Abstract
Jasmonates, such as jasmonic acid (JA), are plant-signaling compounds that trigger induced resistance against certain pathogens and a broad range of arthropod herbivores. One goal of this study was to determine the effects of JA-dependent defenses in tomato on root-knot nematodes. Another was to determine if the artificial induction of these defenses could enhance nematode control on plants that carry Mi-1.2, a nematode resistance gene that is present in many tomato cultivars. At moderate soil temperatures, Mi-1.2 can effectively suppress reproduction of most isolates of the common root-knot nematode species Meloidogyne javanica, M. incognita, and M. arenaria. Mi-mediated resistance has its limitations, however. Mi-1.2 is reported to lose its effectiveness at soil temperatures above 28°C, and certain virulent nematode isolates can overcome resistance even at moderate soil temperatures. This study used a foliar application of JA to activate induced resistance in two near-isogenic lines of tomato (Lycopersicon esculentum) with and without Mi-1.2, and evaluated the effects of induced resistance at moderate soil temperatures on one avirulent nematode isolate (M. javanica isolate VW4) and two virulent isolates (M. javanica isolate VW5 and M. incognita isolate 557R). In addition, the effects of induced resistance on avirulent nematode performance were examined at a high temperature (32°C). The results indicate that JA application induces a systemic defense response that reduces avirulent nematode reproduction on susceptible tomato plants. Furthermore, JA-dependent defenses proved to be heat-stable, whereas the effects of Mi-mediated resistance were reduced but not eliminated at 32°C. JA treatment enhanced Mi-mediated resistance at high temperature, but did not suppress either of the virulent nematode isolates tested.
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References
M. T. Araujo M. J. Bassett J. J. Augustine D. W. Dickson (1982) ArticleTitleEffect of diurnal changes in soil temperatures on resistance to Meloidogyne incognita in tomato J. Nematol. 14 414–416
H. J. Atkinson P. E. Urwin M. C. Clarke M. J. McPherson (1996) ArticleTitleImage analysis of the growth of Globodera pallida and Meloidogyne incognita on transgenic tomato roots expression cystatins J. Nematol. 28 209–215
H. J. Atkinson P. E. Urwin M. J. McPherson (2003) ArticleTitleEngineering plants for nematode resistance Annu. Rev. Phytopathol. 41 615–639 Occurrence Handle10.1146/annurev.phyto.41.052002.095737 Occurrence Handle12730388
K. L. Bajaj P. Singh R. Mahajan (1985) ArticleTitleChanges induced by Meloidogyne incognita in superoxide dismutase, peroxidase and polyphenol oxidase activity in tomato roots Biochem. Physiol. Pflanzen 180 543–546
I. T. Baldwin E. A. Schmelz T. E. Ohnmeiss (1994) ArticleTitleWound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana-sylvestris Spegazzini and Comes J. Chem. Ecol. 20 2139–2157 Occurrence Handle10.1007/BF02066250
M. A. Botella Y. Xu T. N. Prabha Y. Zhao M. L. Narasimhan K. A. Wilson S. S. Nielsen R. A. Bressan P. M. Hasegawa (1996) ArticleTitleDifferential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate Plant Physiol 112 1201–1210 Occurrence Handle10.1104/pp.112.3.1201 Occurrence Handle8938418
C. Branch C. F. Hwang D. A. Navarre V. M. Williamson (2004) ArticleTitleSalicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato Mol. Plant Microb. Interact. 17 351–356
C. R. Brown H. Mojtahedi G. S. Santo V. M. Williamson (1997) ArticleTitleEffect of the Mi gene in tomato on reproductive factors of Meloidogyne chitwoodi and M. hapla J. Nematol. 29 416–419
T. J. Bruce J. L. Martin J. A. Picket B. J. Pye L. E. Smart L. J. Wadhams (2003) ArticleTitleCis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae) Pest Manag. Sci. 59 1031–1036 Occurrence Handle10.1002/ps.730 Occurrence Handle12974355
C. M. Brueske (1980) ArticleTitlePhenylalanine ammonia lyase activity in tomato roots infected and resistant to the root-knot nematode Meloidogyne incognita Physiol. Plant Pathol. 16 409–414
P. Castagnone-Sereno (2002) ArticleTitleGenetic variability in parthenogenetic root-knot nematodes, Meloidogyne spp., and their ability to overcome plant resistance genes Nematology 4 605–608 Occurrence Handle10.1163/15685410260438872
P. Castagnone-Sereno M. Bongiovanni C. Djian-Caporalino (2001) ArticleTitleNew data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepper Plant Breed. 120 429–433 Occurrence Handle10.1046/j.1439-0523.2001.00637.x
Cooper, W. R. and Goggin, F. L. 2005. Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomol. Exp. Appl. 115:107–115.
W. R. Cooper L. Jia F. L. Goggin (2004) ArticleTitleAcquired and R-gene mediated aphid resistance in tomato J. Chem. Ecol. 30 2527–2542 Occurrence Handle10.1007/s10886-004-7948-9 Occurrence Handle15724969
C. Dammann E. Rojo J. J. Sanchez serrano (1997) ArticleTitleAbscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathways Plant J. 11 773–782 Occurrence Handle10.1046/j.1365-313X.1997.11040773.x Occurrence Handle9161035
E. L. Davis J. R. Rich (1987) ArticleTitleNicotine content of tobacco roots and toxicity to Meloidogyne incognita J. Nematol. 19 23–29
Doares, S. H., Narvaez-Vasquez, J., Conconi, A., and Ryan, C. A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108:1741–1746.
V. H. Dropkin (1969) ArticleTitleThe necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature Phytopathology 59 1632–1637
C. Ellis L. Karafyllidis J. G. Turner (2002) ArticleTitleConstitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae Mol. Plant Microb. Interact. 15 1025–1030
E. Farmer E. Johnson C. A. Ryan (1992) ArticleTitleRegulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid Plant Physiol. 98 995–1002
H. H. Flor (1955) ArticleTitleHost parasite interactions in flax rust—its genetic and other implications Phytopathology 45 680–685
K. A. Gomez A. A. Gomez (1984) Statistical Procedures for Agricultural Research Wiley-Interscience New York, NY
S. A. Haroon A. A. Baki R. N. Huettel (1993) ArticleTitleAn in vitro test for temperature sensitivity and resistance to Meloidogyne incognita in tomato J. Nematol. 25 83–88
O. Holtzman (1965) ArticleTitleEffects of soil temperature on resistance of tomato to root-knot nematode (Meloidogyne incognita) Phytopathology 55 990–992
G. A. Howe J. Lightner J. Browse C. A. Ryan (1996) ArticleTitleAn octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack Plant Cell 8 2067–2077 Occurrence Handle10.1105/tpc.8.11.2067 Occurrence Handle8953771
R. S. Hussey K. H. Barker (1973) ArticleTitleA comparison of methods of collecting inocula of Meloidogyne spp., including a new technique Plant Dis. Rep. 57 1025–1028
R. Karban I. T. Baldwin (1997) Induced Responses to Herbivory University of Chicago Press Chicago, IL
K. N. Lambert E. C. Tedford E. P. Caswell V. M. Williamson (1992) ArticleTitleA system for continuous production of root-knot nematode juveniles in hydroponic culture Phytopathology 82 512–515
K. N. Lambert B. J. Ferrie G. Nombela E. D. Brenner V. M. Williamson (1999) ArticleTitleIdentification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection Physiol. Plant Pathol. 55 341–348 Occurrence Handle10.1006/pmpp.1999.0239
C. Li M. M. Williams Y.-T. Loh G. I. Lee G. A. Howe (2002) ArticleTitleResistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway Plant Physiol. 130 494–503 Occurrence Handle10.1104/pp.005314 Occurrence Handle12226528
J. C. Mader (1999) ArticleTitleEffects of jasmonic acid, silver nitrate and L-AOPP on the distribution of free and conjugated polyamines in roots and shoots of Solanum tuberosum in vitro J. Plant Physiol. 154 79–88
M. McConn R. A. Creelman E. Bell J. E. Mullet J. Browse (1997) ArticleTitleJasmonate is essential for insect defense in Arabidopsis Proc. Natl. Acad. Sci. USA 94 5473–5477 Occurrence Handle10.1073/pnas.94.10.5473 Occurrence Handle11038546
H. Medina-Filho S. D. Tanksley (1983) Breeding for nematode resistance W. R. Sharp D. A. Evans P. V. Ammirato Y. Yamada (Eds) Handbook of Plant Cell Culture, Vol. 1 MacMillan Publishers New York, NY 904–923
H. Melakeberhan (1998) ArticleTitleEffects of temperature and nitrogen source on tomato genotypes response to Meloidogyne incognita infection Fundam. Appl. Nematol. 21 25–32
S. B. Milligan J. Bodeau J. Yaghoobi I. Kaloshian P. Zabel V. M. Williamson (1998) ArticleTitleThe root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine rich repeat family of plant genes Plant Cell 10 1307–1319 Occurrence Handle10.1105/tpc.10.8.1307 Occurrence Handle9707531
J. W. Noling (2002) Nematode management in commercial vegetable crops. Institute of Food and Agricultural Sciences document ENY-14, Florida Cooperative Extension Service University of Florida Gainesville, FL
G. Nombela V. M. Williamson M. Muniz (2003) ArticleTitleThe root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci Mol. Plant–Microb. Interact. 16 645–649
Y. Oka Y. Cohen (2001) ArticleTitleInduced resistance to cyst and root-knot nematodes in cereals by DL-B-amino-n-butyric acid Eur. J. Plant Pathol. 107 219–227 Occurrence Handle10.1023/A:1011278717976
A. D. Omer J. Granett R. Karban E. M. Villa (2001) ArticleTitleChemically-induced resistance against multiple pests in cotton Int. J. Pest Manag. 47 49–54 Occurrence Handle10.1080/09670870150215595
A. D. Omer J. S. Thaler J. Granett R. Karban (2000) ArticleTitleJasmonic acid induced resistance in grapevines to a root and leaf feeder J. Econ. Entomol. 93 840–845 Occurrence Handle10902339
R. E. Paulson J. M. Webster (1972) ArticleTitleUltra structure of the hypersensitive reaction in roots of tomato, Lycopersicon esculentum L., to infection by the root-knot nematode, Meloidogyne incognita Physiol. Plant Pathol. 2 227–234
Pena-Cortes, H., Albrecht, T., Weiler, E. W., and Willlmitzer, L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128.
R. D. Riggs N. N. Winstead (1959) ArticleTitleStudies on resistance in tomato to root-knot nematodes and on occurrence of pathogenic biotypes Phytopathology 49 716–724
M. Rossi F. L. Goggin S. B. Milligan I. Kaloshian D. E. Ullman V. M. Williamson (1998) ArticleTitleThe nematode resistance gene Mi of tomato confers resistance against the potato aphid Proc. Natl. Acad. Sci. USA 95 9750–9754 Occurrence Handle10.1073/pnas.95.17.9750 Occurrence Handle9707547
C. A. Ryan (2000) ArticleTitleThe systemin signaling pathway: Differential activation of plant defense genes Biochim. Biophys. Acta 1477 112–121 Occurrence Handle10708853
I. R. Soriano I. T. Riley M. J. Potter W. S. Bowers (2004a) ArticleTitlePhytoecdysteroids: A novel defense against plant-parasitic nematodes J. Chem. Ecol. 30 1885–1899 Occurrence Handle10.1023/B:JOEC.0000045584.56515.11
I. R. Soriano R. E. Asenstorfer O. Schmidt I. T. Riley (2004) ArticleTitleInducible flavone in oats(Avena sativa) is a novel defense against plant-parasitic nematodes Phytopathology 94 1207–1214
P. E. Staswick G. Y. Yuen C. C. Lehman (1998) ArticleTitleJasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare Plant J. 15 747–754 Occurrence Handle10.1046/j.1365-313X.1998.00265.x Occurrence Handle9807813
F. L. W. Takken M. H. A. J. Joosten (2000) ArticleTitlePlant resistance genes: their structure, function, and evolution Eur. J. Plant Pathol. 106 699–713 Occurrence Handle10.1023/A:1026571130477
J. S. Thaler (1999) ArticleTitleInduced resistance in agricultural crops: Effects of jasmonic acid on herbivory and yield in tomato plants Environ. Entomol. 99 30–37
J. S. Thaler M. J. Stout R. Karban S. S. Duffey (1996) ArticleTitleExogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field J. Chem. Ecol. 22 1767–1781 Occurrence Handle10.1007/BF02028503
J. S. Thaler A. L. Fidantsef S. S. Duffey R. M. Bostock (1999) ArticleTitleTrade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistance J. Chem. Ecol. 25 1597–1609 Occurrence Handle10.1023/A:1020840900595
J. S. Thaler B. Owen V. J. Higgins (2004) ArticleTitleThe role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles Plant Physiol. 135 530–538 Occurrence Handle10.1104/pp.104.041566 Occurrence Handle15133157
P. Tung T. S. Hooker P. A. Tampe D. M. Reid T. A. Thorpe (1996) ArticleTitleEffects on growth and development of isolated tomato roots cultured in vitro Int. J. Plant Sci. 157 713–721 Occurrence Handle10.1086/297393
E. A. Tzortzakakis S. R. Gowen (1996) ArticleTitleOccurrence of a resistance breaking pathotype of Meloidogyne javanica on tomatoes in Crete, Greece Fundam. Appl. Nematol. 19 283–288
P. E. Urwin M. J. McPherson H. J. Atkinson (1998) ArticleTitleEnhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs Planta 204 472–479 Occurrence Handle10.1007/s004250050281 Occurrence Handle9684370
P. E. Urwin J. Green H. J. Atkinson (2003) ArticleTitleExpression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistance Mol. Breed. 12 263–269 Occurrence Handle10.1023/A:1026352620308
N. M. Dam Particlevan M. Horn M. Mares I. T. Baldwin (2001) ArticleTitleOntogeny constrains systemic protease inhibitor response in Nicotiana attenuata J. Chem. Ecol. 27 547–568 Occurrence Handle10.1023/A:1010341022761 Occurrence Handle11441445
N. M. Dam Particlevan J. A. Harvey F. L. Wackers T. M. Bezemer W. H. Putten Particlevan der L. E. M. Vet (2003) ArticleTitleInteractions between aboveground and belowground induced responses against phytophages Basic Appl. Ecol. 4 63–77 Occurrence Handle10.1078/1439-1791-00133
R. M. P. Poecke Particlevan M. Dicke (2004) ArticleTitleIndirect defense of plants against herbivores: Using Arabidopsis thaliana as a model plant Plant Biol. 6 387–401 Occurrence Handle10.1055/s-2004-820887 Occurrence Handle15248121
P. Vijayan J. Shockey C. A. Levesque R. J. Cook J. Browse (1998) ArticleTitleA role for jasmonate in pathogen defense of Arabidopsis Proc. Natl Acad. Sci. USA 95 7209–7214 Occurrence Handle10.1073/pnas.95.12.7209 Occurrence Handle9618564
S. C. Wang M. Ichii S. Taketa L. L. Xu K. Xia X. Zhou (2002) ArticleTitleLateral root formation in rice (Oryza sativa): Promotion effect of jasmonic acid J. Plant Physiol. 159 827–832 Occurrence Handle10.1078/0176-1617-00825
V. M. Williamson (1998) ArticleTitleRoot-knot nematode resistance genes in tomato and their potential for future use Annu. Rev. Phytopathol. 36 277–293 Occurrence Handle10.1146/annurev.phyto.36.1.277 Occurrence Handle15012501
V. M. Williamson R. S. Hussey (1996) ArticleTitleNematode pathogenesis and resistance in plants Plant Cell 8 1735–1745 Occurrence Handle10.1105/tpc.8.10.1735 Occurrence Handle8914324
V. M. Williamson C. Gleason (2003) ArticleTitlePlant–nematode interactions Curr. Opin. Plant Biol. 6 327–333 Occurrence Handle10.1016/S1369-5266(03)00059-1 Occurrence Handle12873526
J. Yaghoobi I. Kaloshian Y. Wen V. M. Williamson (1995) ArticleTitleMapping a new nematode resistance locus in Lycoperiscon peruvianum Theor. Appl. Genet. 91 457–464 Occurrence Handle10.1007/BF00222973
G. Zacheo C. Orlando T. Bleve-Zacheo (1993) ArticleTitleCharacterization of anionic peroxidases in tomato isolines infected by Meloidogyne incognita J. Nematol. 25 249–256
Z. P. Zhang I. T. Baldwin (1997) ArticleTitleTransport of [2-C-14] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris Planta 203 436–441 Occurrence Handle10.1007/s004250050211
Acknowledgments
We are grateful to Dr. Valerie Williamson, Waclawa Pudlo, and Dr. Cynthia Gleason for providing nematode isolates for this project. We thank Fangyan Chen and John Geurber for their assistance with greenhouse maintenance, and Dr. Ron McNew and Dr. Andronikos Mauromoustakos for assistance with statistical analysis. We also appreciate the feedback of Dr. Robert Riggs and two anonymous reviewers on this manuscript. This research was funded by the Arkansas Agricultural Experiment Station and the California Tomato Commission, as well as by USDA Southern Agricultural Research and Education program (SARE) grant no. GS03-027.
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Cooper, W.R., Jia, L. & Goggin, L. Effects of Jasmonate-Induced Defenses on Root-Knot Nematode Infection of Resistant and Susceptible Tomato Cultivars. J Chem Ecol 31, 1953–1967 (2005). https://doi.org/10.1007/s10886-005-6070-y
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DOI: https://doi.org/10.1007/s10886-005-6070-y