Abstract
Main conclusion
Sunflower trichomes fully develop on embryonic plumula within 3 days after start of germination. Toxic sesquiterpene lactones are produced immediately thereafter thus protecting the apical bud of the seedling against herbivory.
Helianthus annuus harbors non-glandular and two different types of multicellular glandular trichomes, namely the biseriate capitate glandular trichomes and the uniseriate linear glandular trichomes. The development of capitate glandular trichomes is well known from anther tips on sunflower disk florets, but not from leaves and no information is yet available on the development of the linear glandular trichomes. Scanning electron microscopy of sunflower seedlings unravelled that within the first 40 h of seed germination all three types of trichomes started to emerge on primordia of the first true leaves. Within the following 20–30 h trichomes developed from trichoblasts to fully differentiated hairs. Gene expression studies showed that genes involved in the trichome-based sesquiterpene lactone formation were up-regulated between 72 and 96 h after start of germination. Metabolite profiling with HPLC confirmed the synthesis of sesquiterpene lactones which may contribute to protect the germinating seedlings from herbivory. The study has shown that sunflower leaf primordia can serve as a fast and easy to handle model system for the investigation of trichome development in Asteraceae.
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Abbreviations
- CGT:
-
Capitate glandular trichomes
- GT:
-
Glandular trichomes
- LGT:
-
Linear glandular trichomes
- NGT:
-
Non-glandular trichomes
- RT:
-
Room temperature
- SEM:
-
Scanning electron microscopy
References
Aljancic I, Vajs V, Menkovic N, Karadzic I, Juranic N, Milosavljevic S, Macura S (1999) Flavones and sesquiterpene lactones from Achillea atrata subsp. multifida: antimicrobial activity. J Nat Prod 62:909–911
Amrehn E, Heller A, Spring O (2014) Capitate glandular trichomes of Helianthus annuus (Asteraceae): ultrastructure and cytological development. Protoplasma 251:161–167
Aschenbrenner AK (2014) Die linearen drüsenhaare der sonnenblume: morphologie, vorkommen, metabolitprofil und sesquiterpenbiosynthese. Dissertation, University of Hohenheim, Germany
Aschenbrenner AK, Horakh S, Spring O (2013) Linear glandular trichomes of Helianthus (Asteraceae): morphology, localization, metabolite activity and occurrence. AoB Plants 5:plt028. doi:10.1093/aobpla/plt028
Binet MN, Steinmetz A, Tessier LH (1989) The primary structure of sunflower (Helianthus annuus) ubiquitin. Nucl Acids Res 17:2119
Chacon De-la-Cruz I, Riley-Saldana CA, Gonzalez-Esquinca AR (2013) Secondary metabolites during early development in plants. Phytochem Rev 12:47–64
Favi F, Cantrell CL, Mebrahtu T, Kraemer ME (2008) Leaf peltate glandular trichomes of Vernonia galamensis ssp. galamensis var. ethiopica: development, ultrastructure, and chemical composition. Int J Plant Sci 169:605–614
Gershenzon J, Rossiter M, Mabry TJ, Rogers CE, Blust MH, Hopkins TL (1985) Insect antifeedant terpenoids in wild sunflower. In: Hedin PA, Cutler HC, Hammock BD, Menn JJ, Moreland DE, Plimmer JR (eds) Bioregulators for pest control. ACS Symposium Series 276, pp 433–446
Göpfert JC, Heil N, Conrad J, Spring O (2005) Cytological development and sesquiterpene lactone secretion in capitate glandular trichomes of sunflower. Plant Biol 7:148–155
Göpfert JC, Conrad J, Spring O (2006) 5-Deoxynevadensin, a novel flavone in sunflower and aspects of biosynthesis during trichome development. Nat Prod Commun 1:335–340
Göpfert JC, MacNevin G, Ro DK, Spring O (2009) Identification, functional characterization and developmental regulation of sesquiterpene synthases from sunflower capitate glandular trichomes. BMC Plant Biol 9:86
Göpfert JC, Bülow AK, Spring O (2010) Identification and functional characterization of a new sunflower germacrene-A-synthase (HaGAS3). Nat Prod Commun 5:709–715
Gören N, Woerdenbag HJ, Bozok-Johansson C (1996) Cytotoxic and antibacterial activities of sesquiterpene lactones isolated from Tanacetum praeteritum subsp. praeteritum. Planta Med 62:419–422
Heil N, Spring O (1999) Sesquiterpenlakton-Bildung im Verlauf der Drüsenhaarentwicklung bei Sonnenblumen. Sektionstagung der Sektion pflanzliche Naturstoffe der Deutschen Botanischen Gesellschaft, Bonn
Ikezawa N, Göpfert JC, Nguyen DT, Kim SU, O’Maille PE, Spring O, Ro DK (2011) Lettuce costunolide synthase (CYP71BL2) and its homolog (CYP71BL1) from sunflower catalyze distinct regio- and stereoselective hydroxylations in sesquiterpene lactone metabolism. J Biol Chem 286:21601–21611
Knight DW (1995) Feverfew: chemistry and biological activity. Nat Prod Rep 12:271–276
Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280
Mazeyrat F, Salles S, Drevet J, Roeckel-Drevet P, Tourvieille D, Ledoigt G (1998) Isolation of a complete PAL cDNA from sunflower. Plant Physiol 117:719
Monteiro WR, De Moraes Castro M, Mazzoni-Viveiros SC, Mahlberg PG (2001) Development and some histochemical aspects of foliar glandular trichomes of Stevia rebaudiana (Bert.) Bert.—Asteraceae. Braz J Bot, ISSN 1806-9959. doi:10.1590/S0100-84042001000300013
Mori K, Matsushima Y (1995) Synthesis of mono- and sesquiterpenoids; Homogynolide A, an insect antifeedant isolated from Homogyne alpina. Synthesis 7:845–850
Mullin CA, Alfatafta AA, Harman JL, Everett SL, Serino AA (1991) Feeding and toxic effects of floral sesquiterpene lactones, diterpenes, and phenolics from sunflower (Helianthus annuus L.) on western corn rootworm. J Agric Food Chem 39:2293–2299
Nguyen DT, Göpfert JC, Ikezawa N, MacNevin G, Kathiresan M, Conrad J, Spring O, Ro DK (2010) Biochemical conservation and evolution of germacrene A oxidase in Asteraceae. J Biol Chem 285:16588–16598
Nonogaki H (2010) MicroRNA gene regulation cascades during early stages of plant development. Plant Cell Physiol 51:1840–1846
Rieseberg LH, Soltis DE, Arnold D (1987) Variation and localization of flavonoid aglyconesin Helianthus annuus (Compositae). Am J Bot: 224–233
Ritesh KY, Rajender SS, Farzana S, Awadesh KS, Neelam SS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83
Ro DK, Ehlting J, Keeling CI, Lin R, Mattheus N, Bohlmann J (2006) Microarray expression profiling and functional characterization of AtTPS genes: duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Arch Biochem Biophys 448:104–116
Schilling EE, Panero JL, Storbeck TA (1987) Flavonoids of Helianthus series microcephali. Biochem Syst Ecol 15:671–672
Schmidt CO, Bouwmeester HJ, Bülow N, König WA (1999) Isolation, characterization, and mechanistic studies of (-)-alpha-gurjunene synthase from Solidago canadensis. Arch Biochem Biophys 364:167–177
Schnittger A, Hülskamp M (2002) Trichome morphogenesis: a cell-cyle perspective. Philos T Roy Soc London B 357:823–826
Spring O, Kupka J, Maier B, Hager A (1982) Biological activities of sesquiterpene lactones from Helianthus annuus: antimicrobial and cytotoxic properties; influence on DNA, RNA, and protein synthesis. Z Naturforschung C Biosci 37:1087–1091
Spring O, Bienert U (1987) Capitate glandular hairs from sunflower leaves: development, distribution and sesquiterpene lactone content. J Plant Physiol 130:441–448
Spring O, Bienert U, Klemt V (1987) Sesquiterpene lactones in glandular trichomes of sunflower leaves. J Plant Physiol 130:433–439
Spring O, Schilling EE (1989) Chemosystematic investigation of the annual species of Helianthus (Asteraceae). Part II in the series “The sesquiterpene lactone chemistry of Helianthus”. Biochem Syst Ecol 17:519–528
Spring O, Priester T, Klemt V, Kruppa J (1989a) The possible function of sesquiterpene lactones in sunflower. In: Proc sunflower res workshop. Fargo, pp 21–22
Spring O, Benz T, Ilg M (1989b) Sesquiterpene lactones of the capitate glandular trichomes of Helianthus annuus. Phytochemistry 28:745–749
Spring O (1991) Trichome microsampling of sesquiterpene lactones for the use of systematic studies. In: Fischer NH, Isman MB, Stafford HA (eds) Modern phytochemical methods. Recent advances in phytochemistry, vol 25. Plenum Press, New York, pp 319–345
Spring O, Rodon U, Macias FA (1992) Sesquiterpenes from non-capitate glandular trichomes of Helianthus annuus L. Phytochemistry 31:1541–1544
Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant J 70:51–68
Werker E (2000) Trichome diversity and development. Plant trichomes. Adv Bot Res 31:1–30
Zheng GQ (1994) Cytotoxic terpenoids and flavonoids from Artemisia annua. Planta Med 60:54–57
Acknowledgments
We want to thank J. Prasifka, U.S. Department of Agriculture, Fargo, North Dakota, for helpful suggestions in preparing the manuscript. The technical assistance in capillary electrophoresis by R. Zipper, Institute of Botany, University of Hohenheim, is gratefully acknowledged. This work was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; project SP292/22-1).
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Aschenbrenner, AK., Amrehn, E., Bechtel, L. et al. Trichome differentiation on leaf primordia of Helianthus annuus (Asteraceae): morphology, gene expression and metabolite profile. Planta 241, 837–846 (2015). https://doi.org/10.1007/s00425-014-2223-y
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DOI: https://doi.org/10.1007/s00425-014-2223-y