e-ISSN 2231-8542
ISSN 1511-3701
Nadya Sofia Siti Sa’adah, Nina Mutiara Calvaryni, Sukirno Sukirno, Laurentius Hartanto Nugroho and Tri Rini Nuringtyas
Pertanika Journal of Tropical Agricultural Science, Pre-Press
DOI: https://doi.org/10.47836/pjtas.47.4.05
Keywords: Basil, epidermis, localization, gas chromatography-mass spectrometry, metabolite profile
Published: 2024-09-27
Leaves serve as essential plant organs that facilitate photosynthesis and consist of several layers, such as the mesophyll and epidermis, each of which possesses unique metabolite compositions. These metabolites play a role in the plant’s defensive system against insects. For instance, the leaves of Ocimum basilicum L. (basil) possess biocidal properties against a variety of insects. Although the insecticidal properties of these leaves have been well documented, the distribution studies on the leaf metabolites are inadequate. Thus, this study examined the metabolite profiles of the two leaf layers, epidermis and mesophylls. The separation of epidermis and mesophyll extracts was accomplished using whetstone powder, followed by gas chromatography-mass spectrometry to analyze the obtained metabolite profiles. The leaf trichomes were examined by scanning electron microscopy. Certain chemicals were only detectable within the epidermal or mesophyll tissues. For example, tricosane (16.37%) and geraniol (7.88%) were exclusively detected in the epidermis, whereas limonene oxide (1.26%) and α-humulene (1.04%) were only detected in the mesophyll. Furthermore, certain components were found in higher quantities in the epidermis and mesophyll layers, whereas others were more prevalent in the opposite layer. Our findings relevant to the trichome types, specifically glandular and non-glandular trichomes, indicated that both play a role in the initial defenses against herbivorous insects. This study offers significant insights into the chemicals that serve as plant defenses in basil leaf tissue and trichomes. Future studies on the distribution of chemical compounds in different leaf tissues can provide further insights into the mechanisms of plant-insect interaction and facilitate the development of strategies for identifying compounds that play a role in defense.
Aharoni, A., & Galili, G. (2011). Metabolic engineering of the plant primary-secondary metabolism interface. Current Opinion in Biotechnology, 22(2), 239–244. https://doi.org/10.1016/j.copbio.2010.11.004
Ahmed, A. S., Fanokh, A. K. M., & Mahdi, M. A. (2019). Phytochemical identification and antioxidant study of essential oil constituents of Ocimum basilicum L. growing in Iraq. Pharmacognosy Journal, 11(4), 724–729. https://doi.org/10.5530/pj.2019.11.115
Al-Maawali, S. S., Al-Sadi, A. M., Alsheriqi, S. A. K., Al-Sabahi, J. N., & Velazhahan, R. (2021). The potential of antagonistic yeasts and bacteria from tomato phyllosphere and fructoplane in the control of Alternaria fruit rot of tomato. All Life, 14(1), 34-48. https://doi.org/10.1080/26895293.2020.1858975
Benelli, G., Pavela, R., Maggi, F., Wandjou, J. G. N., Fofie, N. G. B. Y., Koné-Bamba, D., Sagratini, G., Vittori, S., & Caprioli, G. (2019). Insecticidal activity of the essential oil and polar extracts from Ocimum gratissimum grown in Ivory Coast: Efficacy on insect pests and vectors and impact on non-target species. Industrial Crops and Products, 132, 377-385. https://doi.org/10.1016/j.indcrop.2019.02.047
Bensaid, A., Boudard, F., Servent, A., Morel, S., Portet, K., Guzman, C., Vitou, M., Bichon, F., & Poucheret, P. (2022). Differential nutrition-health properties of Ocimum basilicum leaf and stem extracts. Foods, 11(12), 1699. https://doi.org/10.3390/foods11121699
Berenbaum, M., & Feeny, P. (1981). Toxicity of angular furanocoumarins to swallowtail butterflies: Escalation in a coevolutionary arms race? Science, 212(4497), 927–929. https://doi.org/10.1126/science.212.4497.927
Boulamtat, R., Mesfioui, A., El-Fakhouri, K., Oubayoucef, A., Sabraoui, A., Aasfar, A., & El-Bouhssini, M. (2021). Chemical composition, and insecticidal activities of four plant essential oils from Morocco against larvae of Helicoverpa armigera (Hub.) under field and laboratory conditions. Crop Protection, 144, 105607. https://doi.org/10.1016/j.cropro.2021.105607
Brito, V. D., Achimón, F., Dambolena, J. S., Pizzolitto, R. P., & Zygadlo, J. A. (2019). Trans-2-hexen-1-ol as a tool for the control of Fusarium verticillioides in stored maize grains. Journal of Stored Products Research, 82, 123–130. https://doi.org/10.1016/j.jspr.2019.05.002
Cavalier-Smith, T. (2007). Origins of secondary metabolism. In D. J. Chadwick & J. Whelan (Eds.), Ciba Foundation Symposium 171 ‐ Secondary Metabolites: Their Function and Evolution (pp. 64-87). Ciba Foundation. https://doi.org/10.1002/9780470514344.ch5
Chaaban, S. B., Hamdi, S. H., Mahjoubi, K., & Jemâa, J. M. B. (2019). Composition and insecticidal activity of essential oil from Ruta graveolens, Mentha pulegium and Ocimum basilicum against Ectomyelois ceratoniae Zeller and Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Journal of Plant Diseases and Protection, 126, 237-246. https://doi.org/10.1007/s41348-019-00218-8
Chaudhary, A., Bala, K., Thakur, S., Kamboj, R., & Dumra, N. (2018). Plant defenses against herbivorous insects: A review. International Journal of Chemical Studies, 6(5), 681–688.
Chen, W., & Viljoen, A. M. (2010). Geraniol — A review of a commercially important fragrance material. South African Journal of Botany, 76(4), 643–651. https://doi.org/10.1016/j.sajb.2010.05.008
da Silva Moura, E., D’Antonino Faroni, L. R., Heleno, F. F., Rodrigues, A. A. Z., Prates, L. H. F., & de Queiroz, M. E. L. R. (2020). Optimal extraction of Ocimum basilicum essential oil by association of ultrasound and hydrodistillation and its potential as a biopesticide against a major stored grains pest. Molecules, 25(12), 2781. https://doi.org/10.3390/molecules25122781
Dahibhate, N. L., Dwivedi, P., & Kumar, K. (2022). GC–MS and UHPLC-HRMS based metabolite profiling of Bruguiera gymnorhiza reveals key bioactive compounds. South African Journal of Botany, 149, 1044-1048. https://doi.org/10.1016/j.sajb.2022.02.004
Dancewicz, K., Szumny, A., Wawrzeńczyk, C., & Gabryś, B. (2020). Repellent and antifeedant activities of citral-derived lactones against the peach potato aphid. International Journal of Molecular Sciences, 21(21), 8029. https://doi.org/10.3390/ijms21218029
Dangol, S., Poudel, D. K., Ojha, P. K., Maharjan, S., Poudel, A., Satyal, R., Rokaya, A., Timsina, S., Dosoky, N. S., Satyal, P., & Setzer, W. N. (2023). Essential oil composition analysis of Cymbopogon species from eastern Nepal by GC-MS and chiral GC-MS, and antimicrobial activity of some major compounds. Molecules, 28(2), 543. https://doi.org/10.3390/molecules28020543
de Oliveira, E. R., Alves, D. S., Carvalho, G. A., de Oliveira, B. M. R. G., Aazza, S., & Bertolucci, S. K. V. (2018). Toxicity of Cymbopogon flexuosus essential oil and citral for Spodoptera frugiperda. Ciência e Agrotecnologia, 42(4), 408–419. https://doi.org/10.1590/1413-70542018424013918
de Sena Filho, J. G., de Almeida, A. S., Pinto-Zevallos, D., Barreto, I. C., de Holanda Cavalcanti, S. C., Nunes, R., Teodoro, A. V., Xavier, H. S., Filho, J. M. B., Guan, L., Neves, A. L. A., & Duringer, J. M. (2023). From plant scent defense to biopesticide discovery: Evaluation of toxicity and acetylcholinesterase docking properties for Lamiaceae monoterpenes. Crop Protection, 164, 106126. https://doi.org/10.1016/j.cropro.2022.106126
Dmitruk, M., Sulborska, A., Żuraw, B., Stawiarz, E., & Weryszko-Chmielewska, E. (2019). Sites of secretion of bioactive compounds in leaves of Dracocephalum moldavica L.: Anatomical, histochemical, and essential oil study. Brazilian Journal of Botany, 42, 701–715. https://doi.org/10.1007/s40415-019-00559-6
Džamić, A. M., Soković, M. D., Ristić, M. S., Grujić, S. M., Mileski, K. S., & Marin, P. D. (2014). Chemical composition, antifungal and antioxidant activity of Pelargonium graveolens essential oil. Journal of Applied Pharmaceutical Science, 4(3), 1–5. https://doi.org/10.7324/JAPS.2014.40301
Erb, M., & Kliebenstein, D. J. (2020). Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy. Plant Physiology, 184(1), 39–52. https://doi.org/10.1104/PP.20.00433
Farag, M. A., Ezzat, S. M., Salama, M. M., & Tadros, M. G. (2016). Anti-acetylcholinesterase potential and metabolome classification of 4 Ocimum species as determined via UPLC/qTOF/MS and chemometric tools. Journal of Pharmaceutical and Biomedical Analysis, 125, 292-302. https://doi.org/10.1016/j.jpba.2016.03.037
Fürstenberg-Hägg, J., Zagrobelny, M., & Bak, S. (2013). Plant defense against insect herbivores. International Journal of Molecular Sciences, 14(5), 10242-10297. https://doi.org/10.3390/ijms140510242
Gang, D. R., Beuerle, T., Ullmann, P., Werck-Reichhart, D., & Pichersky, E. (2002). Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiology, 130(3), 1536–1544. https://doi.org/10.1104/pp.007146
Gonzáles, W. L., Negritto, M. A., Suárez, L. H., & Gianoli, E. (2008). Induction of glandular and non-glandular trichomes by damage in leaves of Madia sativa under contrasting water regimes. Acta Oecologica, 33(1), 128-132. https://doi.org/10.1016/j.actao.2007.10.004
Govindarajan, M., Sivakumar, R., Rajeswary, M., & Yogalakshmi, K. (2013). Chemical composition and larvicidal activity of essential oil from Ocimum basilicum (L.) against Culex tritaeniorhynchus, Aedes albopictus and Anopheles subpictus (Diptera: Culicidae). Experimental Parasitology, 134(1), 7-11. https://doi.org/10.1016/j.exppara.2013.01.018
Hadacek, F., Bachmann, G., Engelmeier, D., & Chobot, V. (2011). Hormesis and a chemical raison d’être for secondary plant metabolites. Dose-Response, 9(1). https://doi.org/10.2203/dose-response.09-028.Hadacek
Iijima, Y., Gang, D. R., Fridman, E., Lewinsohn, E., & Pichersky, E. (2004). Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiology, 134(1), 370–379. https://doi.org/10.1104/pp.103.032946
Ilmiah, H. H., Nuringtyas, T. R., & Nugroho, L. H. (2018). Accumulation of potential photo-protective compound groups in mangrove (Sonneratia caseolaris (L.) Engler.) leaves. Pharmacognosy Journal, 10(3), 576–580. https://doi.org/10.5530/pj.2018.3.94
Jönsson, M., & Anderson, P. (1999). Electrophysiological response to herbivore-induced host plant volatiles in the moth Spodoptera littoralis. Physiological Entomology, 24(4), 377–385. https://doi.org/10.1046/j.1365-3032.1999.00154.x
Kanehisa, M., & Goto, S. (2000). KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research, 28(1), 27–30.
Kariyat, R. R., Smith, J. D., Stephenson, A. G., De Moraes, C. M., & Mescher, M. C. (2017). Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix. Proceedings of the Royal Society B: Biological Sciences, 284, 20162323. https://doi.org/10.1098/rspb.2016.2323
Kayesth, S., Gupta, K. K., Kumar, S., & Shazad, M. (2018). Effects of Ocimum sanctum hexane extract on survival and development of Dysdercus koenigii Fabricius (Heteroptera: Pyrrhocoriedae). Archives of Phytopathology and Plant Protection, 51(17–18), 993–1007. https://doi.org/10.1080/03235408.2018.1541148
Krzysko-Łupicka, T., Walkowiak, W., & Bialon, M. (2019). Comparison of the fungistatic activity of selected essential oils relative to Fusarium graminearum isolates. Molecules, 24(2), 311. https://doi.org/10.3390/molecules24020311
Lessire, R., & Stumpf, P. K. (1983). Nature of the fatty acid synthetase systems in parenchymal and epidermal cells of Allium porrum L. leaves. Plant Physiology, 73(3), 614-618. https://doi.org/10.1104/pp.73.3.614
Lewinsohn, E., Dudai, N., Tadmor, K., Katzir, I., Ravid, U., Putievsky, E., & Joels, D. M. (1998). Histochemical localization of citral accumulation in lemongrass leaves (Cymbopogon citratus (DC.) Stapf., Poaceae). Annals of Botany, 81(1), 35–39. https://doi.org/10.1006/anbo.1997.0525
Luthra, R., Srivastava, A. K., & Ganjewala, D. (2017). Histochemical localisation of citral accumulating cite in lemongrass (Cymbopogon flexuosus Ness Ex. Steud) wats cultivar OD-19. Asian Journal of Plant Science, 6, 419–422. https://doi.org/10.3923/ajps.2007.419.422
Marotti, M., Piccaglia, R., & Giovanelli, E. (1996). Differences in essential oil composition of Basil (Ocimum basilicum L.) Italian cultivars related to morphological characteristics. Journal of Agricultural and Food Chemistry, 44(12), 3926–3929. https://doi.org/10.1021/jf9601067
Martin, C., Bhatt, K., & Baumann, K. (2001). Shaping in plant cells. Current Opinion in Plant Biology, 4(6), 540–549. https://doi.org/10.1016/S1369-5266(00)00213-2
Miano, R. N., Ayelo, P. M., Musau, R., Hassanali, A., & Mohamed, S. A. (2022). Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant. Scientific Reports, 12, 8965. https://doi.org/10.1038/s41598-022-13125-0
Murata, J., & De Luca, V. (2005). Localization of tabersonine 16‐hydroxylase and 16‐OH tabersonine‐16‐O‐methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. The Plant Journal, 44(4), 581-594. https://doi.org/10.1111/j.1365-313X.2005.02557.x
Murata, J., Roepke, J., Gordon, H., & De Luca, V. (2008). The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell, 20(3), 524–542. https://doi.org/10.1105/tpc.107.056630
Nuringtyas, T. R., Choi, Y. H., Verpoorte, R., Klinkhamer, P. G. L., & Leiss, K. A. (2012). Differential tissue distribution of metabolites in Jacobaea vulgaris, Jacobaea aquatica and their crosses. Phytochemistry, 78, 89–97. https://doi.org/10.1016/j.phytochem.2012.03.011
Peiffer, M., Tooker, J. F., Luthe, D. S., & Felton, G. W. (2009). Plants on early alert: Glandular trichomes as sensors for insect herbivores. New Phytologist, 184(3), 644–656. https://doi.org/10.1111/j.1469-8137.2009.03002.x
Quan, M., Liu, Q. Z., & Liu, Z. L. (2018). Identification of insecticidal constituents from the essential oil from the aerial parts Stachys riederi var. japonica. Molecules, 23(5), 1200. https://doi.org/10.3390/molecules23051200
Rahmani, S., & Azimi, S. (2020). Fumigant toxicity of three Satureja species on tomato leafminers, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Toxin Reviews, 40(4), 724-735. https://doi.org/10.1080/15569543.2020.1767651
Rautio, P., Markkola, A., Martel, J., Tuomi, J., Härmä, E., Kuikka, K., Siitonen, A., Riesco, I. L., & Roitto, M. (2002). Developmental plasticity in birch leaves: Defoliation causes a shift from glandular to nonglandular trichomes. Oikos, 98(3), 437-446. https://doi.org/10.1034/j.1600-0706.2002.980308.x
Sá, R. D., Santana, A. S. C. O., Silva, F. C. L., Soares, L. A. L., & Randau, K. P. (2016). Anatomical and histochemical analysis of Dysphania ambrosioides supported by light and electron microscopy. Revista Brasileira de Farmacognosia, 26(5), 533–543. https://doi.org/10.1016/j.bjp.2016.05.010
Singh, P., Jayaramaiah, R. H., Sarate, P., Thulasiram, H. V., Kulkarni, M. J., & Giri, A. P. (2014). Insecticidal potential of defense metabolites from Ocimum kilimandscharicum against Helicoverpa armigera. PLOS One, 9(8), e0104377. https://doi.org/10.1371/journal.pone.0104377
Sletvold, N., Huttunen, P., Handley, R., Kärkkäinen, K., & Ågren, J. (2010). Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata. Evolutionary Ecology, 24, 1307–1319. https://doi.org/10.1007/s10682-010-9381-6
Sneha, K., Narayanankutty, A., Job, J. T., Olatunji, O. J., Alfarhan, A., Famurewa, A. C., & Ramesh, V. (2022). Antimicrobial and larvicidal activities of different Ocimum essential oils extracted by ultrasound-assisted hydrodistillation. Molecules, 27(5), 1456. https://doi.org/10.3390/molecules27051456
Srivastava, S., Adholeya, A., Conlan, X. A., & Cahill, D. M. (2016). Acidic potassium permanganate chemiluminescence for the determination of antioxidant potential in three cultivars of Ocimum basilicum. Plant Foods for Human Nutrition, 71, 72-80. https://doi.org/10.1007/s11130-016-0527-8
Tian, D., Tooker, J., Peiffer, M., Chung, S. H., & Felton, G. W. (2012). Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta, 236, 1053–1066. https://doi.org/10.1007/s00425-012-1651-9
Traw, M. B., & Bergelson, J. (2003). Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology, 133(3), 1367–1375. https://doi.org/10.1104/pp.103.027086
van Schie, C. C. N., Haring, M. A., & Schuurink, R. C. (2007). Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Molecular Biology, 64, 251–263. https://doi.org/10.1007/s11103-007-9149-8
Wang, X., Shen, C., Meng, P., Tan, G., & Lv, L. (2021). Analysis and review of trichomes in plants. BMC Plant Biology, 21, 70. https://doi.org/10.1186/s12870-021-02840-x
War, A. R., Taggar, G. K., Hussain, B., Taggar, M. S., Nair, R. M., & Sharma, H. C. (2018). Special issue: using non-model systems to explore plant-pollinator and plant-herbivore interactions: plant defence against herbivory and insect adaptations. AoB PLANTS, 10(4), ply037. https://doi.org/10.1093/aobpla/ply037
Xie, Z., Kapteyn, J., & Gang, D. R. (2008). A systems biology investigation of the MEP/terpenoid and shikimate/phenylpropanoid pathways points to multiple levels of metabolic control in sweet basil glandular trichomes. The Plant Journal, 54(3), 349–361. https://doi.org/10.1111/j.1365-313X.2008.03429.x
Zhandi, W., La, Z., Bailian, D., Yundong, S., Yani, W., Guangqiu, L., & Lin, J. (2021). Regulation of pakchoi’s secondary metabolites on the behavior of female Plutella xylostella (Lepidoptera: Plutellidae). Chinese Journal of Pesticide Science, 23(2), 323-330. https://doi.org/10.16801/j.issn.1008-7303.2021.0016
Zhang, X. G., Li, X., Gao, Y. L., Liu, Y., Dong, W. X., & Xiao, C. (2019). Oviposition deterrents in larval frass of potato tuberworm moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Neotropical Entomology, 48, 496-502. https://doi.org/10.1007/s13744-018-0655-y
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