PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

The inflorescence of Etlingera elatior forms tubular, true flowers in an acropetal sequence that blooms ostentatiously. The aromatic plant also produces excellent flavour and fragrance afforded by the presence of secretory structures capable of accumulating, storing, and releasing volatile compounds. However, there is a lack of botanical description of the flowering morphology and the type of secretory structures involved in plant-pollinator interactions. This study aims to describe the floral morphology, characterise the diverse micromorphology of the epidermal outgrowths in the true flower, and analyse their histochemical contents by scanning electron and light microscopes. Labellum defines the anthesis stage of the true flower: unveiling by petals at anthesis and furling inwards that closes the top part of the flower at post-anthesis. In addition to the floral advertisement accessory function demonstrated by the labellum, the closure provides additional exaptation of post-pollination protection to the flower. Both glandular trichomes and osmophores are involved in biochemical functions that release heterogeneous substances (mucilage, terpenes, and phenolic compounds) to help secure anthesis. Non-glandular trichomes, on the other hand, are structurally involved in the floral development by providing physical and mechanical protection to the flower by acting as glue to maintain the closed structure of the flower, connecting floral accessories, and forming a formidable barrier surrounding the ovary, the most important reproductive organ of the flower. Findings from the present study demonstrate that the presence of secretory structures coordinated with the flower’s functional traits enhances the pollination mechanism. It is the maiden report for E. elatior on epidermal outgrowths and their participation in floral structure and development besides plant-pollinator interaction.

• Anzian, A., Muhialdin, B. J., Mohammed, N. K., Kadum, H., Marzlan, A. A., Sukor, R., & Hussin, A. S. B. (2020). Antibacterial activity and metabolomics profiling of torch ginger (Etlingera elatior Jack) flower oil extracted using subcritical carbon dioxide (CO2). Evidence-Based Complementary and Alternative Medicine, 2020, 4373401. https://doi.org/10.1155/2020/4373401

• Armbruster, W. S. (1997). Exaptations link evolution of plant-herbivore and plant-pollinator interactions: A phylogenetic inquiry. Ecology, 78(6), 1661–1672. https://doi.org/10.1890/0012-9658(1997)078[1661:ELEOPH]2.0.CO;2

• Bezerra-Silva, P. C., Dutra, K. A., Santos, G. K. N., Silva, R. C. S., Julek, J., Milet-Pinheiro, P., & Navarro, D. M. A. F. (2016). Evaluation of the activity of the essential oil from an ornamental flower against Aedes aegypti: Electrophysiology, molecular dynamics and behavioral assays. PLOS One, 11(2), e0150008. https://doi.org/10.1371/journal.pone.0150008

• Box, M. S., & Rudall, P. J. (2006). Floral structure and ontogeny in Globba (Zingiberaceae). Plant Systematics and Evolution, 258, 107–122. https://doi.org/10.1007/s00606-005-0395-4

• Bull-Hereñu, K., dos Santos, P., Toni, J. F. G., El Ottra, J. H. L., Thaowetsuwan, P., Jeiter, J., Ronse De Craene, L. P., & Iwamoto, A. (2022). Mechanical forces in floral development. Plants, 11(5), 661. https://doi.org/10.3390/plants11050661

• Caissard, J.-C., Meekijjironenroj, A., Baudino, S., & Anstett, M.-C. (2004). Localization of production and emission of pollinator attractant on whole leaves of Chamaerops humilis (Arecaceae). American Journal of Botany, 91(8), 1190–1199. https://doi.org/10.3732/ajb.91.8.1190

• Chakira, A., Garcia, C., Soria, C., Minier, J., & Chillet, M. (2022). Effect of flower development stages on the dynamics of volatile compounds in ylang-ylang (Cananga odorata) essential oil. Horticulturae, 8(11), 986. https://doi.org/10.3390/horticulturae8110986

• Chalvin, C., Drevensek, S., Dron, M., Bendahmane, A., & Boualem, A. (2020). Genetic control of glandular trichome development. Trends in Plant Science, 25(5), 477-487. https://doi.org/10.1016/j.tplants.2019.12.025

• Choon, S. Y., & Ding, P. (2016). Growth stages of torch ginger (Etlingera elatior) plant. Sains Malaysiana, 45(4), 507–515.

• Choon, S. Y., Ding, P., Mahmud, T. M. M., & Shaari, K. (2016). Phenological growth stages of torch ginger (Etlingera elatior) inflorescence. Pertanika Journal of Tropical Agricultural Science, 39(1), 73–78.

• Choon, S. Y., & Ding, P. (2017a). Physiological changes of torch ginger (Etlingera elatior) inflorescence during development. HortScience, 52(3), 479–482. https://doi.org/10.21273/HORTSCI11189-16

• Choon, S. Y., & Ding, P. (2017b). Developmental changes in cellular structure and cell wall metabolism of torch ginger (Etlingera elatior (Jack) R. M. Smith) inflorescence. Current Plant Biology, 9-10, 3-10. https://doi.org/10.1016/j.cpb.2017.01.001

• de Santiago-Hernández, M.H., Martén-Rodríguez, S., Lopezaraiza-Mikel, M., Oyama, K., González-Rodríguez, A., & Quesada, M. (2019). The role of pollination effectiveness on the attributes of interaction networks: From floral visitation to plant fitness. Ecology, 100(10), e02803. https://doi.org/10.1002/ecy.2803

• El Ottra, J. H. L., Pirani, J. R., & Endress, P. K. (2013). Fusion within and between whorls of floral organs in Galipeinae (Rutaceae): Structural features and evolutionary implications. Annals of Botany, 111(5), 821–837. https://doi.org/10.1093/aob/mct039

• Essenberg, C. J. (2021). Intraspecific relationships between floral signals and rewards with implications for plant fitness. AoB PLANTS, 13(2), plab006. https://doi.org/10.1093/aobpla/plab006

• Guo, Y., Zhang, T., Zhong, J., Ba, T., Xu, T., Zhang, Q., & Sun, M. (2020). Identification of the volatile compounds and observation of the glandular trichomes in Opisthopappus taihangensis and four species of Chrysanthemum. Plants, 9(7), 855. https://doi.org/10.3390/plants9070855

• Huchelmann, A., Boutry, M., & Hachez, C. (2017). Plant glandular trichomes: Natural cell factories of high biotechnological interest. Plant Physiology, 175(1), 6–22. https://doi.org/10.1104/pp.17.00727

• Jensen, W. A. (1962). Botanical histochemistry: Principles and practice. WH Freeman.

• Johansen, D. A. (1940). Plant microtechnique. McGraw-Hill Book Company.

• Johnson, S. R., Lange, I., Srividya, N., & Lange, B. M. (2017). Bioenergetics of monoterpenoid essential oil biosynthesis in non-photosynthetic glandular trichomes. Plant Physiology, 175(2), 681–695. https://doi.org/10.1104/pp.17.00551

• Juwita, T., Puspitasari, M. I., & Levita, J. (2018). Torch ginger (Etlingera elatior): A review on its botanical aspects, phytoconstituents and pharmacological activities. Pakistan Journal of Biological Sciences, 21(4), 151-165. https://doi.org/10.3923/pjbs.2018.151.165

• Karabourniotis, G., Liakopoulo, G., Nikolopoulos, D., & Bresta, P. (2019). Protective and defensive roles of non glandular trichomes against multiple stresses: Structure–function coordination. Journal of Forestry Research, 31, 1-12. https://doi.org/10.1007/s11676-019-01034-4

• Khaw, S. (2001). The genus Etlingera (Zingiberaceae) in Peninsular Malaysia including a new species. Gardens’ Bulletin Singapore, 53(1-2), 191–239.

• Kirchoff, B. K. (1998). Inflorescence and flower development in the Hedychieae (Zingiberaceae): Scaphochlamys kunstleri (Baker) Holttum. International Journal of Plant Sciences, 159(2), 261–274. https://doi.org/10.1086/297547

• Kittipanangkul, N., & Ngamriabsakul, C. N. (2006). Pollen and pollinator limitation of seed initiation in Etlingera littoralis (J. König) Giseke (Zingiberaceae) in Klong Klai Basin, Khao Nan National Park, Thailand. Walailak Journal of Science and Technology, 3(2), 207–217.

• Koptur, S., Barrios, B., Valdes, I., & Nusrat, M. (2020). A fishing expedition to discover the pollinators of several subtropical Apocynaceae. Application in Plant Sciences, 8(2), e11326. https://doi.org/10.1002/aps3.11326

• Lee, Y. L. (2019). Characterization of secretory structures and essential oils in aerial parts of torch ginger [Etlingera elatior (Jack) R. M. Sm.] at different developmental stages. [Doctoral thesis, Universiti Putra Malaysia]. Universiti Putra Malaysia Institutional Repository. http://psasir.upm.edu.my/id/eprint/90923/

• Leica Microsystems. (2013). User manual: Leica S series. Leica Microsystems.

• Lusa, M. G., Cardoso, E. C., Machado, S. R., & Appezzato-da-Glória, B. (2015). Trichomes related to an unusual method of water retention and protection of the stem apex in an arid zone perennial species. AoB PLANTS, 7, plu088. https://doi.org/10.1093/aobpla/plu088

• Machado, S. R., Gregório, E. A., & Guimarães, E. (2006). Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): Developmental ultrastructure and secretion in relation to function. Annals of Botany, 97(3), 357–369. https://doi.org./10.1093/aob/mcj042

• Matías-Hernández, L., Aguilar-Jaramillo, A. E., Cigliano, R. A., Sanseverino, W., & Pelaz, S. (2016). Flowering and trichome development share hormonal and transcription factor regulation. Journal of Experimental Botany, 67(5), 1209–1219. https://doi.org/10.1093/jxb/erv534

• Mesquita-Neto, J. N., Paiva, E. A. S., Galetto, L., & Schlindwein, C. (2020). Nectar secretion of floral buds of Tococa guianensis mediates interactions with generalist ants that reduce florivory. Frontiers in Plant Science, 11, 627. https://doi.org/10.3389/fpls.2020.00627

• Pansarin, E. R., Aguiar, J. M. R. B. V., & Pansarin, L. M. (2014). Floral biology and histochemical analysis of Vanilla edwallii Hoehne (Orchidaceae: Vanilloideae): An orchid pollinated by Epicharis (Apidae: Centridini). Plant Species Biology, 29(3), 242–252. https://doi.org/10.1111/1442-1984.12014

• Pedersen, L. B. (2004). Phylogenetic analysis of the subfamily Alpinioideae (Zingiberaceae), particularly Etlingera Giseke, based on nuclear and plastid DNA. Plant Systematics and Evolution, 245, 239–258. https://doi.org/10.1007/s00606-004-0126-2

• PIñeyro-Nelson, A., De Almeida, A. M. R., Sass, C., Iles, W. J. D., & Specht, C. D. (2017). Change of fate and staminodial laminarity as potential agents of floral diversification in the Zingiberales. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 328(1-2), 41–54. https://doi.org/10.1002/jez.b.22724

• Qiao, Z., Hu, H., Shi, S., Yuan, X., Yan, B., & Chen, L. (2021). An update on the function, biosynthesis and regulation of floral volatile terpenoids. Horticulturae, 7(11), 451. https://doi.org/10.3390/horticulturae7110451

• Rico-Guevara, A., Rubega, M. A., Hurme, K. J., & Dudley, R. (2019). Shifting paradigms in the mechanics of nectar extraction and hummingbird bill morphology. Integrative Organismal Biology, 1(1), oby006. https://doi.org/10.1093/iob/oby006

• Riegert, J., Fainová, D., Antczak, M., Sedláček, O., Hořák, D., Reif, J., & Pešata , M. (2011). Food niche differentiation in two syntopic sunbird species: A case study from the Cameroon Mountains. Journal of Ornithology, 152, 819–825. https://doi.org/10.1007/s10336-011-0650-0

• Sakai, S., Kawakita, A., Ooi, K., & Inoue, T. (2013). Variation in the strength of association among pollination systems and floral traits: Evolutionary changes in the floral traits of Bornean gingers (Zingiberaceae). American Journal of Botany, 100(3), 546–555. https://doi.org/10.3732/ajb.1200359

• Sangthong, S., Promputtha, I., Pintathong, P., & Chaiwut, P. (2022). Chemical constituents, antioxidant, anti-tyrosinase, cytotoxicity, and anti-melanogenesis activities of Etlingera elatior (Jack) leaf essential oils. Molecules, 27(11), 3469. https://doi.org/10.3390/molecules27113469

• Serna, L., & Martin, C. (2006). Trichomes: Different regulatory networks lead to convergent structures. Trends in Plant Science, 11(6), 274–280. https://doi.org/10.1016/j.tplants.2006.04.008

• Song, J.-J., Zou, P., Liao, J.-P., Tang, Y.-J., & Chen, Z. (2007). Floral ontogeny in Alpinia oxyphylla Miq. (Zingiberaceae) and its systematic significance. Gardens’ Bulletin Singapore, 59(1), 221–229.

• Sungthong, B., & Srichaikul, B. (2018). Antioxidant activities, acute toxicity and chemical profiling of torch ginger (Etlingera elatior Jack.) inflorescent extract. Pharmacognosy Journal, 10(5), 979-982. https://doi.org/10.5530/pj.2018.5.166

• Takeda, S., Iwasaki, A., Matsumoto, N., Uemura, T., Tatematsu, K., & Okada, K. (2013). Physical interaction of floral organs controls petal morphogenesis in Arabidopsis. Plant Physiology, 161(3), 1242–1250. https://doi.org/10.1104/pp.112.212084

• Tan, J., Walford, S.-A., Dennis, E. S., & Llewellyn, D. (2016). Trichomes control flower bud shape by linking together young petals. Nature Plants, 2, 16093. https://doi.org/10.1038/nplants.2016.93

• Tissier, A., Morgan, J. A., & Dudareva, N. (2017). Plant volatiles: Going ‘in’ but not ‘out’ of trichome cavities. Trends in Plant Science, 22(11), 930-938. https://doi.org/10.1016/j.tplants.2017.09.001

• Tölke, E. D., Bachelier, J. B., de Lima E. A., Ferreira, M. J. P., Demarco, D., & Carmello-Guerreiro, S. M. (2018). Osmophores and floral fragrance in Anacardium humile and Mangifera indica (Anacardiaceae): An overlooked secretory structure in Sapindales. AoB PLANTS, 10(6), ply062. https://doi.org/10.1093/aobpla/ply062

• Uzelac, B., Janošević, D, Stojićić, D., & Budimir, S, (2015). In vitro morphogenesis and secretion of secondary metabolites of Nicotiana tabacum tall glandular trichomes. Botanica Serbica, 39(2), 103–110.

• van der Kooi, C. J., Vallejo-Marin, M., & Leonhardt, S. D. (2021). Mutualisms and (a)symmetry in plant–pollinator interactions. Current Biology, 31(2), R91-R99. https://doi.org/10.1016/j.cub.2020.11.020

• 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). Plant defence against herbivory and insect adaptations. AoB PLANTS, 10(4), ply037. https://doi.org/10.1093/aobpla/ply037

• Yang, S., Wang, N., Kimani, S., Li, Y., Bao, T., Ning, G., Li, L., Liu, B., Wang, L., & Gao, X. (2022). Characterization of terpene synthase variation in flowers of wild Aquilegia species from Northeastern Asia. Horticulture Research, 9, uhab020. https://doi.org/10.1093/hr/uhab020

• Zhang, X., Grey, P. H., Krishnakumar, S., & Oppenheimer, D. G. (2005). The IRREGULAR TRICHOME BRANCH loci regulate trichome elongation in Arabidopsis. Plant and Cell Physiology, 46(9), 1549–1560. https://doi.org/10.1093/pcp/pci168

• Zhao, Q., & Chen, X.-Y. (2016). Development: A new function of plant trichomes. Nature Plants, 2, 16096. https://doi.org/10.1038/nplants.2016.96