Multiphoton fluorescence lifetime imaging shows spatial segregation of secondary metabolites in Eucalyptus secretory cavities

Journal of Microscopy

Volumn 247, Issue 1, 2012, Pages 33-42

  Heskes, A M ^a   Lincoln, C N ^a,b   Goodger, J Q D ^a   Woodrow, I E ^a   Smith, T A ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Essential oil; Eucalypt; FLIM; Monoterpene; Oil gland; Oleuropeic acid

Indexed keywords

BIOMOLECULES; ESSENTIAL OILS; FLUORESCENCE IMAGING; FLUOROPHORES; METABOLITES; PLANTS (BOTANY);

EUCALYPT; FLIM; FLUORESCENCE LIFETIME IMAGING; MULTIPHOTON FLUORESCENCE; NONVOLATILE; OIL GLANDS; OLEUROPEIC ACID; SECONDARY METABOLITES; SECRETORY CAVITIES; SECRETORY CELLS;

MONOTERPENES;

CINEOLE; ESSENTIAL OIL; TERPENE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; DIFFUSION; EUCALYPTUS; EUCALYPTUS POLYBRACTEA; EXTRACELLULAR MATRIX; METABOLITE; MULTIPHOTON FLUORESCENCE LIFETIME IMAGING; MULTIPHOTON MICROSCOPY; NONHUMAN; PLANT LEAF; PLANT TISSUE; PRIORITY JOURNAL; SECRETORY CELL; SECRETORY PATHWAY;

EUCALYPTUS; EUCALYPTUS POLYBRACTEA;

EID: 84862188929     PISSN: 00222720     EISSN: 13652818     Source Type: Journal    
DOI: 10.1111/j.1365-2818.2011.03593.x     Document Type: Article

References (51)

1. Aker, J., Hesselink, R., Engel, R., Karlova, R., Borst, J.W., Visser, A.J.W.G. & de Vries, S.C. (2007) In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using Förster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy. Plant Physiol. 145, 339-350.
2. Ascensao, L., Marques, N. & Pais, M.S. (1997) Peltate glandular trichomes of Leonotis leonurus leaves: ultrastructure and histochemical characterization of secretions. Int. J. Plant Sci. 158, 249-258.
3. Ascensao, L., Mota, L. & Castro, M.D. (1999) Glandular trichomes on the leaves and flowers of Plectranthus ornatus: morphology, distribution and histochemistry. Ann. Bot. 84, 437-447.
4. Babourina, O. & Rengel, Z. (2009) Uptake of aluminium into Arabidopsis root cells measured by fluorescent lifetime imaging. Ann. Bot. 104, 189-195.
5. Bago, B., Zipfel, W., Williams, R.M. et al. (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol. 128, 108-124.
6. Becker, W. (2005) Advanced Time-Correlated Single Photon Counting Techniques. Springer-Verlag, Berlin.
7. Benayoun, J. & Fahn, A. (1979) Intracellular transport and elimination of resin from epithelial duct-cells of Pinus halepensis. Ann. Bot. 43, 179-181.
8. Berezin, M.Y. & Achilefu, S. (2010) Fluorescence lifetime measurements and biological imaging. Chem. Rev. 110, 2641-2684.
9. Bernoux, M., Timmers, T., Jauneau, A., Brière, C., de Wit, P.J.G.M., Marco, Y. & Deslandes, L. (2008) RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20, 2252-2264.
10. Bosabalidis, A. & Tsekos, I. (1982a) Glandular scale development and essential oil secretion in Origanum dictamnus L. Planta 156, 496-504.
11. Bosabalidis, A. & Tsekos, I. (1982b) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. II. Development of the essential oil-accumulating central space of the gland and process of active secretion. Protoplasma 112, 63-70.
12. Boutant, E., Didier, P., Niehl, A., Mély, Y., Ritzenthaler, C. & Heinlein, M. (2010) Fluorescent protein recruitment assay for demonstration and analysis of in vivo protein interactions in plant cells and its application to Tobacco mosaic virus movement protein. Plant J. 62, 171-177.
13. Broess, K., Borst, J.W. & van Amerongen, H. (2009) Applying two-photon excitation fluorescence lifetime imaging microscopy to study photosynthesis in plant leaves. Photosynth. Res. 100, 89-96.
14. Bücherl, C., Aker, J., de Vries, S. & Borst, J.W. (2010) Probing protein-protein interactions with FRET-FLIM. Methods Mol. Biol. 655, 389-399.
15. Carr, D.J. & Carr, S.G.M. (1970) Oil glands and ducts in Eucalyptus L'Hérit. II. Development and structure of oil glands in the embryo. Aust. J. Bot. 18, 191-212.
16. Centonze, V.E. & White, J.G. (1998) Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging. Biophys. J. 75, 2015-2024.
17. Chappelle, E.W., McMurtrey, J.E. & Kim, M.S. (1991) Identification of the pigment responsible for the blue fluorescence band in the laser induced fluorescence (LIF) spectra of green plants, and the potential use of this band in remotely estimating rates of photosynthesis. Remote Sens. Environ. 36, 213-218.
18. Cser, A., Nagy, K. & Biczók, L. (2002) Fluorescence lifetime of Nile Red as a probe for the hydrogen bonding strength with its microenvironment. Chem. Phys. Lett. 360, 473-478.
19. Denk, W., Strickler, J.H. & Webb, W.W. (1990) Two-photon laser scanning fluorescence microscopy. Science 248, 73-76.
20. Feijó, J.A. & Moreno, N. (2004) Imaging plant cells by two-photon excitation. Protoplasma 223, 1-32.
21. Gersbach, P.V. (2002) The essential oil secretory structures of Prostanthera ovalifolia (Lamiaceae). Ann. Bot. 89, 255-260.
22. Goodger, J.Q.D. & Woodrow, I.E. (2009) The influence of ontogeny on essential oil traits when micropropagating Eucalyptus polybractea. Forest Ecol. Manag. 258, 650-656.
23. Goodger, J.Q.D. & Woodrow, I.E. (2011) α, β-Unsaturated monoterpene acid glucose esters: structural diversity, bioactivities and functional roles. Phytochemistry 72, 2259-2266.
24. Goodger, J.Q.D., Connelly, C.A. & Woodrow, I.E. (2007) Examination of the consistency of plant traits driving oil yield and quality in short-rotation coppice cultivation of Eucalyptus polybractea. Forest Ecol. Manag. 250, 196-205.
25. Goodger, J.Q.D., Cao, B., Jayadi, I., Williams, S.J. & Woodrow, I.E. (2009) Non-volatile components of the essential oil secretory cavities of Eucalyptus leaves: discovery of two glucose monoterpene esters, cuniloside B and froggattiside A. Phytochemistry 70, 1187-1194.
26. Goodger, J.Q.D., Heskes, A.M., Mitchell, M.C., King, D.J., Neilson, E.H. & Woodrow, I.E. (2010) Isolation of intact sub-dermal secretory cavities from Eucalyptus. Plant Methods 6, 20.
27. + antiporter activity of the SOS1 gene: lifetime imaging analysis and electrophysiological studies on Arabidopsis seedlings. Physiol. Plantarum 137, 155-165.
28. Hakki, Z., Cao, B., Heskes, A.M., Goodger, J.Q.D., Woodrow, I.E. & Williams, S.J. (2010) Synthesis of the monoterpenoid esters cypellocarpin C and cuniloside B and evidence for their widespread occurrence in Eucalyptus. Carbohydr. Res. 345, 2079-2084.
29. Helmchen, F. & Denk, W. (2005) Deep tissue two-photon microscopy. Nat. Methods 2, 932-940.
30. Hutzler, P., Fischbach, R., Heller, W. et al. (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J. Exp. Bot. 49, 953-965.
31. Kalachanis, D. & Psaras, G.K. (2005) Structure and development of the secretory cavities of Myrtus communis leaves. Biologia Plantarum 49, 105-110.
32. Knight, T.G., Klieber, A. & Sedgley, M. (2002) Structural basis of the rind disorder oleocellosis in Washington Navel orange (Citrus sinensis L. Osbeck). Ann. Bot. 90, 765-773.
33. Kuimova, M.K., Botchway, S.W., Parker, A.W. et al. (2009) Imaging intracellular viscosity of a single cell during photoinduced cell death. Nat. Chem. 1, 69-73.
34. Lakowicz, J.R., Szmacinski, H., Nowaczyk, K. & Johnson, M.L. (1992) Fluorescence lifetime imaging of free and protein-bound NADH. Proc. Natl. Acad. Sci. U S A 89, 1271-1275.
35. Latouche, G., Cerovic, Z.G., Montagnini, F. & Moya, I. (2000) Light-induced changes of NADPH fluorescence in isolated chloroplasts: a spectral and fluorescence lifetime study. Biochim. Biophys. Acta 1460, 311-329.
36. Levitt, J.A., Matthews, D.R., Ameer-Beg, S.M. & Suhling, K. (2009) Fluorescence lifetime and polarization-resolved imaging in cell biology. Curr. Opin. Biotechnol. 20, 28-36.
37. Lichtenthaler, H.K. & Schweiger, J. (1998) Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of plants. J. Plant Physiol. 152, 272-282.
38. Lippincott-Schwartz, J. & Patterson, G.H. (2009) Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol. 19, 555-565.
39. Morales, F., Cerovic, Z.G. & Moya, I. (1996) Time-resolved blue-green fluorescence of sugar beet (Beta vulgaris L.) leaves. Spectroscopic evidence for the presence of ferulic acid as the main fluorophore of the epidermis. Biochim. Biophys Acta (BBA) - Bioenerg. 1273, 251-262.
40. Morales, F., Cartelat, A., Alvarez-Fernandez, A., Moya, I. & Cerovic, Z.G. (2005) Time-resolved spectral studies of blue-green fluorescence of artichoke (Cynara cardunculus L. var. scolymus) leaves: identification of chlorogenic acid as one of the major fluorophores and age-mediated changes. J. Agric. Food Chem. 53, 9668-9678.
41. Nagy, N.E., Franceschi, V.R., Solheim, H., Krekling, T. & Christiansen, E. (2000) Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am. J. Bot. 87, 302-313.
42. Periasamy, A. & Clegg, R.M. (2009) FLIM Microscopy in Biology and Medicine. Chapman Hall/CRC Press, Boca Raton, FL.
43. Rodrigues, T.M., Teixeira, S.d.P. & Machado, S.R. (2011) The oleoresin secretory system in seedlings and adult plants of copaíba (Copaifera langsdorffii Desf., Leguminosae-Caesalpinioideae). Flora-Morphol. Distrib. Funct. Ecol. Plants 206, 585-594.
44. 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, 329-336.
45. Smith, T.A., Lincoln, C.N. & Bird, D.K. (2009) Time-resolved fluorescence in microscopy. Fluorescence Applications in Biotechnology and the Life Sciences (ed. by E.M. Goldys) pp. 195-222. Wiley-Blackwell, Hoboken, NJ.
46. Suhling, K., Siegel, J., Lanigan, P.M.P. et al. (2004) Time-resolved fluorescence anisotropy imaging applied to live cells. Opt. Lett. 29, 584-586.
47. Turner, G.W., Berry, A.M. & Gifford, E.M. (1998) Schizogenous secretory cavities of Citrus limon (L.) Burm. F. and a reevaluation of the lysigenous gland concept. Int. J. Plant Sci. 159, 75-88.
48. Turner, G.W., Gershenzon, J. & Croteau, R.B. (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol. 124, 665-680.
49. Vroom, J.M., De Grauw, K.J., Gerritsen, H.C. et al. (1999) Depth penetration and detection of pH gradients in biofilms by two-photon excitation microscopy. Appl. Environ. Microbiol. 65, 3502-3511.
50. Wuyts, N., Palauqui, J.C., Conejero, G., Verdeil, J.L., Granier, C. & Massonnet, C. (2010) High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6, 17.
51. Yamasaki, Y. & Akimitsu, K. (2007) In situ localization of gene transcriptions for monoterpene synthesis in irregular parenchymic cells surrounding the secretory cavities in rough lemon (Citrus jambhiri). J. Plant Physiol. 164, 1436-1448.