Protein and metabolite analysis reveals permanent induction of stress defense and cell regeneration processes in a tobacco cell suspension culture

International Journal of Molecular Sciences

Volumn 10, Issue 7, 2009, Pages 3012-3032

  Lippmann, Rico ^a   Kaspar, Stephanie ^a   Rutten, Twan ^a   Melzer, Michael ^a   Kumlehn, Jochen ^a   Matros, Andrea ^a   Mock, Hans Peter ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Apoplast; Extracellular proteins; Secreted putrescine; Suspension culture; Tobacco

Indexed keywords

BETA 1,4 XYLOSIDASE; CHITINASE; PEROXIDASE; PUTRESCINE; SECRETORY PROTEIN; UNCLASSIFIED DRUG; XYLAN 1,4 BETA XYLOSIDASE;

AMINO ACID SEQUENCE; ARTICLE; CELL CULTURE; CELL GROWTH; CELL MATURATION; CELL REGENERATION; CELL SUSPENSION; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; DEFENSE MECHANISM; ENERGY TRANSFER; MASS FRAGMENTOGRAPHY; METABOLITE; METABOLOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN DATABASE; PROTEOMICS; SIGNAL TRANSDUCTION; STRESS; TOBACCO; TWO DIMENSIONAL ELECTROPHORESIS;

APOPLAST; EXTRACELLULAR PROTEINS; SECRETED PUTRESCINE; SUSPENSION CULTURE; TOBACCO;

AMINO ACID SEQUENCE; CELL GROWTH PROCESSES; CELL LINE; CHITINASE; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; METABOLOME; MOLECULAR SEQUENCE DATA; PEROXIDASES; PLANT PROTEINS; PROTEOME; PUTRESCINE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOBACCO; XYLOSIDASES;

NICOTIANA; NICOTIANA TABACUM;

EID: 68949164558     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms10073012     Document Type: Article

References (51)

1. Oksman-Caldentey, K.M.; Inze, D. Plant cell factories in the post-genomic era: New ways to produce designer secondary metabolites. Trends Plant Sci. 2004, 9, 433-440. (Pubitemid 39160939)
2. Yeoman, M.M.; Yeoman, C.L. Tansley review no 90 - Manipulating secondary metabolism in cultured plant cells. New Phytol. 1996, 134, 553-569.
3. Dias, A.P.; Grotewold, E. Manipulating the accumulation of phenolics in maize cultured cells using transcription factors. Biochem. Eng. J. 2003, 14, 207-216. (Pubitemid 36565861)
4. Frick, S.; Kutchan, T.M. Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis. Plant J. 1999, 17, 329-339. (Pubitemid 129518126)
5. Arigoni, D.; Sagner, S.; Latzel, C.; Eisenreich, W.; Bacher, A.; Zenk, M.H. Terpenoid biosynthesis from 1-deoxy-D-xylulose in higher plants by intramolecular skeletal rearrangement. Proc. Natl. Acad. Sci. USA 1997, 94, 10600-10605.
6. Broeckling, C.D.; Huhman, D.V.; Farag, M.A.; Smith, J.T.; May, G.D.; Mendes, P.; Dixon, R.A.; Sumner, L.W. Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J. Exp. Bot. 2005, 56, 323-336.
7. Suzuki, H.; Reddy, M.S.S.; Naoumkina, M.; Aziz, N.; May, G.D.; Huhman, D.V.; Sumner, L.W.; Blount, J.W.; Mendes, P.; Dixon, R.A. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta 2005, 220, 696-707.
8. Sarry, J.E.; Kuhn, L.; Ducruix, C.; Lafaye, A.; Junot, C.; Hugouvieux, V.; Jourdain, A.; Bastien, O.; Fievet, J.B.; Vailhen, D.; Amekraz, B.; Moulin, C.; Ezan, E.; Garin, J.; Bourguignon, J. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 2006, 6, 2180-2198.
9. Kim, J.K.; Bamba, T.; Harada, K.; Fukusaki, E.; Kobayashi, A. Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J. Exp. Bot. 2007, 58, 415-424. (Pubitemid 46363188)
10. Lei, Z.; Elmer, A.M.; Watson, B.S.; Dixon, R.A.; Mendes, P.J.; Sumner, L.W. A two-dimensional electrophoresis proteomic reference map and systematic identification of 1367 proteins from a cell suspension culture of the model legume Medicago truncatula. Mol. Cell Proteomics 2005, 4, 1812-1825.
11. Tran, H.T.; Plaxton, W.C. Proteomic analysis of alterations in the secretome of Arabidopsis thaliana suspension cells subjected to nutritional phosphate deficiency. Proteomics 2008, 8, 4317-4326.
12. Okushima, Y.; Koizumi, N.; Kusano, T.; Sano, H. Secreted proteins of tobacco cultured BY2 cells: identification of a new member of pathogenesis-related proteins. Plant Mol. Biol. 2000, 42, 479-488. (Pubitemid 30213434)
13. Dani, V.; Simon, W.J.; Duranti, M.; Croy, R.R.D. Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 2005, 5, 737-745.
14. Sakurai, N. Dynamic function and regulation of apoplast in the plant body. J. Plant Res. 1998, 111, 133-148. (Pubitemid 128105797)
15. Kunze, I.; Kunze, G.; Broker, M.; Manteuffel, R.; Meins, F.; Muntz, K. Evidence for secretion of vacuolar alpha-mannosidase, class I chitinase, and class I beta-1,3-glucanase in suspension cultures of tobacco cells. Planta 1998, 205, 92-99. (Pubitemid 28205475)
16. Oh, I.S.; Park, A.R.; Bae, M.S.; Kwon, S.J.; Kim, Y.S.; Lee, J.E.; Kang, N.Y.; Lee, S.M.; Cheong, H.; Park, O.K. Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 2005, 17, 2832-2847.
17. Kauss, H.; Jeblick, W.; Ziegler, J.; Krabler, W. Pretreatment of Parsley (Petroselinum-Crispum L.) Suspension-Cultures with Methyl Jasmonate Enhances Elicitation of Activated Oxygen Species. Plant Physiol. 1994, 105, 89-94. (Pubitemid 2105086)
18. Berlin, J.; Mollenschott, C.; Wray, V. Triggered Efflux of Protoberberine Alkaloids from Cell- Suspension Cultures of Thalictrum-Rugosum. Biotechnol. Lett. 1988, 10, 193-198. (Pubitemid 18102065)
19. Kwon, H.K.; Yokoyama, R.; Nishitani, K. A proteomic approach to apoplastic proteins involved in cell wall regeneration in protoplasts of Arabidopsis suspension-cultured cells. Plant Cell Physiol. 2005, 46, 843-857. (Pubitemid 41435472)
20. van Loon, L.C.; van Strien, E.A. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 1999, 55, 85-97.
21. Hall, R.D. Plant metabolomics: from holistic hope, to hype, to hot topic. New Phytol. 2006, 169, 453-468.
22. Cvikrova, M.; Gemperlova, L.; Eder, J.; Zazimalova, E. Excretion of polyamines in alfalfa and tobacco suspension-cultured cells and its possible role in maintenance of intracellular polyamine contents. Plant Cell Rep. 2008, 27, 1147-1156.
23. Silveira, V.; Floh, E.I.S.; Handro, W.; Guerra, M.P. Effect of plant growth regulators on the cellular growth and levels of intracellular protein, starch and polyamines in embryogenic suspension cultures of Pinus taeda. Plant Cell Tissue Organ Cult. 2004, 76, 53-60.
24. Slocum, R.D.; Flores, H.E.; Galston, A.W.; Weinstein, L.H. Improved Method for Hplc Analysis of Polyamines, Agmatine and Aromatic Monoamines in Plant-Tissue. Plant Physiol. 1989, 89, 512-517.
25. Maliga, P.; Szbrezno, A.; Marton, L. Streptomycin-Resistant Plants from Callus Culture of Haploid Tobacco. Nature New Biol. 1973, 244, 29-30.
26. Linsmaier, E.M.; Skoog, F. Organic Growth Factor Requirements of Tobacco Tissue Cultures. Physiol. Plant 1965, 18, 100-127.
27. Widholm, J.M. Use of Fluorescein Diacetate and Phenosafranine for Determining Viability of Cultured Plant-Cells. Stain Technol. 1972, 47, 189-194.
28. Huang, C.N.; Cornejo, M.J.; Bush, D.S.; Jones, R.L. Estimating Viability of Plant-Protoplasts Using Double and Single Staining. Protoplasma 1986, 135, 80-87.
29. Bradford, M.M. Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248-254.
30. Wessel, D.; Flugge, U.I. A Method for the Quantitative Recovery of Protein in Dilute-Solution in the Presence of Detergents and Lipids. Anal. Biochem. 1984, 138, 141-143.
31. Amme, S.; Rutten, T.; Melzer, M.; Sonsmann, G.; Vissers, J.P.C.; Schlesier, B.; Mock, H.P. A proteome approach defines protective functions of tobacco leaf trichomes. Proteomics 2005, 5, 2508-2518.
32. Wen, F.S.; VanEtten, H.D.; Tsaprailis, G.; Hawes, M.C. Extracellular proteins in pea root tip and border cell exudates. Plant Physiol. 2007, 143, 773-783.
33. Masuda, H.; Ozeki, Y.; Amino, S.; Komamine, A. Changes in the Activities of Various Glycosidases during Carrot Cell Elongation in a 2,4-D-Free Medium. Plant Cell Physiol. 1985, 26, 995-1001.
34. Chivasa, S.; Simon, W.J.; Yu, X.L.; Yalpani, N.; Slabas, A.R. Pathogen elicitor-induced changes in the maize extracellular matrix proteome. Proteomics 2005, 5, 4894-4904.
35. Shih, Y.W.; Chou, W.C.; Lin, Y.M.; Huang, D.D.; Liu, Z.H.; Huang, H.J. Changes in protein tyrosine phosphorylation during mannose and senescence induced cell death in rice. Plant Growth Regul. 2004, 42, 271-282.
36. Payne, G.; Ahl, P.; Moyer, M.; Harper, A.; Beck, J.; Meins, F.; Ryals, J. Isolation of Complementary-DNA Clones Encoding Pathogenesis-Related Protein-P and Protein-Q, 2 Acidic Chitinases from Tobacco. Proc. Natl. Acad. Sci. USA 1990, 87, 98-102. (Pubitemid 20033014)
37. Kasprzewska, A. Plant chitinases - Regulation and function. Cell. Mol. Biol. Lett. 2003, 8, 809-824.
38. Vanbuuren, M.; Neuhaus, J.M.; Shinshi, H.; Ryals, J.; Meins, F. The Structure and Regulation of Homeologous Tobacco Endochitinase Genes of Nicotiana-Sylvestris and N-Tomentosiformis Origin. Mol. Gen. Genet. 1992, 232, 460-469.
39. Zhong, R.Q.; Kays, S.J.; Schroeder, B.P.; Ye, Z.H. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 2002, 14, 165-179.
40. van Hengel, A.J.; Tadesse, Z.; Immerzeel, P.; Schols, H.; van Kammen, A.; de Vries, S.C. Nacetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol. 2001, 125, 1880-1890.
41. Bakalovic, N.; Passardi, F.; Ioannidis, V.; Cosio, C.; Penel, C.; Falquet, L.; Dunand, C. PeroxiBase: A class III plant peroxidase database. Phytochemistry 2006, 67, 534-539.
42. Goossens, A.; Hakkinen, S.T.; Laakso, I.; Oksman-Caldentey, K.M.; Inze, D. Secretion of secondary metabolites by ATP-binding cassette transporters in plant cell suspension cultures. Plant Physiol. 2003, 131, 1161-1164. (Pubitemid 36400349)
43. Stevenson, J.M.; Pepera, I.Y.; Heilmann, I.; Persson, S.; Boss, W.F. Inositol signaling and plant growth. Trends Plant Sci. 2000, 5, 252-258.
44. Kusano, T.; Berberich, T.; Tateda, C.; Takahashi, Y. Polyamines: essential factors for growth and survival. Planta 2008, 228, 367-381.
45. Walters, D.R. Polyamines and plant disease. Phytochemistry 2003, 64, 97-107.
46. Bouchereau, A.; Aziz, A.; Larher, F.; Martin-Tanguy, J. Polyamines and environmental challenges: Recent development. Plant Sci. 1999, 140, 103-125.
47. Yoda, H.; Fujimura, K.; Takahashi, H.; Munemura, I.; Uchimiya, H.; Sano, H. Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection. Plant Mol. Biol. 2009, 70, 103-112.
48. Marina, M.; Maiale, S.J.; Rossi, F.R.; Romero, M.F.; Rivas, E.I.; Garriz, A.; Ruiz, O.A.; Pieckenstain, F.L. Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol. 2008, 147, 2164-2178.
49. Yoda, H.; Yamaguchi, Y.; Sano, H. Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 2003, 132, 1973-1981. (Pubitemid 37024158)
50. Boerjan, W.; Ralph, J.; Baucher, M. Lignin biosynthesis. Annu. Rev. Plant Biol. 2003, 54, 519-546.
51. Wink, M. The Cell-Culture Medium - A Functional Extracellular Compartment of Suspension-Cultured Cells. Plant Cell Tissue Organ Cult. 1994, 38, 307-319.