Biotechnology & Biotechnological Equipment 18 (2), 34 - 46 (2004)
Inhibition of apoptotic cell death induced by Pseudomonas syringae pv. tabaci and mycotoxin fumonizin B1
E. Iakimova1 , R. Batchvarova1 , V. Kapchina-Toteva2 , A. Atanassov1 , E. Woltering3 AgroBioInstitute, 1164 Sofia, 8 Dragan Tzankov Blvd., Bulgaria Sofia University “St. Kliment Ohridski”, Faculty of Biology,
Department of Biochemistry, 8 Dragan Tzankov blvd, Sofia, Bulgaria Wageningen University, Unit Agrotechnology & Food Innovation, The Netherlands
Abstract The impact of programmed cell death (PCD) inhibitors on lesion formation and biochemical events in transgenic (ttr line) and non-transgenic (Nevrokop 1164) tobacco infected with Pseudomonas syringae pv. tabaci was tested. Programmed cell death in tomato cell culture was induced by Fumonisin B1 (FUM) and effectively abolished by the administration of protease inhibitors and lanthanum. Caspase inhibitors Ac-YVAD-CMK and Z-asp-CH2-DCB, serine protease inhibitor TLCK and LaCl3 were inoculated together with P. syringae pv tabaci in detached tobacco leaves or applied simultaneously with fungal toxin FUM in the tomato cell suspension. The results illustrate that cell death in normal Nevrokop 1164 and ttr transgenic tobacco at sites infected with P. syringae pv tabaci is apoptotic-like and caspase-like proteases and serine proteases are involved in lesion formation. The cell death in the lesions was accompanied with enhanced H2O2 accumulation and MDA production in the wild type and with reduced levels of both metabolites in the transgenic line. Lanthanum, caspase inhibitors and TLCK reduced the amount of H2O2 and MDA in the affected lesions. FUM-induced cell death in tomato suspension cells was greatly suppressed by the application of protease inhibitors and lanthanum. The results indicated that apoptotic cell death occurs at bacteria inoculation of tobacco leaves, and in fumonisin treated tomato cells.
Hide ReferencesAdams T.L., Townsend J.A. (1983) Plant Cell
Rep., 2 , 165-168.
Anzai HK, Yoneyama K, Yamaguchi I (1989).
Mol. Gen. Genet., 219 , 492-494.
Asai T., Stone J.M., Heard J.E., Kovtun Y.,
Yorgey P., Sheen J., Ausubel F.M. (2000) Plant
Cell, 12 , 1823-1836.
Atkinson M.M., Baker C. J. (1989) Plant
Physiology, 9 , 298-303.
Atkinson M.M., Midland S.L., Sims J.J.,
Keen N.T. (1996) Plant Physiol., 112 , 297-302.
Atkinson M.M., Keppler L.D., Orland E.-
W., Baker C.J., Mischke C.F. (1990) Plant
Physiol., 92 , 215-221.
Batchvarova R., Nikolaeva V., Slavov S.,
Bossolova S., Valkov V., Atanassova S.,
Guelemerov S., Atanassov A., Anzai H. (1998)
TAG, 97 , 986-989.
Beers F.P., Freeman T.B. (1997) Plant
Physio., 113 , 873-880.
Bethke P.C., Jones R.L. (2001) The Plant
Journal, 25 (1), 19-29.
Bolwell G.P. (1999) Curr. Opin. Plant Biol.,
2 , 287-294.
Cohen G.M. (1997) Biochem. J., 326 , 1-16.
De Gara L., de Pinto M.C., Tommasi F.
(2003) Plant Physiol. and Biochem., 41 , 863-
870.
De Jong A.J., Hoeberichts F.A., Yakimova
E.T., Maximova E., Woltering E.J. (2000).
Planta, 211 , 656-662.
De Jong A.J., Yakimova E.T., Kapchina
V.M., Woltering E.J. (2002) Planta, 214 , 537-
545.
Del Pozo O., Lam E. (1998) Curr. Biol., 8 ,
1129-1132. b. Del Pozo O., Lam E. (2003) Mol.
Plant Microbe Interact., 16 , 485-494.
Dhindsa R.S., Plunb-Dhindsa P., Thorpe
T.A. (1981) J. Exp. Bot., 32 , 93-101.
Dickman M.B., Park Y.K., Oltersdorf T.,
Li W., Clemente T., French R. (2001) Proc.
Natl. Acad. Sci., USA, 98 , 6957-6962.
Drew M.C., He I., Morgan P.W. (2000) BIOS
Scientific Publishers Ltd., Oxford, 183-192.
Ekert P.G., Silke J., Vaux D.L. (1999) Cell
Death Differ., 6 , 1081-1086.
Gelli A., Higgins V.J., Blumwald E. (1997)
Plant Physiol, 113 , 269-279.
Gilchrist D.G. (1998) Ann. Rev. Phytopathol.,
39 , 393-414.
Grant M., Mansfield J. (1999). Curr. Opin.
in Plant Biol., 2 , 312-319.
Greenberg J.T., Guo, A., Klessig, D.F.,
Ausubel, F.M. (1994) Cell, 77 , 551-563.
Groover A., Jones A.M. (1999) Plant Physiol.,
119 , 375-384.
Hansen G. (2000) Mol. Plant Microbe Interact.,
13 , 649-657.
Haliwell B., Gutteridge J. (1990) Methods
Enzymol., 186 , 1-85.
He C.-J., Morgan P.W., Drew M.C. (1996)
Plant Physiol., 112 , 463-472.
He X., Kermode R. (2003) Plant Mol. Biol.,
52 , 729-744.
Heath M.C. (2000) Plant Mol. Biol., 44 , 323-
334.
Heath R.L., Packer L. (1968) Archives in
Biochem. and Biophys., 125 , 189-198.
Heath M.C. (2000) Plant Mol. Biol., 44 , 321-
334.
Hengartner M.O. (2000) Nature, 407 , 770-
776.
Hoeberichts F.A., Woltering E.J. (2003).
BioEssays, 25 , 47-57.
Horsch R.B., Fry J.E., Hoffmann N.L.,
Eichholtz D., Rogers S.G, Fraley R.T. (1985)
Science, 227 , 1229-1231.
Jabs T. (1999) Biochemical Pharmacology,
57 , 231-245.
Jabs T., Tschope M., Colling C., Hhlbrock
K., Scheel D. (1997) Proc. Natl. Acad. Sci. USA
94, 4800-4805.
Kasparovsky, T., Milat, M.-L., Humbert,
C., Blein, J.-P., Havel, L., Mikes, V. (2003) Plant
Physiol. And Biochem., 41 , 495-501.
Kombrich E., Somssich I.E. (1995) Adv.
Bot. Res., 21 , 1-34.
Koonin E.V., Aravind L. (2002) Cell Death
Differ., 9 , 394-404.
Koornneef, M., Hanhart C.J., Martinelli,
L. (1987) Theor. Appl. Gen., 74 , 633-641.
Kramer G., Norman H., Krizek D. and
Mirecki R. (1991) Phytochemistry, 30 , 2101-
2108.
Lam E., Del Pozo O., Pontier D. (1999)
Trends Plant Sc., 4 , 419-42.
Lam E., Pontier D., del Pozo O. (1999) Curr.
Opin. in Plant Biol., 2 , 502-507.
Lamb, C. Dixon, R. A. (1997) Annu. Rev.
Plant Physiol., 48 , 251-275.
Leshem Y. (1987). Physiol Plant, 69 , 551-
560.
Levine A., Pennell R.I., Alvarez M.E.,
Palmer R., Lamb C.J. (1996) Curr. Biol., 6 , 427-
437.
Levine A., Tenhaken R., Dixon R., Lamb
C.J. (1994) Cell, 79 , 583-593.
Madeo F., Herker E., Maldener C., Wissing
S., Lächelt S., Herlan M., Fehr M., Lauber K.,
Sigrist S.J., Wesselborg S., Fröhlich K.U.
(2002) Mol Cell, 9 , 1-20.
Melviya A.N., Rogue P.J. (1998). Cell, 92 ,
17-23.
McCabe P.F., Levine A., Meijer P.-J., Tapon
N.A., Pennel R.I. (1997) The Plant Journal, 12
(2), 267-280.
Mittler, R., Feng, X., Cohen, M. (1998)
Plant Cell, 10 , 461-473.
Moore T., Martineau B., Bostock R.M.,
Lincoln J.E., Gilchrist D.G. (1999). Physiol.
Mol. Plant Path., 54 , 73-85.
Morel, J.-B., Dangl, J.L. (1997) Cell death
and Differentiation, 4 , 671-683.
Nicotera P., Zhivotovsky B., Orrenius S.
(1994) Cell Calcium, 16 , 279-288.
Numberger T., Nennsteil D., Jabs T., Sacks
W.R., Hahlbrock Kand Schell D. (1994) Cell,
78 , 449-460.
Orzaez, D., De Jong, A.J., Woltering E.J.
(2001) Plant Mol. Biol., 46 , 459-468.
Overmyer K., Tuominen H., Kettunen R.,
Betz C., Langebartels C., Sandermann H.,
Kangasjarvi J. (2000) Plant Cell, 12 , 1849-1862.
Pasqualini, S., Piccioni, C., Reale, L.,
Ederli, L., Della Torre, G., Ferranti, F. (2003)
Plant Physiol., 133 , 1122-1134.
Peng J.-L., Dong H.-S., Dong H.-P.,
Delaney, T.P., Bomasera J.M., Beer S.V. (2003)
Physiol. And Mol. Plant Pathol., 62 , 317-326.
Richael C., Lincoln J.E., Bostock R.M.,
Gilchrist D.G. (2001) Physiol. And Mol. Plant
Pathol., 59 , 213-221.
Sarath G., de la Motte R., Wagner F. (1990)
Protease assay methods In: Proteolystic enzymes
– a Practical approach ( R. J. Beynon and
J. S. Bond, Eds.), IRI Press, Tokyo.
Schwacke R., Hager A. (1992) Planta, 187 ,
136-141.
Shirasu K., Shulze-Lefert P. (2000) Plant
Mol. Biol., 44 , 371-385.
Spencer M., Ryu Ch.-M., Yang K.-Y., Kim,
Y.Ch., Kloepper J.W., Anderson A.J. (2003)
Physiol. And Mol. Plant Pathol., 63 , 27-34.
Suh, M. Ch., Oh S.-K., Kim, Y.-Ch., Pai,
H.-S., Choi, D. (2003). Physiol. and Mol. Plant
Pathol., 62 , 227-235.
Szallies A., Kubata B.K., Duszenko M.
(2002) FEBS Lett., 517 ,144-150.
Uren A.G., O’Rourke K., Aravind L.,
Pisabarro M.T., Seshagiri S., Koonin E.V.,
Dixit V.M. (2000) Mol. Cell, 6 , 961-967.
Vranova E., Inze D., Van Breusegem F.
(2002) J. Exp. Botany, 53 (372), 1227-1236.
Wang H., Jones C., Ciacci-Zanella J., Holt
T., Gilchrist D.G., Dickman M.B. (1996) Proc
Natl. Acad. Sci. USA 93 , 3461-3465.
Woltering E.J., de Jong, A.J., Iakimova E.,
Kapchina V.M., Hoeberichts F.A. (2003) In:
Biology and Biotechnology of the Plant
Hormone Ethylene III (Eds. Vendrell et al.) IOS
Press, pp.315-323.
Woltering E.J., van der Bent A., Hoeberichts
F.A. (2002) Plant Physiol., 130 , 1764-
1769.
Xu F.-X., Chye M.-L. (1999) The Plant
Journal, 17 (3), 321-327.
Xu H.,Heath M.C. (1998) Plant Cell, 10 , 585-
597.
Yu T.C., Parker J., Bent A.F. (1998) Proc.
Natl. Acad. Sci., U.S.A., 95 , 7819-8724.