Quantification of plant surface metabolites by matrix-assisted laser desorption-ionization mass spectrometry imaging: Glucosinolates on Arabidopsis thaliana leaves

Plant Journal

Volumn 81, Issue 6, 2015, Pages 961-972

  Shroff, Rohit ^a   Schramm, Katharina ^a,c   Jeschke, Verena ^a   Nemes, Peter ^b   Vertes, Akos ^b   Gershenzon, Jonathan ^a   Svatoš, Aleš ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

abaxial surface; adaxial surface; Arabidopsis thaliana; insect oviposition; leaf surface; liquid extraction surface analysis; MALDI imaging; Pieris rapae; Plutella xylostella; technical advance

Indexed keywords

BIOMOLECULES; DESORPTION; ELECTROSPRAY IONIZATION; EXTRACTION; LASER ABLATION; MASS SPECTROMETRY; PLANTS (BOTANY); SULFUR COMPOUNDS; SURFACE ANALYSIS;

ARABIDOPSIS THALIANA; INSECT OVIPOSITION; LEAF SURFACES; LIQUID EXTRACTION; PIERIS RAPAE; PLUTELLA XYLOSTELLA; TECHNICAL ADVANCES;

METABOLITES;

ARABIDOPSIS THALIANA; BRASSICALES; HEXAPODA; LEPIDOPTERA; PIERIS RAPAE; PLUTELLA XYLOSTELLA;

4-METHYLTHIOBUTYLGLUCOSINOLATE; BUTYRIC ACID DERIVATIVE; GLUCOSINOLATE; THIOGLYCOSIDE;

ANIMAL; ARABIDOPSIS; BUTTERFLY; EGG LAYING; FEMALE; MASS SPECTROMETRY; METABOLISM; MOTH; PHYSIOLOGY; PLANT LEAF; PROCEDURES;

ANIMALS; ARABIDOPSIS; BUTTERFLIES; BUTYRATES; FEMALE; GLUCOSINOLATES; MOTHS; OVIPOSITION; PLANT LEAVES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THIOGLUCOSIDES;

EID: 84924322632     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12760     Document Type: Article

References (61)

1. Badenes-Pérez, F.R., Reichelt, M., Gershenzon, J., and, Heckel, D.G., (2011) Phylloplane location of glucosinolates in Barbarea spp. (Brassicaceae) and misleading assessment of host suitability by a specialist herbivore. New Phytol. 189, 549-556.
2. Bednarek, P., Pislewska-Bednarek, M., Svatos, A., et al. (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science, 323, 101-106.
3. Brader, G., Tas, E., and, Palva, E.T., (2001) Jamsonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol. 126, 849-860.
4. Brooks, J.S., Williams, E.H., and, Feeny, P., (2003) Quantification of contact oviposition stimulants for black swallowtail butterfly, Papilio polyxenes, on the leaf surfaces of wild carrot, Daucus carota. J. Chem. Ecol. 22, 2341-2357.
5. Brown, P.D., Tokuhisa, J.G., Reichelt, M., and, Gershenzon, J., (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry, 62, 471-481.
6. Buschhaus, C., and, Jetter, R., (2012) Composition and physiological function of the wax layers coating Arabidopsis leaves: β-amyrin negatively affects the intracuticular water barrier. Plant Physiol. 120, 1160-1169.
7. Clay, N.K., Adio, A.M., Denoux, C., Jander, G., and, Ausubel, F.M., (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science, 323, 95-101.
8. Dominguez, E., Heredia-Guerrero, J.A., and, Heredia, A., (2011) The biophysical design of plant cuticles: an overview. New Phytol. 189, 938-949.
9. Ensikat, H.J., Neinhuis, C., and, Barthlott, W., (2000) Direct access to plant epicuticular wax crystals by a new mechanical isolation method. Int. J. Plant Sci. 161, 143-148.
10. Franke, R., Briesen, I., Wojciechowski, T., Faust, A., Yephremov, A., Nawrath, C., and, Schreiber, L., (2005) Apoplastic polyesters in Arabidopsis surface tissues-A typical suberin and a particular cutin. Phytochemistry, 66, 2643-2658.
11. Frerigmann, H., Böttcher, C., Baatout, D., and, Gigolashvili, T., (2012) Glucosinolates are produced in trichomes of Arabidopsis thaliana. Front. Plant Sci. 3, 242.
12. Green, P.W.C., Stevenson, P.C., Simmonds, M.S.J., and, Sharma, H.C., (2003) Phenolic compounds on the pod-surface of pigeonpea, Cajanus cajan, mediate feeding behavior of Helicoverpa armigera larvae. J. Chem. Ecol. 29, 811-821.
13. Griffiths, D.W., Deighton, N., Birch, A.N.E., Patrian, B., Baur, R., and, Städler, E., (2001) Identification of glucosinolates on the leaf surface of plants from the Cruciferae and other closely related species. Phytochemistry, 57, 693-700.
14. Halkier, B.A., and, Gershenzon, J., (2006) Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
15. Hankin, J.A., Barkley, R.M., and, Murphy, R.C., (2007) Sublimation as a method of matrix application for mass spectrometric imaging. J. Am. Soc. Mass Spectrom. 18, 1646-1652.
16. Hiruna, K., Onozawa-Komori, M., Takahashi, F., Asakura, M., Bednarek, P., Okuno, T., Schulze-Lefert, P., and, Takano, Y., (2010) Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell, 22, 2429-2443.
17. Hölscher, D., Shroff, R., Knop, K., Gottschaldt, M., Crecelius, A., Schneider, B., Heckel, D.G., Schubert, U.S., and, Svatos, A., (2009) Matrix-free UV-laser desorption/ionization (LDI) mass spectrometric imaging at the single-cell level: distribution of secondary metabolites of Arabidopsis thaliana and Hypericum species. Plant J. 60, 907-918.
18. Hopkins, R.J., Birch, A.N.E., Griffiths, D.W., Baur, R., Städler, E., and, McKinlay, R.G., (1997) Leaf surface compounds and oviposition preference of turnip root fly Delia floralis: the role of glucosinolate and non-glucosinolate compounds. J. Chem. Ecol. 23, 629-643.
19. Huang, X.P., and, Renwick, J.A.A., (1994) Relative activities of glucosinolates as oviposition stimulants for Pieris rapae and P. napi oleracea. J. Chem. Ecol. 20, 1025-1037.
20. Huang, X.P., Renwick, J.A.A., and, Sachdev-Gupta, K., (1994) Oviposition stimulants in Barbarea vulgaris for Pieris rapae and P. napi oleracea: isolation, identification and differential activity. J. Chem. Ecol. 20, 423-438.
21. Hughes, P.R., Renwick, J.A., and, Lopez, K.D., (1997) New oviposition stimulants for the diamondback moth in cabbage. Entomol. Exp. Appl. 85, 281-283.
22. Jetter, R., and, Schäffer, S., (2001) Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant Physiol. 126, 1-13.
23. Kaspar, S., Peukert, M., Svatoš, A., Matros, A., and, Mock, H.-P., (2011) MALDI-Imaging mass spectrometry-an emerging technique in plant biology. Proteomics, 11, 1840-1850.
24. Kertesz, V., and, Van Berkel, G.J., (2009) Fully automated liquid extraction-based surface sampling and ionization using a chip-based robotic nanoelectrospray platform. J. Mass Spectrom. 45, 252-260.
25. Kolb, C.A., and, Pfündel, E.E., (2005) Origins of non-linear and dissimilar relationships between epidermal UV absorbance and UV absorbance of extracted phenolics in leaves of grapevine and barley. Plant Cell Environ. 25, 580-590.
26. Lee, Y.J., Perdian, D.C., Song, Z.H., Yeung, E.S., and, Nikolau, B.J., (2012) Use of mass spectrometry for imaging metabolites in plants. Plant J. 70, 81-95.
27. van Loon, J.J.A., Blaakmeer, A., Griepink, F.C., van Beek, T.A., Schoonhoven, L.M., and, de Groot, A., (1992) Leaf surface compound from Brassica oleracea (Cruciferae) induces oviposition by Pieris brassicae (Lepidoptera: Pieridae). Chemoecology, 3, 39-44.
28. Marazzi, C., Patrian, B., and, Städler, E., (2004) Secondary metabolites of the leaf surface affected by sulfur fertilization and perceived by the cabbage root fly. Chemoecology, 14, 87-94.
29. Mewis, I.Z., Ulrich, C., and, Schnitzler, W.H., (2002) The role of glucosinolates and their hydrolysis products in oviposition and host-plant finding by cabbage webworm, Hellula undalis. Entomol. Exp. Appl. 105, 129-139.
30. Miles, C.I., del Campo, M., and, Renwick, J.A.A., (2005) Behavioral and chemosensory responses to a host recognition cue by larvae of Pieris rapae. J. Comp. Physiol. A. 191, 147-155.
31. Müller, C., and, Riederer, M., (2005) Plant-surface properties in chemical ecology. J. Chem. Ecol. 31, 2621-2651.
32. Müller, R., de Vos, M., Sun, J.Y., Sonderby, I.E., Halkier, B.A., Wittstock, U., and, Jander, G., (2010) Differential effects of indole and aliphatic glucosinolates on lepidopteran herbivores. J. Chem. Ecol. 36, 905-913.
33. Nemes, P., and, Vertes, A., (2007) Laser ablation electrospray ionization for atmospheric pressure, in vivo, and imaging mass spectrometry. Anal. Chem. 79, 8098-8106.
34. Nemes, P., and, Vertes, A., (2010) Atmospheric-pressure molecular imaging of biological tissues and biofilms by LAESI mass spectrometry. J. Vis. Exp. 43, e2097. doi: 10.3971/2097.
35. Nemes, P., Barton, A.A., and, Vertes, A., (2009) Three-Dimensional imaging of metabolites in tissues under ambient conditions by laser ablation electrospray ionization mass spectrometry. Anal. Chem. 81, 6668-6675.
36. Nemes, P., Woods, A.S., and, Vertes, A., (2010) Simultaneous imaging of small metabolites and lipids in rat brain tissues at atmospheric pressure by laser ablation electrospray ionization mass spectrometry. Anal. Chem. 3, 982-988.
37. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org/.
38. Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T., and, Kroymann, J., (2002) Disarming the mustard oil bomb. Proc. Natl Acad. Sci. USA, 99, 11223-11228.
39. Reed, D.W., Pivnick, K.A., and, Underhill, E.W., (1989) Identification of chemical oviposition stimulants for the diamondback moth, Plutella xylostella, present in three species of Brassicaceae. Entomol. Exp. Appl. 53, 277-286.
40. Reifenrath, K., Riederer, M., and, Müller, C., (2005) Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae. Entomol. Exp. Appl. 115, 41-50.
41. Renwick, J.A.A., Radke, C.D., Sachdev-Gupta, K., and, Städler, E., (1992) Leaf surface chemicals stimulating oviposition by Pieris rapae (Lepidoptera: Pieridae) on cabbage. Chemoecology, 3, 33-38.
42. Renwick, J.A.A., Haribel, M., Gouinguene, S., and, Städler, E., (2006) Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella. J. Chem. Ecol. 32, 755-766.
43. Ringelmann, A., Riedel, M., Riederer, M., and, Hildebrandt, U., (2009) Two sides of a leaf blade: Blumeria graminis needs chemical cues in cuticular waxes of Lolium perenne for germination and differentiation. Planta, 230, 95-105.
44. Sarsby, J., Towers, M.W., Stain, C., Cramer, R., and, Koroleva, O.A., (2012) Mass spectrometry imaging of glucosinolates in Arabidopsis flowers and siliques. Phytochemistry, 77, 110-118.
45. Scheubert, K., Hufsky, F., Zichner, T., Kai, M., Svatoš, A., and, Böcker, S., (2012) Identifying the unknowns by aligning fragmentation trees. Anal. Chem. 84, 3417-3426.
46. Schmitt, M., Knopp, G., Materny, A., and, Kiefer, W., (1997) Femtosecond timeresolved coherent anti-Stokes Raman scattering for the simultaneous study of ultrafast ground and excited state dynamics: iodine vapour. Chem. Phys. Lett. 270, 9-15.
47. Schoonhoven, L.M., van Loon, J.J.A., and, Dicke, M., (2005) Insect-Plant Biology, 2nd edn. Oxford: Oxford University Press, p. 421.
48. Shelton, A.M., Cooley, R.J., Kroening, M.K., Wilsey, W.T., and, Eigenbrode, S.D., (1991) Comparative analysis of two rearing procedures for diamondback moth, Plutella xylostella (Lepidoptera:Plutellidae). J. Entomol. Sci., 26, 17-26.
49. Shroff, R., Vergara, F., Muck, A., Svatos, A., and, Gershenzon, J., (2008) Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl Acad. Sci. USA, 105, 6196-6201.
50. Spencer, J.L., Pillai, S., and, Bernays, E.A., (1999) Synergism in the oviposition behavior of Plutella xylostella: sinigrin and wax compounds. J. Insect Behav. 12, 483-499.
51. Städler, E., (1991) Behavioral responses of insects to plant secondary compounds. In Herbivores: Their Interaction with Secondary Metabolites, 2nd edn, Vol. 2 (, Rosenthal, G.A., and, Berenbaum, M.R., eds). New York: Academic Press, pp. 45-88.
52. Städler, E., and, Reifenrath, K., (2009) Glucosinolates on the leaf surface perceived by insect herbivores: review of ambiguous results and new investigations. Phytochem. Rev. 8, 207-225.
53. Städler, E., and, Roessingh, P., (1991) Perception of surface chemicals by feeding and ovipositing insects. In Proceedings of the 7th International Symposium on Insect-Plant Relationships. Symp Biol Hung 39 (, Szentesi, A., and, Jermy, T., eds). Budapest: Akadémia Kiadó, pp. 71-86.
54. Stracke, R., Ishihara, H., Huep, G., Barsch, A., Mehrtens, F., Niehaus, K., and, Weisshar, B., (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J. 50, 660-677.
55. Sun, J.Y., Sonderby, I.E., Halkier, B.A., Jander, G., and, de Vos, M., (2009) Non-volatile intact indole glucosinolates are host recognition cues for ovipositing Plutella xylostella. J. Chem. Ecol. 35, 1427-1436.
56. Svatos, A., (2010) Mass spectrometric imaging of small molecules. Trends Biotechnol. 28, 425-434.
57. Svatoš, A., and, Mock, H.-P., (2013) MALDI mass spectrometric imaging of plants. In The Handbook of Plant Metabolomics. (, Weckwerth, W., and, Kahl, G., eds). Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA, pp. 93-110.
58. Takai, N., Tanaka, Y., Inazawa, K., and, Saji, H., (2012) Quantitative analysis of pharmaceutical drug distribution in multiple organs by imaging mass spectrometry. Rapid Commun. Mass Spectrom. 26, 1549-1556.
59. Traynier, R.M.M., and, Truscott, R.J.W., (1991) Potent natural egg-laying stimulant for cabbage butterfly Pieris rapae. J. Chem. Ecol. 17, 1371-1380.
60. Vrkoslav, V., Muck, A., Cvacka, J., and, Svatos, A., (2010) MALDI imaging of neutral cuticular lipids in insects and plants. J. Am. Soc. Mass Spectrom. 21, 220-231.
61. Walter, A., Erdmann, S., Bocklitz, T., Jung, E.M., Vogler, N., Akimov, D., Dietzek, B., Roesch, P., Kothe, E., and, Popp, J., (2010) Analysis of the cytochrome distribution via linear and nonlinear Raman spectroscopy. Analyst, 138, 908-917.