First published online October 9, 2003; 10.1104/pp.103.030379
Plant Physiology 133:1181-1189 (2003)
© 2003 American Society of Plant Biologists
DEVELOPMENT AND HORMONE ACTION
Multiple Hormones Act Sequentially to Mediate a Susceptible Tomato Pathogen Defense Response1
Philip J. O'Donnell,
Eric Schmelz,
Anna Block,
Otto Miersch,
Claus Wasternack,
Jeffrey B. Jones and
Harry J. Klee*
Department of Horticultural Sciences (P.J.O., A.B., H.J.K.) and Department of Plant Pathology (J.B.J.), University of Florida, Gainesville, Florida 32611; United States Department of Agriculture-Agricultural Research Service, Center for Medical Agricultural and Veterinary Entomology, 1700 SW 23 Drive, Gainesville, Florida 32608 (E.S.); and Institute of Plant Biochemistry, D–06018 Halle, Germany (O.M., C.W.)
Phytohormones regulate plant responses to a wide range of biotic and abiotic stresses. How a limited number of hormones differentially mediate individual stress responses is not understood. We have used one such response, the compatible interaction of tomato (Lycopersicon esculentum) and Xanthomonas campestris pv vesicatoria (Xcv), to examine the interactions of jasmonic acid (JA), ethylene, and salicylic acid (SA). The role of JA was assessed using an antisense allene oxide cyclase transgenic line and the def1 mutant to suppress Xcv-induced biosynthesis of jasmonates. Xcv growth was limited in these lines as was subsequent disease symptom development. No increase in JA was detected before the onset of terminal necrosis. The lack of a detectable increase in JA may indicate that an oxylipin other than JA regulates basal resistance and symptom proliferation. Alternatively, there may be an increase in sensitivity to JA or related compounds following infection. Hormone measurements showed that the oxylipin signal must precede subsequent increases in ethylene and SA accumulation. Tomato thus actively regulates the Xcv-induced disease response via the sequential action of at least three hormones, promoting expansive cell death of its own tissue. This sequential action of jasmonate, ethylene, and SA in disease symptom development is different from the hormone interactions observed in many other plant-pathogen interactions.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.030379.
1 This work was supported by the National Science Foundation (grant no. IBN–0091064 to H.K.), by the Deutsche Forschunggemeinschaft (project C5 of the SFB363 to C.W. and O.M.), and in part by the Florida Agricultural Experiment Station. This is Florida Agricultural Experiment Station journal series number R-09718.
* Corresponding author; e-mail hjklee{at}ifas.ufl.edu; fax 352–846–2063.
Received July 18, 2003;
returned for revision July 30, 2003;
accepted August 7, 2003.
This article has been cited by other articles:
|
|
|
|
 
H. Wuriyanghan, B. Zhang, W.-H. Cao, B. Ma, G. Lei, Y.-F. Liu, W. Wei, H.-J. Wu, L.-J. Chen, H.-W. Chen, et al.
The Ethylene Receptor ETR2 Delays Floral Transition and Affects Starch Accumulation in Rice
PLANT CELL,
May 1, 2009;
21(5):
1473 - 1494.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-G. Kim, K. W. Taylor, A. Hotson, M. Keegan, E. A. Schmelz, and M. B. Mudgett
XopD SUMO Protease Affects Host Transcription, Promotes Pathogen Growth, and Delays Symptom Development in Xanthomonas-Infected Tomato Leaves
PLANT CELL,
July 1, 2008;
20(7):
1915 - 1929.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Balaji, M. Mayrose, O. Sherf, J. Jacob-Hirsch, R. Eichenlaub, N. Iraki, S. Manulis-Sasson, G. Rechavi, I. Barash, and G. Sessa
Tomato Transcriptional Changes in Response to Clavibacter michiganensis subsp. michiganensis Reveal a Role for Ethylene in Disease Development
Plant Physiology,
April 1, 2008;
146(4):
1797 - 1809.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Mosblech, S. Konig, I. Stenzel, P. Grzeganek, I. Feussner, and I. Heilmann
Phosphoinositide and Inositolpolyphosphate Signalling in Defense Responses of Arabidopsis thaliana Challenged by Mechanical Wounding
Mol Plant,
March 1, 2008;
1(2):
249 - 261.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Schmelz, S. LeClere, M. J. Carroll, H. T. Alborn, and P. E.A. Teal
Cowpea Chloroplastic ATP Synthase Is the Source of Multiple Plant Defense Elicitors during Insect Herbivory
Plant Physiology,
June 1, 2007;
144(2):
793 - 805.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. A.T. Adie, J. Perez-Perez, M. M. Perez-Perez, M. Godoy, J.-J. Sanchez-Serrano, E. A. Schmelz, and R. Solano
ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis
PLANT CELL,
May 1, 2007;
19(5):
1665 - 1681.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. F. Bent, T. K. Hoffman, J. S. Schmidt, G. L. Hartman, D. D. Hoffman, P. Xue, and M. L. Tucker
Disease- and Performance-Related Traits of Ethylene-Insensitive Soybean
Crop Sci.,
February 24, 2006;
46(2):
893 - 901.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A.J. Mur, P. Kenton, R. Atzorn, O. Miersch, and C. Wasternack
The Outcomes of Concentration-Specific Interactions between Salicylate and Jasmonate Signaling Include Synergy, Antagonism, and Oxidative Stress Leading to Cell Death
Plant Physiology,
January 1, 2006;
140(1):
249 - 262.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Block, E. Schmelz, P. J. O'Donnell, J. B. Jones, and H. J. Klee
Systemic Acquired Tolerance to Virulent Bacterial Pathogens in Tomato
Plant Physiology,
July 1, 2005;
138(3):
1481 - 1490.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y.-F. CHEN, N. ETHERIDGE, and G. E. SCHALLER
Ethylene Signal Transduction
Ann. Bot.,
May 1, 2005;
95(6):
901 - 915.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Mayrose, A. Bonshtien, and G. Sessa
LeMPK3 Is a Mitogen-activated Protein Kinase with Dual Specificity Induced during Tomato Defense and Wounding Responses
J. Biol. Chem.,
April 9, 2004;
279(15):
14819 - 14827.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
