Plant Biol (Stuttg) 2005; 7(2): 148-155
DOI: 10.1055/s-2005-837575
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Cytological Development and Sesquiterpene Lactone Secretion in Capitate Glandular Trichomes of Sunflower

J. C. Göpfert1 , N. Heil1 , J. Conrad2 , O. Spring1
  • 1Institute of Botany, University of Hohenheim, Garbenstraße 30, 70599 Stuttgart, Germany
  • 2Bioorganic Chemistry, University of Hohenheim, Garbenstraße 30, 70599 Stuttgart, Germany
Further Information

Publication History

Received: October 26, 2004

Accepted: January 19, 2005

Publication Date:
11 April 2005 (online)

Abstract

The secretion of sesquiterpene lactones (STL) in capitate glandular trichomes from the anther appendages of Helianthus annuus L. (Asteraceae) was observed by light and fluorescence microscopy and HPLC analysis. Disk flowers within the sunflower capitulum showed the known ontogenetic progression from the centre to the margin. During development of the florets, the trichomes in the anther appendages secreted their metabolites into the subcuticular secretion storage space in front of the two apical cells. All stages of forming the cuticular globe, from the pre-secretory to the post-secretory phase, could be observed microscopically and secretory activity was simultaneously monitored. Six germacrolides and heliangolides of known structure were selected for quantitative analysis. The increase in STL content during extension of the subcuticular space was monitored by HPLC analysis. Thereby, the start and termination of STL biosynthesis was defined in relation to other developmental stages of floret ontogenesis, particularly, the pollen formation. Part of the secreted material showed autofluorescence which could be attributed to a hydroxy-trimethoxy-flavone, as determined by NMR and mass spectroscopy. The anther trichomes were cytologically and chemically similar to foliar glandular trichomes of sunflower and represent the multicellular capitate glandular trichome type common to many Asteraceae. The ease with which anther trichomes of H. annuus can be harvested and analyzed suggests that they can provide a valuable model system for investigation of STL and flavonoid metabolism in Asteraceae.

References

  • 1 Bohlmann J., Meyer-Gauen G., Croteau R.. Plant terpenoid synthases: molecular biology and phylogenetic analysis.  Proceedings of the National Academy of Science of the USA. (1998);  95 4126-4133
  • 2 Bouwmeester H. J., Kodde J., Verstappen F. W. A., Altug I. G., de Kraker J.-W., Wallaart T. E.. Isolation and characterization of two germacrene A synthase cDNA clones from chicory.  Plant Physiology. (2002);  129 134-144
  • 3 Buschmann H., Spring O.. Sesquiterpene lactones as a result of interspecific hybridization in Helianthus species.  Phytochemistry. (1995);  39 367-371
  • 4 Ciccio J. F., Calzada J.. Haagenolide, the major sesquiterpene lactone of Baltimora recta. .  Phytochemistry. (1981);  20 517
  • 5 Chappell J.. Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants.  Annual Reviews of Plant Physiology and Plant Molecular Biology. (1995);  46 521-547
  • 6 Court W. A., Roy R. C., Pocs R.. Effect of harvest date on the yield and quality of the essential oil of peppermint.  Canadian Journal of Plant Science. (1993);  73 815-824
  • 7 Croteau R., Johnson M. A.. Biosynthesis of terpenoids in glandular trichomes. Rodriguez, E., Healy, P. L., and Mehta, I., eds. Biology and Chemistry of Plant Trichomes. New York, London; Plenum Press (1984): 133-185
  • 8 Davis E. M., Croteau R.. Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes.  Topics in Current Chemistry. (2000);  209 54-95
  • 9 de Keukeleire J., Ooms G., Roldan-Ruiz I., van Bockstaele E., de Keukeleire D.. Formation and accumulation of α-acids, β-acids, desmethylxanthohumol, and xanthohumol during flowering of hops (Humulus lupulus L.).  Journal of Agricultural and Food Chemistry. (2003);  51 4436-4441
  • 10 de Kraker J.-W., Franssen M. C. R., Dalm M. C. F., de Groot A., Bouwmeester H. J.. Biosynthesis of germacrene A carboxylic acid in chicory roots. Demonstration of a cytochrome P450 (+)-germacrene A hydroxylase and NADP+-dependent sesquiterpenoid dehydrogenase(s) involved in sesquiterpene lactone biosynthesis.  Plant Physiology. (2001);  125 1930-1940
  • 11 de Kraker J.-W., Franssen M. C. R., de Groot A. D., König A., Bouwmeester H. J.. (+)-Germacrene A biosynthesis - the committed step in the biosynthesis of bitter sesquiterpene lactones in chicory.  Plant Physiology. (1998);  117 1381-1392
  • 12 Duke S. O., Canel C., Rimado A. M., Tellez M. R., Duke M. V., Paul R. N.. Current potential exploitation of plant glandular trichome productivity.  Advances in Botanical Research. (2000);  31 121-141
  • 13 Duke S. O., Paul R. N.. Development and fine structure of the glandular trichomes of Artemisia annua L.  International Journal of Plant Sciences. (1993);  142 107-118
  • 14 Gershenzon J., McConkey M. E., Croteau R. B.. Regulation of monoterpene accumulation in leaves of peppermint.  Plant Physiology. (2000);  122 205-213
  • 15 Gershenzon J., Duffy M. A., Karp F., Croteau R.. Mechanized techniques for the selective extraction of enzymes from plant epidermal glands.  Analytical Biochemistry. (1987);  163 159-164
  • 16 Gershenzon J., Maffei M., Croteau R.. Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). .  Plant Physiology. (1989);  89 1351-1357
  • 17 Hallahan D. L.. Monoterpenoid biosynthesis in glandular trichomes of labiate plants.  Advances in Botanical Research. (2000);  31 77-121
  • 18 Ferreira J. F. S., Janick J.. Floral morphology of Artemisia annua with special reference to trichomes.  International Journal of Plant Sciences. (1995);  156 807-815
  • 19 Kelsey R. G., Reynolds G. W., Rodriguez E.. The chemistry of biologically active constituents secreted and stored in plant glandular trichomes. Rodriguez, E., Healy, P. L., and Metha, I., eds. Biology and Chemistry of Plant Trichomes. New York, London; Plenum Press (1984): 187-241
  • 20 Klayman D. L.. Qinghaosu (artemisinin): an antimalarial drug from China.  Science. (1985);  228 1049-1055
  • 21 Langenheim J. H.. Higher plant terpenoids: a phytocentric overview of their ecological roles.  Journal of Chemical Ecology. (1994);  20 1223-1280
  • 22 Lichtenthaler H. K., Rohmer M., Schwender J.. Two independent biochemical pathways for isopentenyl diphosphat and isoprenoid biosynthesis in higher plants.  Physiologia Plantarum. (1997);  101 643-652
  • 23 Mahmoud S. S., Croteau R. B.. Strategies for transgenic manipulation of monoterpene biosynthesis in plants.  Trends in Plant Science. (2002);  7 366-373
  • 24 Marles R. J., Pazos-Sanou L., Compadre C. M., Pezzuto J. M., Bloszyk E., Arnason J. T.. Sesquiterpene lactones revisited: recent developments in the assessment of biological activities and structure relationship.  Phytochemistry of Medicinal Plants. (1995);  29 333-356
  • 25 Martin V. J. J., Pitera D. J., Withers S. T., Newman J. D., Keasling J. D.. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids.  Nature Biotechnology. (2003);  21 796-802
  • 26 McCaskill D., Croteau R.. Strategies for bioengineering the development and metabolism of glandular tissues in plants.  Nature Biotechnology. (1999);  17 31-36
  • 27 McConkey M. E., Gershenzon J., Croteau R. B.. Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint.  Plant Physiology. (2000);  122 215-223
  • 28 Picman A. K.. Biological activities of sesquiterpene lactones.  Biochemical Systematics and Ecology. (1986);  14 255-281
  • 29 Rohmer M., Knani M., Simonin P., Sutter B., Sahm H.. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate.  Biochemical Journal. (1993);  295 517-524
  • 30 Seaman F. C.. Sesquiterpene lactones as taxonomic characters in the Asteraceae.  The Botanical Review. (1982);  48 121-592
  • 31 Spring O.. Trichome microsampling of sesquiterpene lactones for the use of systematic studies. Fischer, N. H., Isman, M. B., and Stafford, H. A., eds. Modern Phytochemical Methods. New York, London; Plenum Press (1991): 319-345
  • 32 Spring O.. Chemotaxonomy based on metabolites from glandular trichomes.  Advances in Botanical Research. (2000);  31 153-169
  • 33 Spring O., Albert K., Hager A.. Three biologically active heliangolides from Helianthus annuus. .  Phytochemistry. (1982);  21 2551-2553
  • 34 Spring O., Benz T., Ilg M.. Sesquiterpene lactones of the capitate glandular trichomes of Helianthus annuus. .  Phytochemistry. (1989);  28 745-749
  • 35 Spring O., Bienert U.. Capitate glandular hairs from sunflower leaves: development, distribution and sesquiterpene lactone content.  Journal of Plant Physiology. (1987);  130 441-448
  • 36 Spring O., Bienert U., Klemt V.. Sesquiterpene lactones in glandular trichomes of sunflower leaves.  Journal of Plant Physiology. (1987);  130 433-439
  • 37 Trapp S. C., Croteau R.. Genomic organization of plant terpene synthases and molecular evolutionary implications.  Genetics. (2001);  158 811-832
  • 38 Turner G. W., Gershenzon J., Croteau R.. Distribution of peltate glandular trichomes on developing leaves of peppermint.  Plant Physiology. (2000);  124 655-663
  • 39 Umlauf D., Zapp J., Becker H., Adam K. P.. Biosynthesis of the irregular monoterpene artemisia ketone, the sesquiterpene germacrene D and other isoprenoids in Tanacetum vulgare L. (Asteraceae).  Phytochemistry. (2004);  65 2463-2470
  • 40 Vermeer J., Peterson R. L.. Glandular trichomes on the inflorescence of Chrysanthemum morifolium cv. Dramatic (Compositae). I. Development and morphology.  Canadian Journal of Botany. (1979 a);  57 705-713
  • 41 Vermeer J., Peterson R. L.. Glandular trichomes on the inflorescence of Chrysanthemum morifolium cv. Dramatic (Compositae). II. Ultrastructure and histochemistry.  Canadian Journal of Botany. (1979 b);  57 714-729
  • 42 Wagner G. J., Wang E., Shepherd R. W.. New approaches for studying and exploiting an old protuberance, the plant trichome.  Annals of Botany. (2004);  93 3-11
  • 43 Wallaart T. E., Bouwmeester H. J., Hille J., Poppinga L., Maijers N. C. A.. Amorpha-4,11-diene synthase: cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin.  Planta. (2001);  212 460-465
  • 44 Werker E.. Trichome diversity and development.  Advances in Botanical Research. (2000);  31 1-30
  • 45 Werker E., Putievsky E., Ravid U., Dudai N., Katzir I.. Glandular hairs and essential oil in developing leaves of Ocimum basilicum L. (Lamiaceae).  Annals of Botany. (1993);  34 31-45
  • 46 Yerger E. H., Grazzini R. A., Hesk D., Cox-Foster D. L., Craif R., Mumma R. O.. A rapid method for isolating glandular trichomes.  Plant Physiology. (1992);  99 1-7
  • 47 Zhang X., Oppenheimer D. G.. A simple and efficient method for isolating trichomes for downstream analyses.  Plant Cell Physiology. (2004);  45 221-224

O. Spring

Universität Hohenheim
Institut für Botanik (210)

70593 Stuttgart

Germany

Email: spring@uni-hohenheim.de

Editor: E. Pichersky

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