|
THE PLANT CELL, Vol 8, Issue 11 2067-2077, Copyright © 1996 by American Society of Plant Biologists
An Octadecanoid Pathway Mutant (JL5) of Tomato Is Compromised in Signaling for Defense against Insect Attack
G. A. Howe, J. Lightner, J. Browse and C. A. Ryan
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164-6340
The activation of defense genes in tomato plants has been shown to be
mediated by an octadecanoic acid-based signaling pathway in response to
herbivore attack or other mechanical wounding. We report here that a tomato
mutant (JL5) deficient in the activation of wound-inducible defense genes
is also compromised in resistance toward the lepidopteran predator Manduca
sexta (tobacco hornworm). Thus, we propose the name defenseless1 (def1) for
the mutation in the JL5 line that mediates this altered defense response.
In experiments designed to define the normal function of DEF1, we found
that def1 plants are defective in defense gene signaling initiated by
prosystemin overexpression in transgenic plants as well as by
oligosaccharide (chitosan and polygalacturonide) and polypeptide (systemin)
elicitors. Supplementation of plants through their cut stems with
intermediates of the octadecanoid pathway indicates that def1 plants are
affected in octadecanoid metabolism between the synthesis of
hydroperoxylinolenic acid and 12-oxo-phytodienoic acid. Consistent with
this defect, def1 plants are also compromised in their ability to
accumulate jasmonic acid, the end product of the pathway, in response to
wounding and the aforementioned elicitors. Taken together, these results
show that octadecanoid metabolism plays an essential role in the
transduction of upstream wound signals to the activation of antiherbivore
plant defenses.
This article has been cited by other articles:

|
 |

|
 |
 
R. Liechti and E. E. Farmer
Jasmonate Biochemical Pathway
Sci. Signal.,
September 2, 2008;
1(35):
cm3 - cm3.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. AbuQamar, M.-F. Chai, H. Luo, F. Song, and T. Mengiste
Tomato Protein Kinase 1b Mediates Signaling of Plant Responses to Necrotrophic Fungi and Insect Herbivory
PLANT CELL,
July 1, 2008;
20(7):
1964 - 1983.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Browse and G. A. Howe
New Weapons and a Rapid Response against Insect Attack
Plant Physiology,
March 1, 2008;
146(3):
832 - 838.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Erb, J. Ton, J. Degenhardt, and T. C.J. Turlings
Interactions between Arthropod-Induced Aboveground and Belowground Defenses in Plants
Plant Physiology,
March 1, 2008;
146(3):
867 - 874.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. B. Runyon, M. C. Mescher, and C. M. De Moraes
Parasitism by Cuscuta pentagona Attenuates Host Plant Defenses against Insect Herbivores
Plant Physiology,
March 1, 2008;
146(3):
987 - 995.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L.-L. Gao, J. P. Klingler, J. P. Anderson, O. R. Edwards, and K. B. Singh
Characterization of Pea Aphid Resistance in Medicago truncatula
Plant Physiology,
March 1, 2008;
146(3):
996 - 1009.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Kavroulakis, S. Ntougias, G. I. Zervakis, C. Ehaliotis, K. Haralampidis, and K. K. Papadopoulou
Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain
J. Exp. Bot.,
November 29, 2007;
(2007)
erm230v1.
[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]
|
 |
|

|
 |

|
 |
 
M. De Vos, W. Van Zaanen, A. Koornneef, J. P. Korzelius, M. Dicke, L.C. Van Loon, and C. M.J. Pieterse
Herbivore-Induced Resistance against Microbial Pathogens in Arabidopsis
Plant Physiology,
September 1, 2006;
142(1):
352 - 363.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Li, J. Zhao, H. Jiang, X. Wu, J. Sun, C. Zhang, X. Wang, Y. Lou, and C. Li
The Wound Response Mutant suppressor of prosystemin-mediated responses6 (spr6) is a Weak Allele of the Tomato Homolog of CORONATINE-INSENSITIVE1 (COI1)
Plant Cell Physiol.,
May 1, 2006;
47(5):
653 - 663.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Liechti and E. E. Farmer
Jasmonate Biochemical Pathway
Sci. Signal.,
February 14, 2006;
2006(322):
cm3 - cm3.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Reymond, N. Bodenhausen, R. M.P. Van Poecke, V. Krishnamurthy, M. Dicke, and E. E. Farmer
A Conserved Transcript Pattern in Response to a Specialist and a Generalist Herbivore
PLANT CELL,
November 1, 2004;
16(11):
3132 - 3147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ament, M. R. Kant, M. W. Sabelis, M. A. Haring, and R. C. Schuurink
Jasmonic Acid Is a Key Regulator of Spider Mite-Induced Volatile Terpenoid and Methyl Salicylate Emission in Tomato
Plant Physiology,
August 1, 2004;
135(4):
2025 - 2037.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Boter, O. Ruiz-Rivero, A. Abdeen, and S. Prat
Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis
Genes & Dev.,
July 1, 2004;
18(13):
1577 - 1591.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Thaler, B. Owen, and V. J. Higgins
The Role of the Jasmonate Response in Plant Susceptibility to Diverse Pathogens with a Range of Lifestyles
Plant Physiology,
May 1, 2004;
135(1):
530 - 538.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Takahashi, K. Kasai, and K. Ochi
Identification of the bacterial alarmone guanosine 5'-diphosphate 3'-diphosphate (ppGpp) in plants
PNAS,
March 23, 2004;
101(12):
4320 - 4324.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Zavala, A. G. Patankar, K. Gase, D. Hui, and I. T. Baldwin
Manipulation of Endogenous Trypsin Proteinase Inhibitor Production in Nicotiana attenuata Demonstrates Their Function as Antiherbivore Defenses
Plant Physiology,
March 1, 2004;
134(3):
1181 - 1190.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. O'Donnell, E. Schmelz, A. Block, O. Miersch, C. Wasternack, J. B. Jones, and H. J. Klee
Multiple Hormones Act Sequentially to Mediate a Susceptible Tomato Pathogen Defense Response
Plant Physiology,
November 1, 2003;
133(3):
1181 - 1189.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Orozco-Cardenas and C. A. Ryan
Polygalacturonase {beta}-Subunit Antisense Gene Expression in Tomato Plants Leads to a Progressive Enhanced Wound Response and Necrosis in Leaves and Abscission of Developing Flowers
Plant Physiology,
October 1, 2003;
133(2):
693 - 701.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. DEVOTO and J. G. TURNER
Regulation of Jasmonate-mediated Plant Responses in Arabidopsis
Ann. Bot.,
September 1, 2003;
92(3):
329 - 337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-T. Wu and K. J. Bradford
Class I Chitinase and {beta}-1,3-Glucanase Are Differentially Regulated by Wounding, Methyl Jasmonate, Ethylene, and Gibberellin in Tomato Seeds and Leaves
Plant Physiology,
September 1, 2003;
133(1):
263 - 273.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. R. Holley, R. D. Yalamanchili, D. S. Moura, C. A. Ryan, and J. W. Stratmann
Convergence of Signaling Pathways Induced by Systemin, Oligosaccharide Elicitors, and Ultraviolet-B Radiation at the Level of Mitogen-Activated Protein Kinases in Lycopersicon peruvianum Suspension-Cultured Cells
Plant Physiology,
August 1, 2003;
132(4):
1728 - 1738.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. E. Dombrowski
Salt Stress Activation of Wound-Related Genes in Tomato Plants
Plant Physiology,
August 1, 2003;
132(4):
2098 - 2107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Li, G. Liu, C. Xu, G. I. Lee, P. Bauer, H.-Q. Ling, M. W. Ganal, and G. A. Howe
The Tomato Suppressor of prosystemin-mediated responses2 Gene Encodes a Fatty Acid Desaturase Required for the Biosynthesis of Jasmonic Acid and the Production of a Systemic Wound Signal for Defense Gene Expression
PLANT CELL,
July 1, 2003;
15(7):
1646 - 1661.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. H. Spoel, A. Koornneef, S. M. C. Claessens, J. P. Korzelius, J. A. Van Pelt, M. J. Mueller, A. J. Buchala, J.-P. Metraux, R. Brown, K. Kazan, et al.
NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol
PLANT CELL,
March 1, 2003;
15(3):
760 - 770.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Li, M. M. Williams, Y.-T. Loh, G. I. Lee, and G. A. Howe
Resistance of Cultivated Tomato to Cell Content-Feeding Herbivores Is Regulated by the Octadecanoid-Signaling Pathway
Plant Physiology,
September 1, 2002;
130(1):
494 - 503.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Yalamanchili and J. W. Stratmann
Ultraviolet-B Activates Components of the Systemin Signaling Pathway in Lycopersicon peruvianum Suspension-cultured Cells
J. Biol. Chem.,
August 2, 2002;
277(32):
28424 - 28430.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Xu, F. Liu, E. Lechner, P. Genschik, W. L. Crosby, H. Ma, W. Peng, D. Huang, and D. Xie
The SCFCOI1 Ubiquitin-Ligase Complexes Are Required for Jasmonate Response in Arabidopsis
PLANT CELL,
August 1, 2002;
14(8):
1919 - 1935.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Diaz, A. ten Have, and J. A.L. van Kan
The Role of Ethylene and Wound Signaling in Resistance of Tomato to Botrytis cinerea
Plant Physiology,
July 1, 2002;
129(3):
1341 - 1351.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Cui, G. Jander, L. R. Racki, P. D. Kim, N. E. Pierce, and F. M. Ausubel
Signals Involved in Arabidopsis Resistance to Trichoplusia ni Caterpillars Induced by Virulent and Avirulent Strains of the Phytopathogen Pseudomonas syringae
Plant Physiology,
June 1, 2002;
129(2):
551 - 564.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. G. Turner, C. Ellis, and A. Devoto
The Jasmonate Signal Pathway
PLANT CELL,
May 1, 2002;
14(90001):
S153 - 164.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Li, C. Li, G. I. Lee, and G. A. Howe
Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato
PNAS,
April 30, 2002;
99(9):
6416 - 6421.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Audenaert, G. B. De Meyer, and M. M. Hofte
Abscisic Acid Determines Basal Susceptibility of Tomato to Botrytis cinerea and Suppresses Salicylic Acid-Dependent Signaling Mechanisms
Plant Physiology,
February 1, 2002;
128(2):
491 - 501.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Li, C. Li, and G. A. Howe
Genetic Analysis of Wound Signaling in Tomato. Evidence for a Dual Role of Jasmonic Acid in Defense and Female Fertility
Plant Physiology,
December 1, 2001;
127(4):
1414 - 1417.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. R. Jaglo, S. Kleff, K. L. Amundsen, X. Zhang, V. Haake, J. Z. Zhang, T. Deits, and M. F. Thomashow
Components of the Arabidopsis C-Repeat/Dehydration-Responsive Element Binding Factor Cold-Response Pathway Are Conserved in Brassica napus and Other Plant Species
Plant Physiology,
November 1, 2001;
127(3):
910 - 917.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Howe
Cyclopentenone signals for plant defense: Remodeling the jasmonic acid response
PNAS,
October 23, 2001;
98(22):
12317 - 12319.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Stintzi, H. Weber, P. Reymond, J. Browse, and E. E. Farmer
Plant defense in the absence of jasmonic acid: The role of cyclopentenones
PNAS,
October 5, 2001;
(2001)
211311098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. S. Moura and C. A. Ryan
Wound-Inducible Proteinase Inhibitors in Pepper. Differential Regulation upon Wounding, Systemin, and Methyl Jasmonate
Plant Physiology,
May 1, 2001;
126(1):
289 - 298.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. A. Winz and I. T. Baldwin
Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. IV. Insect-Induced Ethylene Reduces Jasmonate-Induced Nicotine Accumulation by Regulating Putrescine N-Methyltransferase Transcripts
Plant Physiology,
April 1, 2001;
125(4):
2189 - 2202.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. Hermsmeier, U. Schittko, and I. T. Baldwin
Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. I. Large-Scale Changes in the Accumulation of Growth- and Defense-Related Plant mRNAs
Plant Physiology,
February 1, 2001;
125(2):
683 - 700.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
F. Schaller
Enzymes of the biosynthesis of octadecanoid-derived signalling molecules
J. Exp. Bot.,
January 1, 2001;
52(354):
11 - 23.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. U. Stotz, B. R. Pittendrigh, J. Kroymann, K. Weniger, J. Fritsche, A. Bauke, and T. Mitchell-Olds
Induced Plant Defense Responses against Chewing Insects. Ethylene Signaling Reduces Resistance of Arabidopsis against Egyptian Cotton Worm But Not Diamondback Moth
Plant Physiology,
November 1, 2000;
124(3):
1007 - 1018.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
A. Stintzi and J. Browse
The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis
PNAS,
September 5, 2000;
(2000)
190264497.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
C. P. Constabel, L. Yip, J. J. Patton, and M. E. Christopher
Polyphenol Oxidase from Hybrid Poplar. Cloning and Expression in Response to Wounding and Herbivory
Plant Physiology,
September 1, 2000;
124(1):
285 - 296.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. Stratmann, J. Scheer, and C. A. Ryan
Suramin inhibits initiation of defense signaling by systemin, chitosan, and a beta -glucan elicitor in suspension-cultured Lycopersicon peruvianum cells
PNAS,
August 1, 2000;
97(16):
8862 - 8867.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Shoji, Y. Yamada, and T. Hashimoto
Jasmonate Induction of Putrescine N-Methyltransferase Genes in the Root of Nicotiana sylvestris
Plant Cell Physiol.,
July 1, 2000;
41(7):
831 - 839.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. M. Sanders, P. Y. Lee, C. Biesgen, J. D. Boone, T. P. Beals, E. W. Weiler, and R. B. Goldberg
The Arabidopsis DELAYED DEHISCENCE1 Gene Encodes an Enzyme in the Jasmonic Acid Synthesis Pathway
PLANT CELL,
July 1, 2000;
12(7):
1041 - 1062.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
G. A. Howe, G. I. Lee, A. Itoh, L. Li, and A. E. DeRocher
Cytochrome P450-Dependent Metabolism of Oxylipins in Tomato. Cloning and Expression of Allene Oxide Synthase and Fatty Acid Hydroperoxide Lyase
Plant Physiology,
June 1, 2000;
123(2):
711 - 724.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
P. Reymond, H. Weber, M. Damond, and E. E. Farmer
Differential Gene Expression in Response to Mechanical Wounding and Insect Feeding in Arabidopsis
PLANT CELL,
May 1, 2000;
12(5):
707 - 720.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. Kramell, O. Miersch, R. Atzorn, B. Parthier, and C. Wasternack
Octadecanoid-Derived Alteration of Gene Expression and the "Oxylipin Signature" in Stressed Barley Leaves. Implications for Different Signaling Pathways
Plant Physiology,
May 1, 2000;
123(1):
177 - 188.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. Sivasankar, B. Sheldrick, and S. J. Rothstein
Expression of Allene Oxide Synthase Determines Defense Gene Activation in Tomato
Plant Physiology,
April 1, 2000;
122(4):
1335 - 1342.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
G. A. Howe and C. A. Ryan
Suppressors of Systemin Signaling Identify Genes in the Tomato Wound Response Pathway
Genetics,
November 1, 1999;
153(3):
1411 - 1421.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. Narváez-Vásquez, J. Florin-Christensen, and C. A. Ryan
Positional Specificity of a Phospholipase A Activity Induced by Wounding, Systemin, and Oligosaccharide Elicitors in Tomato Leaves
PLANT CELL,
November 1, 1999;
11(11):
2249 - 2260.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. E. Dombrowski, G. Pearce, and C. A. Ryan
Proteinase inhibitor-inducing activity of the prohormone prosystemin resides exclusively in the C-terminal systemin domain
PNAS,
October 26, 1999;
96(22):
12947 - 12952.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Harsulkar, A. P. Giri, A. G. Patankar, V. S. Gupta, M. N. Sainani, P. K. Ranjekar, and V. V. Deshpande
Successive Use of Non-Host Plant Proteinase Inhibitors Required for Effective Inhibition of Helicoverpa armigera Gut Proteinases and Larval Growth
Plant Physiology,
October 1, 1999;
121(2):
497 - 506.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
M. Orozco-Cardenas and C. A. Ryan
Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway
PNAS,
May 25, 1999;
96(11):
6553 - 6557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Royo, J. Leon, G. Vancanneyt, J. P. Albar, S. Rosahl, F. Ortego, P. Castanera, and J. J. Sanchez-Serrano
Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests
PNAS,
February 2, 1999;
96(3):
1146 - 1151.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. T. Baldwin
Jasmonate-induced responses are costly but benefit plants under attack in native populations
PNAS,
July 7, 1998;
95(14):
8113 - 8118.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Vijayan, J. Shockey, C. A. Levesque, R. J. Cook, and J. Browse
A role for jasmonate in pathogen defense of Arabidopsis
PNAS,
June 9, 1998;
95(12):
7209 - 7214.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|