Advertisement

Protoplasma

pp 1–15 | Cite as

Glandular trichomes of the leaves in three Doronicum species (Senecioneae, Asteraceae): morphology, histochemistry, and ultrastructure

  • Lyudmila E MuravnikEmail author
  • Olga V Kostina
  • Anna A Mosina
Original Article

Abstract

Two types of glandular tichomes (GTs) develop on the leaves in three Doronicum species. The purpose of the work was to establish common and distinctive morphological, anatomical, histochemical, and ultrustructural features of the trichomes. It turned out that differences between types of trichomes are more significant than interspecific ones. For each Doronicum species, differences between GTs of two types include the dimensions, intensity of coloration by histochemical dyes, as well as ultrastructural features of the cells. The GTs of the first type are higher than GTs of the second type. Two to three upper cell layers of the first trichomes develop histochemical staining, whereas in the second ones, only apical cells give a positive histochemical reaction. In all trichomes, polysaccharides, polyphenols, and terpenoids are detected. In the GTs of the first type, polysaccharides are synthesized in larger quantity; in the GTs of the second type, synthesis of the secondary metabolites predominates. Main ultrastructural features of the GTs of the first type include proliferation of RER and an activity of Golgi apparatus denoting the synthesis of enzymes and pectin; however, development of SER, diversiform leucoplasts with reticular sheaths, and chloroplasts with peripheral plastid reticulum also demonstrate the synthesis of lipid substances. The ultrastructural characteristics of the second type GTs indicate the primary synthesis of lipid components. Secretion is localized in a periplasmic space of the upper cell layers. The secretory products pass through the cell wall, accumulate in the subcuticular cavity, and rupture it.

Keywords

Glandular trichomes Morphology Anatomy Histoxhemistry Ultrastructure Secretion 

Notes

Acknowledgments

We appreciate the Core Centre “Cell and Molecular Technology in the Plant Science” at the Komarov Botanical Institute (St. Petersburg) for provision of equipment for light and electron microscopy. The present study was carried out within the framework of the institutional research project (01201255608) of the Komarov Botanical Institute of the Russian Academy of Sciences. We also thank the two anonymous reviewers for their comments on this manuscript.

Author contribution statement

LEM conceived and coordinated all experiments, analyzed data, and wrote the manuscript; OVK and AAM contributed to histochemistry and microscopy.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adedeji O, Jewoola OA (2008) Importance of leaf epidermal characters in the Asteraceae family. Not Bot Hort Agrobot Cluj 36:7–16Google Scholar
  2. Afolayan AJ, Meyer JJM (1995) Morphology and ultrastructure of secreting and nonsecreting foliar trichomes of Helichrysum aureonitens (Asteraceae). Int J Plant Sci 156:481–487CrossRefGoogle Scholar
  3. Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10:1135–1149CrossRefGoogle Scholar
  4. Alieva SA, Abdullaev UA, Telezhenetskaya MV, Yunusov SY (1976) Alkaloids of Doronicum macrophyllum. Chem Nat Compd 12:194–196CrossRefGoogle Scholar
  5. Alieva SA, Omurkamzinova VB, Glizin VI (1979) Flavonoids of Doronicum macrophyllum and Doronicum oblongifolium. Chem Nat Compd 15:82CrossRefGoogle Scholar
  6. Amrehn E, Heller A, Spring O (2014) Capitate glandular trichomes of Helianthus annuus (Asteraceae): ultrastructure and cytological development. Protoplasma 251:161–167CrossRefGoogle Scholar
  7. Andreeva AV, Kutuzov MA, Evans DE, Hawes CR (1998) The structure and function of the Golgi apparatus: a hundred years of questions [review]. J Exp Bot 49:1281–1291CrossRefGoogle Scholar
  8. Andreucci AC, Ciccarelli D, Desideri I, Pagni AM (2008) Glandular hairs and secretory ducts of Matricaria chamomilla (Asteraceae): morphology and histochemistry. Ann Bot Fennici 45:11–18CrossRefGoogle Scholar
  9. 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 207:878–887CrossRefGoogle Scholar
  10. Ascensão L, Marques N, Pais MS (1997) Peltate glandular trichomes of Leonotis leonurus leaves: ultrastructure and histochemical characterization of secretions. Int J Plant Sci 158:249–258CrossRefGoogle Scholar
  11. Ascensão L, Pais MS (1998) The leaf capitate trichomes of Leonotis leonurus: histochemistry, ultrastructure and secretion. Ann Bot 81:263–271CrossRefGoogle Scholar
  12. Ascensão L, Pais MS (1987) Glandular trichomes of Artemisia campestris (ssp. maritima): ontogeny and histochemistry of the secretory product. Bot Gaz 148:221–227CrossRefGoogle Scholar
  13. Beevers L (1996) Clathrin-coated vesicles in plants. Int Rev Cytol 167:1–37CrossRefGoogle Scholar
  14. Bohlmann F, Abraham W (1979) Naturally occurring terpene derivatives. New sesquiterpene alcohol and other substances from Doronicum pardalianches. Phytochemistry 18: 668–671Google Scholar
  15. Castro MM, Leitão-Filho HF, Monteiro WR (1997) Utilização de estruturas secretoras na identificação dos gêneros de Asteraceae de uma vegetação de cerrado. Rev Bras Bot 20:163–174CrossRefGoogle Scholar
  16. Ciccarelli D, Garbari F, Pagni AM (2007) Glandular hairs of the ovary: a helpful character for Asteroideae (Asteraceae) taxonomy? Ann Bot Fennici 44:1–7Google Scholar
  17. Combrinck S (2006) Chemical constituents of Lippia scaberrima Sond. (Verbenaceae), Dissertation, Tshwane University of TechnologyGoogle Scholar
  18. Cron GV, Balkwill K, Knox EB (2006) Two new species of Cineraria (Senecioneae, Asteraceae) from KwaZulu-Natal, South Africa. SAJB 72:34–39CrossRefGoogle Scholar
  19. David R, Carde J-P (1964) Coloration differentiele des inclusions lipidique et terpeniques des pseudophilles du pin maritime au moyen du reactif nadi. CR Acad Sci D 258:1338–1340Google Scholar
  20. Duke SO, Paul RN (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Int J Plant Sci 154:107–118CrossRefGoogle Scholar
  21. Favi F, Cantrell CL, Mebrahtu T, Kraemer MВE (2008) Leaf peltate glandular trichomes of Vernonia galamensis ssp. galamensis var. ethiopica Gilbert: development, ultrastructure, and chemical composition. Int J Plant Sci 169:605–614CrossRefGoogle Scholar
  22. Fernández IA (2003) Systematics of Eurasian and North African Doronicum (Asteraceae: Senecioneae). Ann Mo Bot Gard 90:319–389CrossRefGoogle Scholar
  23. Figueiredo AC, Pais MS (1994) Ultrastructural aspects of the glandular cells from the secretory trichomes and from the cell suspension cultures of Achillea millefolium L. ssp. millefolium. Ann Bot 74:179–190CrossRefGoogle Scholar
  24. Furst GG (1979) Methods of anatomical and histochemical studies of plant tissues. Nauka, MoscowGoogle Scholar
  25. Glauert AM (1980) Fixation, dehydration and embedding of biological specimens. North-Holland, Amsterdam. New York. OxfordGoogle Scholar
  26. Gliszczyńska A, Brodelius PE (2012) Sesquiterpene coumarins. Phytochem Rev 11:77–96CrossRefGoogle Scholar
  27. Gobbo-Neto L, Gates PJ, Lopes NP (2008) Negative ion ‘chip-based’ nanospray tandem mass spectrometry for the analysis of flavonoids in glandular trichomes of Lychnophora ericoides Mart. (Asteraceae). Rapid Commun Mass Sp 22:3802–3808CrossRefGoogle Scholar
  28. Göpfert JC, Heil N, Conrad J, Spring O (2005) Cytological development and sesquiterpene lactone secretion in capitate glandular trichomes of sunflower. Plant Biol 7:148–155CrossRefGoogle Scholar
  29. Gutmann M (1995) Improved staining procedures for photographic documentation of phenolic deposits in semithin sections of plant tissue. J Microsc 179:277–281CrossRefGoogle Scholar
  30. Hariri EB, Salle G, Andary C (1991) Involvement of flavonoids in the resistance of two poplar cultivars to mistletoe (Viscum album L.). Protoplasma 162:20–26CrossRefGoogle Scholar
  31. Hawes CR, Satiat-Jeunemaitre B (1996) Stacks of questions - how does the plant Golgi work? Trends Plant Sci 1:395–401CrossRefGoogle Scholar
  32. Heinrich G, Pfeifhofer HW, Stabentheiner E, Sawidis T (2002) Glandular hairs of Sigesbeckia jorullensis Kunth (Asteraceae): morphology, histochemistry and composition of essential oil. Ann Bot 89:459–469CrossRefGoogle Scholar
  33. Heinrich G, Sawidis T, Ingolic E, Stabentheiner E, Pfeifhofer HW (2010) Ultrastructure of glandular hairs of Sigesbeckia jorullensis Kunth (Asteraceae). Isr J Plant Sci 58:297–308CrossRefGoogle Scholar
  34. Holloway PJ (1982) Structure and histochemistry of plant cuticular membranes: an overview. In: Cutler DF, Alvin KL, Price CE (eds) The plant cuticle: pp. 1–32Google Scholar
  35. Jensen WA (1962) Botanical histochemistry. Freeman, San FranciscoGoogle Scholar
  36. Karabourniotis G, Fasseas C (1996) The dense indumentum with its polyphenol content may replace the protective role of the epidermis in some young xeromorphic leaves. Can J Bot 74:347–351CrossRefGoogle Scholar
  37. Kelsey RG, Shafizadeh F (1980) Glandular trichomes and sesquiterpene lactones of Artemisia nova (Asteraceae). Biochem Syst Ecol 8:371–377CrossRefGoogle Scholar
  38. Komissarenko N, Chernobai V, Derkach A (1988) Flavonoids of inflorescences of Calendula officinalis. Chem Nat Compd 24:675–680CrossRefGoogle Scholar
  39. Kostina ОV, Muravnik LE (2014) Structure and chemical content of the trichomes in two Doronicum species (Asteraceae). Modern Phytomorphology 5:167–171Google Scholar
  40. Koteyeva NK (2005) A novel structural type of plant cuticle. Dokl Biol Sci 403:272–274CrossRefGoogle Scholar
  41. Kowalkowska AK, Turzyński S, Kozieradzka-Kiszkurno M, Wiśniewska N (2017) Floral structure of two species of Bulbophyllum section Cirrhopetalum Lindl.: B. weberi Ames and B. cumingii (Lindl.) Rchb. f. (Bulbophyllinae Schltr., Orchidaceae). Protoplasma 254:1431–1449CrossRefGoogle Scholar
  42. Lyshede OB (1982) Structure of the outer epidermal wall in xerophytes. In: Cutler DF, Alvin KL, Price CE (eds) The plant cuticle: 87–98Google Scholar
  43. Machado SR, Gregorio EA, Guimaraes E (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function. Ann Bot 97:357–369CrossRefGoogle Scholar
  44. Monteiro WR, Castro MM, Mazzoni-Viveiros SC (2001) Development and some histochemical aspects of foliar glandular trichomes of Stevia rebaudiana (Bert.) Bert. - Asteraceae. Rev Bras Bot 24:349–357CrossRefGoogle Scholar
  45. Muravnik LE, Kostina OV, Shavarda AL (2016) Glandular trichomes of Tussilago farfara (Senecioneae, Asteraceae). Planta 244:737–752CrossRefGoogle Scholar
  46. Muravnik LE, Shavarda AL (2012) Leaf glandular trichomes in Empetrum nigrum: morphology, histochemistry, ultrastructure and secondary metabolites. Nord J Bot 30:470–481CrossRefGoogle Scholar
  47. Nikolakaki A, Christodoulakis NS (2004) Leaf structure and cytochemical investigation of secretory tissues in Inula viscosa. Bot J Linn Soc 144:437–448CrossRefGoogle Scholar
  48. Olsson ME, Olofsson LM, Lindahl AL, Lundgren A, Brodelius M, Brodelius PE (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70:1123–1128CrossRefGoogle Scholar
  49. Pagni AM, Orlando R, Masini A, Ciccarelli D (2003) Secretory structures of Santolina ligustica Arrigoni (Asteraceae), an Italian endemic species. Isr J Plant Sci 51:185–192CrossRefGoogle Scholar
  50. Paolini J, Muselli A, Bernardini AF, Bighelli A, Casanova J, Costa J (2007) Thymol derivatives from essential oil of Doronicum corsicum L. Flavour Frag J 22:479–487CrossRefGoogle Scholar
  51. Pizza C, de Tommasi N (1987) Plants metabolites. A new sesquiterpene glycoside from Calendula arvensis. J Nat Prod 50: 784–789Google Scholar
  52. Sacchetti G, Romagnoli C, Nicoletti M, Di Fabio A, Bruni A, Poli F (1999) Glandular trichomes of Calceolaria adscendens Lidl. (Scrophulariaceae): histochemistry, development and ultrastructure. Ann Bot 83:87–92CrossRefGoogle Scholar
  53. Sanderfoot AA, Raikhel NV (1999) The specificity of vesicle trafficking: coat proteins and SNAREs. Plant Cell 11:629–642CrossRefGoogle Scholar
  54. Schnepf E 1969 Über den Feinbau von Öldrüsen. I. Die Drüsenhaare von Arctium lappa Protoplasma 67: 185–194Google Scholar
  55. Schönherr J (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J Exp Bot 57:2471–2491CrossRefGoogle Scholar
  56. 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 196:712–719CrossRefGoogle Scholar
  57. Schreiber L (2005) Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Ann Bot 95:1069–1073CrossRefGoogle Scholar
  58. Seaman F (1982) Sesquiterpene lactones as taxonomic characters in the Asteraceae. Bot Rev 48:121–594CrossRefGoogle Scholar
  59. Serrato-Valenti G, Bisio A, Cornara L, Ciarallo G (1997) Structural and histochemical investigation of the glandular trichomes of Salvia aurea L. leaves, and chemical analysis of the essential oil. Ann Bot 79:329–336CrossRefGoogle Scholar
  60. Skubatz H, Kunkel DD (1999) Further studies of the glandular tissue of the Sauromatum guttatum (Araceae) appendix. Am J Bot 86:841–854CrossRefGoogle Scholar
  61. Szakiel A, Ruszkowski D, Janiszowska W (2005) Saponins in Calendula officinalis L. – structure, biosynthesis, transport and biological activity. Phytochem Rev 4:151–158CrossRefGoogle Scholar
  62. Spring O (2000) Chemotaxonomy based on metabolites from glandular trichomes. Adv Bot Res 31:153–174CrossRefGoogle Scholar
  63. Swenson U (1995) Systematics of Abrotanella an amphi-pacific genus of Asteraceae (Senecioneae). Plant Syst Evol 197:149–193CrossRefGoogle Scholar
  64. Tateo F, Cornara L, Bononi M, Mariotti MG, Serrato-Valenti G (2001) Trichomes on vegetative and reproductive organs of Stevia rebaudiana (Asteraceae). Structure and secretory products. Plant Biosyst 135:25–37CrossRefGoogle Scholar
  65. Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136:4215–4227CrossRefGoogle Scholar
  66. Turner GW, Gershenzon J, Croteau RB (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–679CrossRefGoogle Scholar
  67. Urzúa A, Andrade L, Munoz E, Rodriguez ME, Belmonte E (1997) Flavonoids in the trichome resinous exudate from Diplosthepium cinereum. Biochem Syst Ecol 25:681–682CrossRefGoogle Scholar
  68. Vassilyev AE (2000) Quantitative ultrastructural data of secretory duct epithelial cells in Rhus toxicodendron. Int J Plant Sci 161:615–630CrossRefGoogle Scholar
  69. Vermeer J, Peterson RL (1979) Glandular trichomes on the inforescence of Chrysanthemum morifolium cv. Dramatic (Compositae). II. Ultrastructure and histochemistry. Can J Bot 57:714–729CrossRefGoogle Scholar
  70. Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96:675–679CrossRefGoogle Scholar
  71. Werker E (2000) Trichome diversity and development. Adv Bot Res 31:1–35CrossRefGoogle Scholar
  72. Werker E, Fahn A (1981) Secretory hairs of Inula viscosa (L.) Ait. - development, ultrastructure and secretion. Bot Gaz 142:461–476CrossRefGoogle Scholar
  73. Werker E, Putievsky E, Ravid U, Dudai N, Katzir I (1994) Glandular hairs, secretory cavities, and the essential oil in the leaves of tarragon (Artemisia dracunculus L.). J Herbs Spices Med Plants 2:19–32CrossRefGoogle Scholar
  74. Winkel-Shirley B (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol Plant 107:142–149CrossRefGoogle Scholar
  75. Wist TJ, Davis AR (2006) Floral nectar production and nectary anatomy and ultrastructure of Echinacea purpurea (Asteraceae). Ann Bot 97:177–193CrossRefGoogle Scholar
  76. Wollenweber E (1993) Flavones and flavonols. In: Harborne JB (ed) The flavonoids. Advances in research since 1986. Chapman & Hall, LondonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Plant Anatomy and MorphologyKomarov Botanical Institute of the Russian Academy of SciencesSt. PetersburgRussia

Personalised recommendations