Loading...

Role of trichomes in plant defence – A crop specific review 


DOI: 10.31830/2454-1761.2022.895    | Article Id: 895 | Page : 460-475
Citation :- Role of trichomes in plant defence – A crop specific review. Crop Res. 57: 460-475
DEBARATI NANDI, ANINDA CHAKRABORTY, TUFLEUDDIN BISWAS, DURGADATTA MEHER AND ADITYA PRATAP SINGH aninda.chakraborty@cutm.ac.in
Address : Department of Agricultural and Food Engineering, Indian Institute of Technology, Kharagpur, Kharagpur-721 302 (West Bengal), India

Abstract

Trichomes have long been investigated as an initial line of defence against insect herbivores. The structure, categorization and diversity of trichomes in flowering plants, as well as their mechanisms of action against abiotic and biotic stresses, are discussed. Plant-herbivore interactions are complicated interactions involving intricate networks of chemicals, signals and tactics to overcome each other's defences. To gain nutrients from host plants, herbivores employ a variety of feeding techniques. Plants respond by activating several defence mechanisms. Context of this review is based over the research on herbivore-trichome interactions and how trichomes are involved in both direct and indirect plant defences. Importance of trichome exudates like terpenes, acyl sugars, phenyl propanoid derivatives, methyl ketones, flavonoids and defensive proteins have been discussed. In our study, we emphasized on the relevance of trichomes as a reliable indicator of plant defence and how it is involved in defence responses of some economically important crops. Finally, we suggest several promising new study avenues for future work on trichomes and trichome-mediated responses.
 

Keywords

Defence glandular trichomes nonglandular trichomes plant trichomes

References

Adie, M. M. and Krisnawati, A. (2017). Variability of pod trichome and agronomic characters of several soybean genotypes. Biodiversitas J. Biol. Diversity 18.
Agati, G. and Tattini, M. (2010). Multiple functional roles of flavonoids in photoprotection. The New Phytologist 186 : 786-93.
Bensoussan, N., Zhurov, V., Yamakawa, S., O'Neil, C. H., Suzuki, T., Grbić, M. and Grbić, V. (2018). The digestive system of the two-spotted spider mite, Tetranychus urticae Koch, in the context of the mite-plant interaction. Frontiers in Plant Sci. 9 : 1206.
Bleeker, P. M., Diergaarde, P. J., Ament, K., Schütz, S., Johne, B., Dijkink, J. and Schuurink, R. C. (2012). Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry 72 : 68-73.
Bonierbale, M. W., Plaisted, R. L., Pineda, O. and Tanksley, S. D. (1994). QTL analysis of trichome-mediated insect resistance in potato. Theoretical and Applied Gene87 : 973-87.
Chatterjee, A., Sukul, N. C., Laskar, S. and Ghoshmajumdar, S. (1982). Nematicidal principles from two species of Lamiaceae. J. Nematol14 : 118.
Dai, H., Wang, Y., Du, Y. and Ding, J. (2010). Effects of plant trichomes on herbivores and predators on soybeans. Insect Sci17 : 406-13.
Domann, E., Wehland, J., Rohde, M., Pistor, S., Hartl, M., Goebel, W. and Chakraborty, T. (1992). A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. The EMBO J. 11 : 1981-90.
Eisner, T., Eisner, M. and Hoebeke, E. R. (1998).When defence backfires : detrimental effect of a plant’s protective trichomes on an insect beneficial to the plant. Proc. National Academy of Sciences 95 : 4410-14.
Fahn, A. (2000). Structure and function of secretory cells. Adv. Bot. Res. 31 : 37-75.
Felton, G. W., Donato, K. K., Broadway, R. M. and Duffey, S. S. (1992). Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exiguaJ. Insect Physiol38 : 277-285.
Fernandes, M. J. G., Pereira, R. B., Pereira, D. M., Fortes, A. G., Castanheira, E. M. and Gonçalves, M. S. T. (2020). New eugenol derivatives with enhanced insecticidal activity. Int. J. Mole. Sci. 21 : 9257.
Fridman, E., Wang, J., Iijima, Y., Froehlich, J. E., Gang, D. R., Ohlrogge, J. and Pichersky, E. (2005). Metabolic, genomic and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones. The Plant Cell 17 : 1252-67.
Gang, D. R., Wang, J., Dudareva, N., Nam, K. H., Simon, J. E., Lewinsohn, E. and Pichersky, E. (2001). An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol125 : 539-55.
Gershenzon, J. and Croteau, R. (1992). Terpenoids. In : Herbivores : Their Interactions with Secondary Plant Metabolites, 2nd edn. vol. 1. The Chemical Participants 1 : 165-219.
Glas, J. J., Schimmel, B. C., Alba, J. M., Escobar-Bravo, R., Schuurink, R. C. and Kant, M. R. (2012). Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mole. Sci. 13 : 17077-17103.
Goffreda, J. C., Mutschler, M. A., Avé, D. A., Tingey, W. M. and Steffens, J. C. (1989). Aphid deterrence by glucose esters in glandular trichome exudate of the wild tomato, Lycopersicon pennelliiJ. Chem. Ecol15 : 2135-47.
Gregory, P., Tingey, W. M., Ave, D. A. and Bouthyette, P. Y. (1986). Potato glandular trichomes : A physico-chemical defense mechanism against insects. pp. 160-67.
Guimarães, A. C., Meireles, L. M., Lemos, M. F., Guimarães, M. C. C., Endringer, D. C., Fronza, M. and Scherer, R. (2019). Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules 24 : 2471.
Handley, R., Ekbom, B. and Agren, J. (2005). Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana. Ecol. Entomol30 : 284-92.
Harada, E., Kim, J. A., Meyer, A. J., Hell, R., Clemens, S. and Choi, Y. E. (2010). Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant and Cell Physiol51 : 1627-37.
Hedin, P. A., Jenkins, J. N. and Parrott, W. L. (1992). Evaluation of flavonoids in Gossypium arboreum (L.) cottons as potential source of resistance to tobacco budworm. J. Chem. Ecol18 : 105-14.
Hoeven, R. S., Monforte, A. J., Breeden, D., Tanksley, S. D. and Steffens, J. C. (2000). Genetic control and evolution of sesquiterpene biosynthesis in Lycopersicon esculentum and L. hirsutum. The Plant Cell 12 : 2283-94.
Horgan, F. G., Quiring, D. T., Lagnaoui, A. and Pelletier, Y. (2009). Effects of altitude of origin on trichome-mediated anti-herbivore resistance in wild Andean potatoes. Flora-Morphology, Distribution, Functional Ecology of Plants 204 : 49-62.
Huang, Y., Ho, S. H., Lee, H. C., and Yap, Y. L. (2002). Insecticidal properties of eugenol, isoeugenol and methyleugenol and their effects on nutrition of Sitophilus zeamais Motsch. (Coleoptera : Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera : Tenebrionidae). J. Stored Products Res. 38 : 403-12.
Iwashina, T. (2003). Flavonoid function and activity to plants and other organisms. Biol. Sci. in Space 17 : 24-44.
Juvik, J. A., Babka, B. A. and Timmermann, E. A. (1988). Influence of trichome exudates from species of Lycopersicon on oviposition behaviour of Heliothis zea (Boddie). J. Chem. Ecol14 : 1261-78.
Karabourniotis, G., Liakopoulos, G., Nikolopoulos, D., Bresta, P., Stavroulaki, V. and Sumbele, S. (2014). “Carbon gain vs. water saving, growth vs. defence” : two dilemmas with soluble phenolics as a joker. Plant Sci227 : 21-27.
Koudounas, K., Manioudaki, M., Kourti, A., Banilas, G. and Hatzopoulos, P. (2015). Transcriptional profiling unravels potential metabolic activities of the olive leaf non-glandular trichome. Frontiers in Pl. Sci6 : 633.
Kroumova, A. B. and Wagner, G. G. (2003). Different elongation pathways in the biosynthesis of acyl groups of trichome exudate sugar esters from various solanaceous plants. Planta. 216 : 1013-21.
Lam, W. K. F. and Pedigo, L. P. (2001). Effect of trichome density on soybean pod feeding by adult bean leaf beetles (Coleoptera : Chrysomelidae). J. Econ. Entomol. 94 : 1459-63.
Li, A. X. and Steffens, J. C. (2000). An acyltransferase catalyzing the formation of diacylglucose is a serine carboxipeptidase-like protein. Proc. Natl. Acad. Sci. 97 : 6902-07.
Lin, S. Y. H. and Trumble, J. T. (1986). Resistance in wild tomatoes to larvae of a specialist herbivore, Keiferia lycopersicellaEntomologia Experimentalis et Applicata 41 : 53-60.
Lovinger, A., Liewehr, D. and Lamp, W. O. (2000). Glandular trichomes on alfalfa impede searching behaviour of the potato leafhopper parasitoid. Biol. Control 18 : 187-92.
Luu, V. T., Weinhold, A., Ullah, C., Dressel, S., Schoettner, M., Gase, K. and Baldwin, I. T. (2017). O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore. Plant Physiol. 174 : 370-86.
Mak, K. K., Kamal, M., Ayuba, S., Sakirolla, R., Kang, Y. B., Mohandas, K. and Pichika, M. (2019). A comprehensive review on eugenol's antimicrobial properties and industry applications : A transformation from ethnomedicine to industry. Pharmacognosy Reviews 13 : 1-9.
Mathesius, U. (2018). Flavonoid functions in plants and their interactions with other organisms. Plants 7 : 30.
Mierziak, J., Kostyn, K. and Kulma, A. (2014). Flavonoids as important molecules of plant interactions with the environment. Molecules 19 : 16240-65.
Miyao, S. (1975). Inhibitory effects of ethanol extract of mace and eugenol on the growth of micro-organisms isolated from Vienna sausages. Food Hygiene and Safety Science (Shokuhin eiseigaku Zasshi). 16 : 412-16.
Moudgal, R., Lakra, R., Dahiya, B. and Dhillon, M. (2008). Physico-chemical traits of Cajanus cajan (L.) Mill sp. pod wall affecting Melanagromyza obtusa (Malloch) damage. Euphytica 161 : 429-36.
Mourey, A. and Canillac, N. J. F. C. (2002). Anti-listeria monocytogenes activity of essential oils components of conifers. Food Control 13 : 289-92.
Nasiou, E. and Giannakou, I. O. (2020). The potential of eugenol as a nematicidal agent against (Treub) Chitwood. J. Nematol. 52 : 1-10.
Nayidu, N. K., Bonham-Smith, P. and Gruber, M. (2015). Brassica villosa–a potential tool to improve the insect or disease resistance of brassica crop species. Transcriptomics 3 : 2.
Nepi, M., Grasso, D. A. and Mancuso, S. (2018). Nectar in plant-insect mutualistic relationships : From food reward to partner manipulation. Frontiers in Plant Science 9 : 1063.
Obeng-Ofori, D. E. and Reichmuth, C. H. (1997). Bioactivity of eugenol–A major component of essential oil of Ocimum suave (Wild.) against four species of stored-product coleoptera. Int. J. Pest Manage43 : 89-94.
Palaniswamy, P. and Bodnaryk, R. P. (1994). A wild brassica from Sicily provides trichome-based resistance against flea beetles, Phyllotreta cruciferae (Goeze) (Coleoptera : Chrysomelidae). The Canadian Entomologist 126 : 1119-30.
Patil, S. D., Padhye, A. P. and Katare, S. (2016). Resistance sources for wheat aphid : An update. Int. J. Plant Prot9 : 628-31.
Pelletier, Y., Horgan, F. G. and Pompon, J. (2013). Potato resistance against insect herbivores : Resources and opportunities. Insect-pests of Potato : Global Perspectives on Biology and Management. pp. 439-62.
Puterka, G. J. and Severson, R. F. (1995). Activity of sugar esters isolated from leaf trichomes of Nicotiana gossei to pear psylla (Homoptera : Psyllidae). J. Econ. Entomol88 : 615-19.
Quideau, S., Deffieux, D., Douat-Casassus, C. and Pouységu, L. (2011). Plant polyphenols : Chemical properties, biological activities and synthesis. Angewandte Chemie Int. Edition 50 : 586-621.
Roka, L., Koudounas, K., Daras, G., Zoidakis, J., Vlahou, A., Kalaitzis, P. and Hatzopoulos, P. (2018). Proteome of olive non-glandular trichomes reveals protective protein network against (a) biotic challenge. J. Plant Physiol231 : 210-18.
Ryu, D. and Holt, D. L. (1993). Growth inhibition of Penicillium expansum by several commonly used food ingredients. J. Food Protection 56 : 862-67.
Santos Tozin, L. R. D., de Melo Silva, S. C. and Rodrigues, T. M. (2016). Non-glandular trichomes in Lamiaceae and Verbenaceae species : Morphological and histochemical features indicate more than physical protection. New Zealand J. Bot. 54 : 446-57.
Sasse, J., Schlegel, M., Borghi, L., Ullrich, F., Lee, M., Liu, G. W. and Kretzschmar, T. (2016). Petunia hybrida PDR2 is involved in herbivore defense by controlling steroidal contents in trichomes. Plant, Cell & Environ. 39 : 2725-39.
Sato, Y., Shimizu-Inatsugi, R., Yamazaki, M., Shimizu, K. K. and Nagano, A. J. (2019). Plant trichomes and a single gene Glabra 1 contribute to insect community composition on field-grown Arabidopsis thalianaBMC Plant Biol. 19 : 163.
Schnee, C., Köllner, T. G., Held, M., Turlings, T. C., Gershenzon, J. and Degenhardt, J. (2006). The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. National Academy of Sciences 103 : 1129-34.
Sharma, H. C., Sujana, G. and Rao, D. M. (2009). Morphological and chemical components of resistance to pod borer, Helicoverpa armigera in wild relatives of pigeonpea. Arthropod-Plant Interactions 3 : 151-61.
Shepherd, R. W., Bass, W. T., Houtz, R. L. and Wagner, G. J. (2005). Phylloplanins of tobacco are defensive proteins deployed on aerial surfaces by short glandular trichomes. The Plant Cell 17 : 1851-61.
Simmons, A. T. and Gurr, G. M. (2004). Trichome-based host plant resistance of Lycopersicon species and the biocontrol agent Mallada signata : Are they compatible? Entomologia Experimentalis et Applicata 113 : 95-101.
Sisk, C. B., Shorey, H. H., Gerber, R. G. and Gaston, L. K. (1996). Semiochemicals that disrupt foraging by the Argentine ant (Hymenoptera : Formicidae) : Laboratory bioassays. J. Econ. Entomol89 : 381-85.
Slocombe, S. P., Schauvinhold, I., McQuinn, R. P., Besser, K., Welsby, N. A. and Harper, A. (2008). Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiol. 148 : 1830-46.
Soroka, J. J., Holowachuk, J. M., Gruber, M. Y. and Grenkow, L. F. (2011). Feeding by flea beetles (Coleoptera : Chrysomelidae; Phyllotreta spp.) is decreased on canola (Brassica napus) seedlings with increased trichome density. J. Econ. Entomol104 : 125-36.
Sunitha, V., Rao, G. R., Lakshmi, K. V., Saxena, K. B., Rao, V. R. and Reddy, Y. V. R. (2008). Morphological and biochemical factors associated with resistance to Maruca vitrata (Lepidoptera : Pyralidae) in short-duration pigeonpea. Int. J. Trop. Insect Sci28 : 45-52.
Tan, H., Xiao, L., Gao, S., Li, Q., Chen, J., Xiao, Y. and Zhang, L. (2015). Trichome and artemisinin regulator 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua. Molecular Plant 8 : 1396-1411.
Taranto, F., Pasqualone, A., Mangini, G., Tripodi, P., Miazzi, M. M., Pavan, S. and Montemurro, C. (2017). Polyphenol oxidases in crops : Biochemical, physiological and genetic aspects. Int. J. Mole. Sci. 18 : 377.
Tattini, M., Gravano, E., Pinelli, P., Mulinacci, N. and Romani, A. (2000). Flavonoids accumulate in leaves and glandular trichomes of Phillyrea latifolia exposed to excess solar radiation. The New Phytologist 148 : 69-77.
Tian, D., Tooker, J., Peiffer, M., Chung, S. H. and Felton, G. W. (2012). Role of trichomes in defence against herbivores : Comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236 : 1053-66.
Valverde, P. L., Fornoni, J. and Nunez-Farfan, J. (2001). Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J. Evolu. Biol14 : 424-32.
Van Dam, N. M. and Hare, J. D. (1998). Biological activity of Datura wrightii glandular trichome exudate against Manduca sexta larvae. J. Chem. Ecol24 : 1529-49.
Verheggen, F. J., Capella, Q., Schwartzberg, E. G., Voigt, D. and Haubruge, E. (2009). Tomato-aphid-hoverfly : A tritrophic interaction incompatible for pest management. Arthropod-Plant Interactions 3 : 141-49.
Wagner, G. J., Wang, E. and Shepherd, R. (2004). New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93 : 3.
Wang, X., Chen, H., Shan, Z., Hao, Q., Zhang, C., Yang, Z. and Jiao, Y. (2015). Herbivore defence responses and associated herbivore defence mechanism as revealed by comparing a resistant wild soybean with a susceptible cultivar. The Crop J3 : 451-67.
War, A. R., Hussain, B. and Sharma, H. C. (2013). Induced resistance in groundnut by jasmonic acid and salicylic acid through alteration of trichome density and oviposition by Helicoverpa armigera (Lepidoptera : Noctuidae). AoB Plants 5.
Weinhold, A. and Baldwin, I. T. (2011). Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. National Academy of Sciences 108 : 7855-59.
Xing, Z., Liu, Y., Cai, W., Huang, X., Wu, S. and Lei, Z. (2017). Efficiency of trichome-based plant defence in Phaseolus vulgaris depends on insect behaviour, plant ontogeny and structure. Frontiers in Plant Science 8 : 2006.
 

Global Footprints