Abstract
Main conclusion
Three types of the glandular trichomes are developed on the flowers and leaves of Millingtonia hortensis. Morphology, cell ultrastructure and content of the volatile compounds are specific to each trichome type.
Abstract
The aim of this study was to characterize the structural and histochemical features of the glandular trichomes (GTs) of two types localized on the different flower parts and leaves in Millingtonia hortensis, as well as to identify the composition of the internal pool of metabolites. The peltate GTs are most common; they are founded on peduncle, calyx, ovary, and leaves. GTs consist of 12–24-cell disk-shaped head and a single-celled neck. The capitate GTs are located on corolla tube and have four to eight-cell head, single-celled neck and a wide multicellular stalk. A series of histochemical reactions and fluorescent microscopy revealed the various substances in the chemical composition of GTs. Acid polysaccharides are predominately identified in the capitate trichomes of the corolla tube and peltate trichomes of calyx, terpenes present in larger quantity in the trichomes of the corolla tube and ovary, whilst phenolic substances prevail in the trichomes of the calyx and ovary. GTs of each type are characterized by specific ultrastructural traits. Smooth endoplasmic reticulum (SER) and leucoplasts prevail in the peltate trichomes of peduncle, calyx and ovary; Golgi apparatus is the common organelle in the capitate trichomes of the corolla tube and peltate trichomes of calyx; the huge aggregates of the RER cisterns there are in cytoplasm of all leaf trichomes. Synthesized secretion accumulates in the subcuticular cavity of all GTs except the leaf peltate trichomes. In the trichomes of the leaves secretion is stored in the thick upper cell wall with the wide cutinized layer. For the first time content of the internal pool of metabolites from the flowers and leaves was identified by GC–MS. Seventeen compounds, including alcohols, fatty acid derivatives, monoterpenes, sesquiterpenes, and benzenoids were identified. 1-octen 3-ol, 3-carene, methyl salicylate, p-hydroxybenzeneethanol and 1-hydroxy-2,4-di-tertbutyl-benzene were the main compounds of the flower scent. We consider GTs of the reproductive organs in M. hortensis synthesizing acid polysaccharides and volatile compounds as secretory structures attracting of pollinators, whereas the leaf peltate trichomes accumulating predominately non-volatile phenols, protect young vegetative shoots against small herbivorous insects and pathogens.
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Abbreviations
- GT:
-
Glandular trichome
- SER:
-
Smooth endoplasmic reticulum
- RER:
-
Rough endoplasmic reticulum
References
Anulakanapakorn K, Bunyapraphatsara N, Satayavivad J (1989) Phytochemical and pharmacological studies of the flowers of Millingtonia hortensis Linn. J Sci Soc Thailand 13:71–83
Appezzato-da-Glória B, Da Costa FB, da Silva VC, Gobbo-Neto L, Rehder VLG, Hayashi AH (2012) Glandular trichomes on aerial and underground organs in Chrysolaena species (Vernonieae–Asteraceae): structure, ultrastructure and chemical composition. FLORA 207:878–887. https://doi.org/10.1016/j.flora.2012.10.003
Ascensão L, Pais MS (1998) The leaf capitate trichomes of Leonotis leonurus: histochemistry, ultrastructure and secretion. Ann Bot 81:263–271
Ascensão L, Marques N, Pais MS (1997) Peltate glandular trichomes of Leonotis leonurus leaves: ultrastructure and histochemical characterization of secretions. Int J Plant Sci 158:249–258
Ascensão L, Mota L, Castro DM (1999) Glandular trichomes on the leaves and flowers of Plectranthus ornatus: morphology, distribution and histochemistry. Ann Bot 84:437–447
Aschenbrenner A-K, Amrehn E, Bechtel L, Spring O (2015) Trichome differentiation on leaf primordia of Helianthus annuus (Asteraceae): morphology, gene expression and metabolite profile. Planta 241:837–846
Barman M, Mitra A (2019) Temporal relationship between emitted and endogenous floral scent volatiles in summer- and winter-blooming Jasminum species. Physiol Plant 166:946–959
Beevers L (1996) Clathrin-coated vesicles in plants. Int Rev Cytol 167:1–37
Bera P, Mukherjee C, Mitra A (2017) Enzymatic production and emission of floral scent volatiles in Jasminum sambac. Plant Sci 256:25–38. https://doi.org/10.1016/j.plantsci.2016.11.013
Berggren B (1987) Structure and cytochemistry of the procambium in Salix buds during dormancy and dormancy breaking. Nord J Bot 7:153–167. https://doi.org/10.1111/j.1756-1051.1987.tb00928.x
Bhattacharya R, Saha S, Kostina O, Muravnik L, Mitra A (2020) Replacing critical point drying with a low-cost chemical drying provides comparable surface image quality of glandular trichomes from leaves of Millingtonia hortensis L. f. in scanning electron micrograph. Appl Microsc 50:15. https://doi.org/10.1186/s42649-020-00035-6
Bisio A, Corallo A, Gastaldo P, Romussi G, Ciarallo G, Fontana N, De Tommasi N, Profumo P (1999) Glandular hairs and secreted material in Salvia blepharophylla Brandegee ex Epling grown in Italy. Ann Bot 83:441–452
Bittencourt NS Jr, Semir J (2004) Pollination biology and breeding system of Zeyheria montana (Bignoniaceae). Plant Syst Evol 247:241–254. https://doi.org/10.1007/s00606-004-0142-2
Bunyapraphatsara N, Blaskó G, Cordell GA (1989) Hortensin, an unusual flavone from Millingtonia hortensis. Phytochemistry 28:1555–1556. https://doi.org/10.1016/S0031-9422(00)97793-8zxc
Cheniclet C, Carde J-P (1985) Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: a correlative study. Israel J Bot 34:219–238
Corsi G, Bottega S (1999) Glandular hairs of Salvia officinalis: new data on morphology, localization and histochemistry in relation to function. Ann Bot 84:657–664
David R, Carde J-P (1964) Coloration differentiele des inclusions lipidique et terpeniques des pseudophilles du pin maritime au moyen du reactif nadi. C R Acad Sci (Paris) 258:1338–1340
de Fróes Castro FFP, Gama TSS, Feio AC, Demarco D, Aguiar-Dias ACA (2015) Structure and distribution of glandular trichomes in three species of Bignoniaceae. Acta Amazonica 45:347–354
Duke SO, Paul RN (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Int J Plant Sci 154:107–118
Gahan PB (1984) Plant histochemistry and cytochemistry. Academic Press, London
Gershenzon J, McCaskill D, Rajaonarivony JIM, Mihaliak C, Karp F, Croteau R (1992) Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal Biochem 200:130–138
Giuliani C, Maleci Bini L (2008) Insight into the structure and chemistry of glandular trichomes of Labiatae, with emphasis on subfamily Lamioideae. Plant Syst Evol 276:199–208
Glauert AM (1980) Fixation, dehydration and embedding of biological specimens. Practical methods in electron microscopy, Elsevier, Amsterdam
Gonzalez AM (2013) Indumento, nectarios extraflorales y anatomía foliar en Bignoniáceas de la Argentina. Bol Soc Argent Bot 48:221–245
Guimaraes E, Di Stasi LC, De Cassia S, Nia Maimoni-Rodella R (2008) Pollination biology of Jacaranda oxyphylla with an emphasis on staminode function. Ann Bot 102:699–711
Gutmann M (1995) Improved staining procedures for photographic documentation of phenolic deposits in semithin sections of plant tissue. J Microsc 179:277–281
Harborne JH, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504
Hase T, Ohtani K, Kasai R, Yamasaki K, Picheansoonthon C (1995) Revised structure for hortensin, a flavonoid from Millingtonia hortensis. Phytochemistry 40:287–290. https://doi.org/10.1016/0031-9422(95)00206-M
Jensen WA (1962) Botanical histochemistry. Freeman, San Francisco
Karabourniotis G, Kotsabassidis D, Manetas Y (1995) Trichome density and its protective potential against ultraviolet-B radiation damage during leaf development. Can J Bot 73:376–383
Kaushik R, Saini P (2008) Larvicidal activity of leaf extract of Millingtonia hortensis (family: Bignoniaceae) against Anopheles stephensi, Culex quinquefasciatus and Aedes aegypti. J Vector Borne Dis 45:66–69
Keene CK, Wagner GJ (1985) Direct demonstration of duvatrienediol biosynthesis in glandular heads of tobacco trichomes. Plant Physiol 79:1026–1032. https://doi.org/10.1104/pp.79.4.1026
Kim E-S, Mahlberg PG (1991) Secretory cavity development in glandular trichomes of Cannabis sativa L. (Cannabaceae). Am J Bot 78:220–229
Kotamreddy JNR, Hansda C, Mitra A (2020) Semi-targeted metabolomic analysis provides the basis for enhanced antioxidant capacities in pigmented rice grains. Food Meas 14:1183–1191. https://doi.org/10.1007/s11694-019-00367-2
Koteyeva NK (1997) Ultrastructural changes in shoot apical meristem cells of Pinus sylvestris (Pinaceae) in annual cycle. Botanichiskii Zhurnal 82:10–23
Lopes AV, Vogel S, Machado IC (2002) Secretory trichomes, a substitutive floral nectar source in Lundia A. DC. (Bignoniaceae), a genus lacking a functional disc. Ann Bot 90:169–174. https://doi.org/10.1093/aob/mcf169
Machado SR, Gregorio EA, Guimaraes E (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function. Ann Bot 97:357–369
Mehra KR, Kulkarni AR (1989) Floral trichomes in some members of Bignoniaceae. Proc Indian Acad Sci 99:97–105
Meyberg M, Krohn S, Brummer B, Kristen U (1991) Ultrastructure and secretion of glandular trichomes of tobacco leaves. Flora 185:357–363
Muravnik LE, Shavarda AL (2011) Pericarp peltate trichomes in Pterocarya rhoifolia: histochemistry, ultrastructure, and chemical composition. Int J Plant Sci 172:159–172
Muravnik LE, Shavarda AL (2012) Leaf glandular trichomes in Empetrum nigrum: morphology, histochemistry, ultrastructure and secondary metabolites. Nord J Bot 30:470–481
Muravnik LE, Vassilyev AE, Potapova YY (1995) Ultrastructural aspects of digestive gland functioning in Aldrovanda vesiculosa. Russ J Plant Physiol 42:1–8
Muravnik LE, Kostina OV, Mosina AA (2019) Glandular trichomes of the leaves in three Doronicum species (Senecioneae, Asteraceae): morphology, histochemistry and ultrastructure. Protoplasma 256(3):789–803. https://doi.org/10.1007/s00709-018-01342-2
Nair AGR, Sivakumar R (1992) Non-identity of hortensin from Millingtonia hortensis with 3,4′-dihydroxy-6,7-dimethoxyflavone. Phytochemistry 31:671–673. https://doi.org/10.1016/0031-9422(92)90057-W
Nogueira A, El Ottra JHL, Guimarães E, Machado SR, Lohmann LG (2013) Trichome structure and evolution in Neotropical lianas. Ann Bot 112:1331–1350. https://doi.org/10.1093/aob/mct201
Rivera GL (1996) Floral trichomes in four Tecomeae (Bignoniaceae). Darwiniana 34:19–26
Schnepf E (1971) Die Feinstruktur der lamellären Einschlußkörper im Zellkern und im Cytoplasma der Drüsenhaare von Salvia glutinosa. Protoplasma 73:67–72. https://doi.org/10.1007/BF01286412
Schopker H, Kneisel M, Beerhues L, Robenek H, Wiermann R (1995) Phenylalanine ammonia-lyase and chalkone synthase in glands of Primula kewensis (W. Wats): immunofluorescence and immunogold localization. Planta 196:712–719
Seibert RJ (1948) The use of glands in a taxonomic consideration of the family Bignoniaceae. Ann Missouri Bot Gard 35:123–137. https://doi.org/10.2307/2394389
Sharma RC, Zaman A, Kidwai AR (1968) Chemical examination of Millingtonia hortensis. Phytochemistry 7:1891–1892. https://doi.org/10.1016/S0031-9422(00)86669-8
Souza L, Santos G, Moschetta IS (2010) Morfoanatomia floral de espe´cies lianescentes de Bignoniaceae. Iheringia 65:5–15
Spring O (2000) Chemotaxonomy based on metabolites from glandular trichomes. Adv Bot Res 31:153–174. https://doi.org/10.1016/s0065-2296(00)31009-6
Subramanian SS, Nagarajan S, Sulochana N (1971) Flavonoids of Millingtonia hortensis. Curr Sci 40:194–195
Tozin LRS, Carvalho SF, Machado SR, Rodrigues TM (2015) Glandular trichome diversity on leaves of Lippia origanoides and Lippia stachyoides (Verbenaceae): morphology, histochemistry, and ultrastructure. Botany 93:297–306. https://doi.org/10.1139/cjb-2014-0251
Turner GW, Gershenzon J, Nielsen EE, Froehlich JE, Croteau R (1999) Limonene synthase, the enzyme responsible for monoterpene biosynthesis in peppermint, is localized to leucoplasts of oil gland secretory cells. Plant Physiol 120:879–886
Turner GW, Gershenzon J, Croteau RB (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–679
Ugbabe GE, Ayodele AE, Kalpana SJ, Okogun JI (2014) Ultra-structure of the leaf surfaces of the family Bignoniaceae Juss. in Nigeria. Global J Bot Sci 2:37–44
Valkama E, Salminen J-P, Koricheva J, Pihlaja K (2003) Comparative analysis of leaf trichome structure and composition of epicuticular flavonoids in finnish birch species. Ann Bot 91:643–655
Vassilyev AE (2000) Quantitative ultrastructural data of secretory duct epithelial cells in Rhus toxicodendron. Int J Plant Sci 161:615–630
Vassilyev AE, Gamaley YV (1975) Protein crystals in plant cells. Tsitologia 17:371–389
Vassilyev AE, Muravnik LE (1988) The ultrastructure of the digestive glands in Pinguicula vulgaris L. (Lentibulariaceae) relative to their function. I The changes during maturation. Ann Bot 62:329–341. https://doi.org/10.1093/oxfordjournals.aob.a087665
Vogel S (1997) Remarkable nectaries: structure, ecology, organophyletic perspectives I. Substitutive nectaries. Flora 192:305–333
Winkel-Shirley B (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol Plant 107:142–149
Wong DCJ, Pichersky E, Peakall R (2017) The biosynthesis of unusual floral volatiles and blends involved in orchid pollination by deception: current progress and future prospects. Front Plant Sci 8:1955. https://doi.org/10.3389/fpls.2017.01955
Acknowledgements
The authors are grateful to the Core Centre “Cell and Molecular Technology in the Plant Science” at the Komarov Botanical Institute (St. Petersburg, Russia) for providing of equipment for light and electron microscopy. The present study was supported by an Indo-Russian Research Grant funded jointly by the Russian Foundation for Basic Research, Moscow (RFBR grant no. 18-54-45010 to L. E. Muravnik) and the Government of India, Department of Science and Technology, New Delhi (DST grant no. INT/RUS/RFBR/P-329 to A. Mitra). We also thank the two anonymous reviewers for their comments on this manuscript.
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Muravnik, L.E., Mosina, A.A., Zaporozhets, N.L. et al. Glandular trichomes of the flowers and leaves in Millingtonia hortensis (Bignoniaceae). Planta 253, 13 (2021). https://doi.org/10.1007/s00425-020-03541-9
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DOI: https://doi.org/10.1007/s00425-020-03541-9