Encycl Plant Anat IV, 1962, 5: 1-206.

[133] Václaník T, Beckmann M, Cord AF, Bindewald AM. Effects of UV-B radiation on leaf hair traits of invasive plants—combining historical herbarium records with novel remote sensing data. PLoS ONE, 2017 12 4 e0175671

[134] Valkama E, Salminen JP, Koricheva J, Pihlaja K. Changes in leaf trichomes and epicuticular flavonoids during leaf development in three birch taxa. Ann Bot, 2004, 94(2): 233-242.

[135] Vermeij GJ. Plants that lead: do some surface features direct enemy traffic on leaves and stems?. Biol J Linn Soc, 2015, 116: 288-294.

[136] Wagner GJ, Wand E, Shepherd RW. New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot, 2004, 93(1): 3-11.

[137] Werker E. Trichome diversity and development. Adv Bot Res, 2000, 31: 1-35.

[138] Weston LA, Mathesius U. Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol, 2013, 39: 283-297.

[139] Wieser G Gasche R Ozone. Trace gas exchange in forest ecosystems, 2002, New York: Kluwer Academic Publishers 211 226

[140] Xiao K, Mao X, Lin Y, Xu H, Zhu Y, Cai Q, Xie H, Zhang J. Trichome, a functional diversity phenotype in plant. Mol Biol, 2017, 6: 183.

[141] Yamasaki S, Murakami Y. Continuous UV-B irradiation induces endoreduplication and trichome formation in cotyledons, and reduces epidermal cell division and expansion in the first leaves of pumpkin seedlings (Cucurbita maxima Duch. × C. moschata Duch.). Environ Control Biol, 2014, 52: 203-209.

[142] Yamasaki S, Noguchi N, Mimaki K. Continuous UV-B irradiation induces morphological changes and the accumulation of polyphenolic compounds on the surface of cucumber cotyledons. J Radiat Res, 2007, 48: 443-454.

[143] Yan A, Pan J, An L, Gan Y, Feng H. The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. J Photochem Photobiol B Biol, 2012, 113: 29-35.

[144] Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K. Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development, 2009, 136: 1039-1048.

[145] Zeiger C, Rodrigues da Silva IC, Mail M, Kavalenka MN, Barthlott W, Hölscher H. Microstructures of superhydrophobic plant leaves—inspiration for efficient oil spill cleanup materials. Bioinspir Biomim, 2016, 11: 056003.

[146] Zhang B, Schrader A. TRANSPARENT TESTA GLABRA 1-dependent regulation of flavonoid biosynthesis. Plants, 2017, 6: 65.

[147] Zhang T-J, Chow WS, Liu X-T, Zhang P, Liu N, Peng C-L. A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition. Tree Physiol, 2016, 36: 1296-1306.

[148] Zhao F-J, Lombi E, Breedon T, McGrath SP. Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ, 2000, 23: 507-514.

[149] Zhou LH, Liu SB, Wang PF, Lu TJ, Xu F, Genin GM, Pickard BG. The Arabidopsis trichome is an active mechanosensory switch. Plant Cell Environ, 2016, 40: 611-621.