High resolution mass spectrometry imaging reveals the occurrence of phenylphenalenone-type compounds in red paracytic stomata and red epidermis tissue of Musa acuminata ssp. zebrina cv. 'Rowe Red'

Phytochemistry

Volumn 116, Issue 1, 2015, Pages 239-245

  Hölscher, Dirk ^a,b   Fuchser, Jens ^c   Knop, Katrin ^d,e   Menezes, Riya C ^a   Buerkert, Andreas ^b   Svatoš, Aleš ^a   Schubert, Ulrich S ^d   Schneider, Bernd ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b UNIVERSITY OF KASSEL   (Germany)

^c BRUKER DALTONIK GMBH   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e LONZA AG   (Switzerland)

Author keywords

Cell specific natural product analysis; Fourier transform ion cyclotron resonance; Laser microdissection; Mass spectrometric imaging; Matrix free UV laser desorption ionization; Musa acuminata ssp. zebrina cv. 'Rowe Red'; Musaceae; Phenylphenalenones

Indexed keywords

FUNGI; MUSA ACUMINATA; MUSACEAE; ZEBRINA;

PHENALENE DERIVATIVE;

CHEMICAL STRUCTURE; CHEMISTRY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; MUSA; PLANT EPIDERMIS;

MOLECULAR STRUCTURE; MUSA; PHENALENES; PLANT EPIDERMIS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84935018165     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2015.04.010     Document Type: Article

References (51)

1. Amantonico, A., Urban, P. L., Fagerer, R., Balabin, R. M., Zenobi, R., 2010. Single-cell MALDI-MS as an analytical tool for studying intrapopulation metabolic heterogeneity of unicellular organisms. Anal. Chem. 82, 7394-7400.
2. Arias, P., Dankers, C., Liu, P., Pilkauskas, P., 2003. The World Banana Economy 1985-2002. FAO Commodities Study 1. Raw Materials, Tropical and Horticultural Products Service (ESCR). Commodity and Trade Division FAO, Rome, Italy. Available at: (accessed January 03, 2014).
3. Beveraggi, A., Mourichon, X., Salle, G., 1995. Etude des interactions hôte-parasite chez des bananiers sensibles et résistants inoculés par Cercospora fijiensis (Mycosphaerella fijiensis) responsable de la maladie des raies noires. Can. J. Bot. 73, 1328-1337.
4. Brandt, S., Kloska, S., Altmann, T., Kehr, J., 2002. Using array hybridization to monitor gene expression at the single cell level. J. Exp. Bot. 53, 2315-2323.
5. Burrell, M. M., Earnshaw, C. J., Clench, M. R., 2007. Imaging matrix assisted laser desorption ionization mass spectrometry: a technique to map plant metabolites within tissues at high resolution. J. Exp. Bot. 58, 757-763.
6. Collingborn, F. M. B., Gowen, S. R., Mueller-Harvey, I., 2000. Investigations into the biochemical basis for nematode resistance in roots of three Musa cultivars in response to Radopholus similis infection. J. Agric. Food Chem. 48, 5297-5301.
7. Cooke, R. G., Segal, W., 1955. Colouring matters of Australian plants. IV. Haemocorin: a unique glycoside from Haemodorum corymbosum Vahl. Aust. J. Chem. 8, 107-113.
8. Cooke, R. G., Edwards, J. M., 1981. Naturally occurring phenalenones and related compounds. Fortschr. Chem. Org. Naturst. 40, 153-190.
9. Della Greca, M., Previtera, L., Zarrelli, A., 2008. Revised structures of phenylphenalene derivatives from Eichhornia crassipes. Tetrahedron Lett. 49, 3268-3272.
10. Dias, D. A., Goble, D. J., Silva, C. A., Urban, S., 2009. Phenylphenalenones from the Australian Plant Haemodorum simplex. J. Nat. Prod. 72, 1075-1080.
11. Emmert-Buck, M. R., Bonner, R. F., Smith, P. D., Chuaqui, R. F., Zhuang, Z., Goldstein, S. R., Weiss, R. A., Lotta, L. A., 1996. Laser capture microdissection. Science 274, 998-1001.
12. FAOSTAT, 2014. Trade - Crops and livestock products - Import and Export Quantity of Banana and Plantains for 2011. And Production - Crops - Production Quantity of Bananas and Plantains for 2012. Food and Agriculture Organization of United Nations. Available at: faostat3.fao-org (accessed January 03, 2014).
13. Fang, J. J., Paetz, C., Hölscher, D., Munde, T., Schneider, B., 2011. Phenylphenalenones and related natural products from Wachendorfia thyrsiflora L. Phytochem. Lett. 4, 203-208.
14. Fingolo, C. E., Braga, J. M. A., Vieira, A. C. M., Moura, M. R. L., Kaplan, M. A. C., 2012. The natural impact of banana inflorescences (Musa acuminata) on human nutrition. An. Acad. Bras. Ciênc. 84, 891-898.
15. Grassl, J., Taylor, N. L., Millar, A. H., 2011. Matrix-assisted laser desorption/ionization mass spectrometry imaging and its development for plant protein imaging. Plant Methods 7, 21.
16. Hirai, N., Ishida, H., Koshimizu, K., 1994. A phenalenone-type phytoalexin from Musa acuminata. Phytochemistry 37, 383-385.
17. Hölscher, D., Schneider, B., 1995. A diarylheptanoid intermediate in the biosynthesis of phenylphenalenones in Anigozanthos preissii. J. Chem. Soc. Chem. Commun., 525-526
18. Hölscher, D., Schneider, B., 2000. Phenalenones from Strelitzia reginae. J. Nat. Prod. 63, 1027-1028.
19. Hölscher, D., Schneider, B., 2007. Laser microdissection and cryogenic nuclear magnetic resonance spectroscopy: an alliance for cell type-specific metabolites profiling. Planta 225, 763-770.
20. Hölscher, D., Shroff, R., Knop, K., Gottschaldt, M., Crecelius, A., Schneider, B., Heckel, D. G., Schubert, U. S., Svatoš, 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.
21. Hölscher, D., Dhakshinamoorthy, S., Alexandrov, T., Becker, M., Bretschneider, T., Buerkert, A., Crecelius, A. C., De Waele, D., Elsen, A., Heckel, D. G., Heklau, H., Hertweck, C., Kai, M., Knop, K., Krafft, C., Maddula, R. K., Matthäus, C., Popp, J., Schneider, B., Schubert, U. S., Sikora, R. A., Svatoš, A., Swennen, R. L., 2014. Phenalenone-type phytoalexins mediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis. Proc. Natl. Acad. Sci. U. S. A. 111, 105-110.
22. Horn, P. J., Chapman, K. D., 2014. Lipidomics in situ: insights into plant lipid metabolism from high resolution spatial maps of metabolites. Prog. Lipid Res. 54, 32-52.
23. Jitsaeng, K., Schneider, B., 2010. Metabolic profiling of Musa acuminata with Sporobolomyces salmonicolor. Phytochem. Lett. 3, 84-87.
24. Jones, D. R. (Ed.), 1999. Diseases of Banana, Abacá and Enset. CABI Publishing, Wallingford, UK.
25. Kaftan, F., Vrkoslav, V., Kynast, P., Kulkarni, P., Böcker, S., Cvačka, J., Knaden, M., Svatoš, A., 2014. Mass spectrometry imaging of surface lipids on intact Drosophila melanogaster flies. J. Mass Spectrom. 49, 223-232.
26. Kruse, R. A., Rubakhin, S. S., Romanova, V., Bohn, P. W., Sweedler, J. V., 2001. Direct assay of Aplysia tissues and cells with laser desorption/ionization mass spectrometry on porous silicon. J. Mass Spectrom. 36, 1317-1322.
27. Lange, B. M., 2005. Single-cell genomics. Curr. Opin. Plant Biol. 8, 236-241.
28. Li, S. H., Nagy, N. E., Hammerbacher, A., Krokene, P., Niu, X. M., Gershenzon, J., Schneider, B., 2012. Localization of phenolics in phloem parenchyma cells of Norway spruce (Picea abies). Chembiochem 13, 2707-2713.
29. Li, B., Bhandari, D. R., Janfelt, C., Römpp, A., Spengler, B., 2014. Natural products in Glycyrrhiza glabra (licorice) rhizome imaged at the cellular level by atmospheric pressure matrix-assisted laser desorption/ionization tandem mass spectrometry imaging. Plant J. 80, 161-171.
30. Luis, J. G., Echeverri, F., Quiñones, W., Brito, I., López, M., Torres, F., Cardona, G., Aguiar, Z., Pelaez, C., Rojas, M., 1993. Irenolone and emenolone: two new types of phytoalexin from Musa paradisiaca. J. Org. Chem. 58, 4306-4308.
31. Luis, J. G., Fletcher, W. Q., Echeverri, F., Grillo, T. A., 1994. Phenalenone-type phytoalexins from Musa acuminata - synthesis of 4-phenyl-phenalenones. Tetrahedron 50, 10963-10970.
32. Mobambo, K., Gauhl, F., Vuylsteke, D., Ortiz, R., Pasberg-Gauhl, C., Swennen, R., 1993. Yield losses in plantain from black sigatoka leaf spot and field performance of resistant hybrids. Field Crops Res. 35, 35-42.
33. Munde, T., Brand, S., Hidalgo, W., Maddula, R. K., Svatoš, A., Schneider, B., 2013. Biosynthesis of tetraoxygenated phenylphenalenones in Wachendorfia thyrsiflora. Phytochemistry 91, 165-176.
34. Opitz, S., Schnitzler, J.-P., Hause, B., Schneider, B., 2003. Histochemical analysis of phenylphenalenone-related compounds in Xiphidium caeruleum (Haemodoraceae). Planta 216, 881-889.
35. Ostrowski, S. G., Van Bell, C. T., Winograd, N., Ewing, A. G., 2004. Mass spectrometric imaging of highly curved membranes during Tetrahymena mating. Science 305, 71-73.
36. Ostrowski, S. G., Kurczy, M. E., Roddy, T. P., Winograd, N., Ewing, A. G., 2007. Secondary ion MS imaging to relatively quantify cholesterol in the membranes of individual cells from differentially treated populations. Anal. Chem. 79, 3554-3560.
37. Otálvaro, F., Görls, F., Hölscher, D., Schmitt, B., Echeverri, F., Quiñones, W., Schneider, B., 2002. Dimeric phenylphenalenones from Musa acuminata and various Haemodoraceae species. Crystal structure of anigorootin. Phytochemistry 60, 61-66.
38. Otálvaro, F., Nanclares, J., Vásquez, L. E., Quiñones, W., Echeverri, F., Arango, R., Schneider, B., 2007. Phenalenone-type compounds from Musa acuminata var. "Yangambi km 5" (AAA) and their activity against Mycosphaerella fijiensis. J. Nat. Prod. 70, 887-890.
39. Schneider, B., Paetz, C., Hölscher, D., Opitz, S., 2005. HPLC-NMR for tissue-specific analysis of phenylphenalenone-related compounds in Xiphidium caeruleum (Haemodoraceae). J. Magn. Reson. 43, 724-728.
40. Schulze, R., 1893. Beiträge zur vergleichenden Anatomie der Liliaceen, Haemodoraceen, Hypoxidioideen und Velloziaceen. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 17, 295-394.
41. Shen, M., Xiang, P., Shi, Y., Pu, H., Yan, H., Shen, B., 2014. Mass imaging of ketamine in a single scalp hair by MALDI-FTMS. Anal. Bioanal. Chem. 406, 4611-4616.
42. Shroff, R., Vergara, F., Muck, A., Svatoš, A., Gershenzon, J., 2008. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl. Acad. Sci. U. S. A. 105, 6196-6201.
43. Sumner, L. W., Mendes, P., Dixon, R. A., 2003. Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62, 817-836.
44. Toue, S., Sugiura, Y., Kubo, A., Ohmura, M., Karakawa, S., Mizukoshi, T., Yoneda, J., Miyano, H., Noguchi, Y., Kobayashi, T., Kabe, Y., Suematsu, M., 2014. Microscopic imaging mass spectrometry assisted by on-tissue chemical derivatization for visualizing multiple amino acids in human colon cancer xenografts. Proteomics 14, 810-819.
45. Tsai, Y. P., Chen, H. P., Liu, S. H., 1993. Freckle disease of banana in Taiwan. In: Proceedings of the International Symposium on Recent Developments in Banana Cultivation Technology, Pingtung, Taiwan. INIBAP-ASPNET, Los Banos (PHL), pp. 298-307.
46. Vargas, A., Sandoval, J., 2005. Agronomic evaluation of production and quality of 'Yangambi km 5' (AAA) and 'Dátil' (AA). InfoMusa 14, 6-10.
47. Walker, B. N., Antonakos, C., Retterer, T., Vertes, A., 2013. Metabolic differences in microbial cell populations revealed by nanophotonic ionization. Angew. Chem. Int. Ed. 52, 3650-3653.
48. Webb, L. J., 1948. Guide to the medicinal and poisonous plants of Queensland. Bulletin No. 232, p. 65.
49. Winters, K., Batterton, J. C., Van Baalen, C., 1977. Phenalen-1-one: occurrence in a fuel oil and toxicology to microalgae. Environ. Sci. Technol. 11, 270-272.
50. Wong, M.-H., Crous, P. W., Henderson, J., Groenewald, J. Z., Drenth, A., 2012. Phyllosticta species associated with freckle disease of banana. Fungal Divers. 56, 173-187.
51. Zhang, L., Foreman, D. P., Grant, P. A., Shrestha, B., Moody, S. A., Villiers, F., Kwak, J. M., Vertes, A., 2014. In situ metabolic analysis of single plant cells by capillary microsampling and electrospray ionization mass spectrometry with ion mobility separation. Analyst 139, 5079-5085.