Skip to main content
Log in

Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

A study was performed to determine the effect of the systemin polypeptide on the bio-protective effect of arbuscular mycorrhizal fungi (AMF) in tomato plants infected with Alternaria solani, Phytophthora infestans or P. parasitica. Before infection, tomato plants were colonized with two different AMF, Glomus fasciculatum or G. clarum. In addition, a group of inoculated plants was treated with systemin, just after emergence. The exogenous application of systemin marginally suppressed the resistance against A. solani leaf blight observed in G. fasciculatum mycorrhizal plants but significantly enhanced it in plants colonized with G. clarum. Systemin induced resistance to P. parasitica in leaves of G. fasciculatum mycorrhizal plants, in which AMF colonization alone was shown to have no protective effect. Conversely, none of the treatments led to resistance to root or stem rots caused by P. infestans or P. parasitica. The above effects did not correlate with changes in the activity levels of β-1,3-glucanase (BG), chitinase (CHI), peroxidase (PRX), and phenylalanine ammonium lyase (PAL) in leaves of infected plants. However, they corroborated previous reports showing that colonization by AMF can lead to a systemic resistance response against A. solani. Systemic resistance to A. solani was similarly observed in non-mycorrhizal systemin-treated plants, which, in contrast, showed increased susceptibility to P. infestans and P. parasitica. The results indicated that the pattern of systemic disease resistance conferred by mycorrhizal colonization was dependent on the AMF employed and could be altered by the exogenous application of systemin, by means of a still undefined mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agrios GN (ed) (1997) Plant pathology, 4th edn. Academic, Amsterdam

    Google Scholar 

  • Álvarez M, De Armas G, Martínez B (1997) Informe de nuevas variedades. Amalia y Mariela, dos nuevas variedades de tomate de consumo fresco. Cult Trop 18:83

    Google Scholar 

  • Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Barksdale TH, Stoner AK (1977) A study of the inheritance of tomato early blight resistance. Plant Dis Rep 61:63–65

    Google Scholar 

  • Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053–12058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boller T, Gehri A, Mauch F, Vogeli U (1983) Chitinase in bean leaves: induction by ethylene, purification, properties and possible function. Planta 157:22–31

    Article  CAS  PubMed  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the determination of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burleigh SH, Cavagnaro T, Jakobsen I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53:1593–1601

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonization patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232

    Article  CAS  Google Scholar 

  • Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microb Interact 11:1017–1028

    Article  CAS  Google Scholar 

  • David R, Itzhaki H, Ginzberg I, Gafni Y, Galili G, Kapulnik Y (1998) Suppression of tobacco basic chitinase gene expression in response to colonization by the arbuscular mycorrhizal fungus Glomus intraradices. Mol Plant Microb Interact 11:489–497

    Article  CAS  Google Scholar 

  • Díaz J, ten Have A, van Kan JAL (2002) The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol 129:1341–1351

    Article  PubMed  PubMed Central  Google Scholar 

  • Doares SH, Narváez-Vásquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugassa GD, von Alten H, Schönbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182

    Article  CAS  Google Scholar 

  • Dumas-Gaudot E, Gollote A, Cordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of host defence systems. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 173–200

    Chapter  Google Scholar 

  • Elsen A, Declerck S, De Waele D (2001) Effects of Glomus intraradices on the reproduction of the burrowing nematode (Radopholus similis) in dixenic culture. Mycorrhiza 11:49–51

    Article  Google Scholar 

  • Fernández F, Gómez R, Vanegas LF, Noval BM de la, Martínez MA (2000) Producto inoculante micorrizógeno. Oficina Nacional de Propiedad Industrial (Cuba). Patente No. 22641

  • Food and Agriculture Organization (2004) FAOSTAT Data http://faostat.fao.org/faostat/form?collection=Production.-Crops.Primary&Domain=Production&servlet=1&hasbulk=&version=ext&language=EN. Last updated February 2004

  • Foolad MR, Ntahimpera N, Christ BJ, Lin GY (2000) Comparison between field, greenhouse, and detached-leaflet evaluations of tomato germplasm for early blight resistance. Plant Dis 84:967–972

    Article  Google Scholar 

  • Fric F (1976) Oxidative enzymes. Encycl Plant Physiol 4:617–631

    CAS  Google Scholar 

  • Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhizal reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419

    Article  PubMed  Google Scholar 

  • Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87

    Article  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeun YC, Siegrist J, Buchenauer H (2000) Biochemical and cytological studies on mechanisms of systemically induced resistance to Phytophthora infestans in tomato plants. J Phytopathol 148:129–140

    CAS  Google Scholar 

  • Jones JB, Jones JP, Stall RE, Zitter TA (1993) Compendium of tomato diseases. American Phytopathological Society, St. Paul, MN, USA

    Google Scholar 

  • Judelson HS (1997) The genetics and biology of Phytophthora infestans: modern approaches to a historical challenge. Fungal Genet Biol 22:65–76

    Article  CAS  PubMed  Google Scholar 

  • Kalloo G, Banerjee MK (1993) Early blight resistance in Lycopersicon esculentum Mill. transferred from L. pimpinellifolium (L.) and L. hirsutum f. glabratum (Mill.). Gartenbauwissenschaft 58:238–240

    Google Scholar 

  • Kamoun S, Huitema E, Vleeshouwers VGAA (1999) Resistance to oomycetes: a general role for the hypersensitive response? Trends Plant Sci 4:196–200

    Article  CAS  PubMed  Google Scholar 

  • Lambais MR (2000) Regulation of plant defense-related genes in arbuscular mycorrhizae. In: Podila GK, Douds DD Jr (eds) Current advances in mycorrhizae research. APS Press, USA, pp 45–59

    Google Scholar 

  • Langsdorf G, Furuichi N, Doke N, Nishimura S (1990) Investigations on Alternaria solani infections: detection of alternaric acid and a susceptibility-inducing factor in the spore-germination fluid of A. solani. J Phytopathol 128:271–282

    Article  CAS  Google Scholar 

  • Lawrence CB, Singh NP, Qiu J, Gardner RG, Tuzun S (2000) Constitutive hydrolytic enzymes are associated with polygenic resistance of tomato to Alternaria solani and may function as an elicitor release mechanism. Physiol Mol Plant Pathol 57:211–220

    Article  CAS  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maiero M, Ng TJ, Barksdale TH (1989) Combining ability estimates for early blight resistance in tomato. J Am Soc Hortic Sci 114:118–121

    Google Scholar 

  • Maiero M, Bean GA, Ng TJ (1991) Toxin production by Alternaria solani and its related phytotoxicity to tomato breeding lines. Phytopathology 81:1030–1033

    Article  CAS  Google Scholar 

  • Martin FW, Hepperly P (1987) Sources of resistance to early blight, Alternaria solani, and transfer to tomato, Lycopersicon esculentum. J Agric Univ P R 71:85–95

    Google Scholar 

  • Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonium lyase enzymes in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mora MM, Earle ED (2001) Resistance to Alternaria brassicicola in transgenic broccoli expressing a Trichoderma harzianum endochitinase gene. Mol Breed 8:1–9

    Article  CAS  Google Scholar 

  • Nagarathna KC, Shetty SA, Shetty HS (1993) Phenylalanine ammonia lyase activity in pearl millet seedlings and its relation to downy mildew disease resistance. J Exp Bot 44:1291–1296

    Article  CAS  Google Scholar 

  • Narváez-Vásquez J, Ryan CA (2002) The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosum. Proc Natl Acad Sci USA 99:15818–15821

    Article  PubMed  PubMed Central  Google Scholar 

  • Narváez-Vásquez J, Ryan CA (2004) The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218:360–369

    Article  PubMed  Google Scholar 

  • Nash AF, Gardner R (1988) Heritability of tomato early blight resistance derived from Lycopersicon hirsutum P.I. 126445. J Am Soc Hortic Sci 113:268

    Google Scholar 

  • Niderman T, Genetet I, Bruyere T, Gees R, Stinzi A, Legrand M, Fritig B, Mosinger E (1995) Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108:17–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noval de la BM (2000) Influencia de la sistemina sobre la actividad β-1,3-glucanasa y quitinasa en plántulas de tomate (Lycopersicon esculentum Mill) micorrizadas. MSc Thesis. Cinvestav—Campus Guanajuato, México

  • Noval de la BM, Pérez E, Olalde V, Délano JP, Martínez N (2004) Inducción de β-1,3-glucanasa y quitinasas en plántulas de tomate por hongos micorrizógenos y sistemina. Cult Trop 2:5–12

    Google Scholar 

  • Nuez F, Diez MJ, Pico B, Fernández P (1996) Catálogo de semillas de tomate. Banco de germoplasma de la Universidad Politécnica de Valencia. Instituto Nacional de Investigación y Tecnología Agraria y Alimentación. Colección Monografías INIA No. 95. Ministerio de Agricultura, Pesca y Alimentación, Madrid

    Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898

    Article  CAS  PubMed  Google Scholar 

  • Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Metraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez E, Rodríguez Y, Hernández MA, Noval BM de la (2004) Dinámica de inducción de algunos sistemas de defensa en la interacción HMA-tomate (Lycopersicon esculentum Mill.) var. Amalia (I). Inducción de PR2; PR3 y fenilalanina amonio liasa en raíces de tomate de la variedad Amalia. Cult Trop 25:37–44

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534

    Article  CAS  PubMed  Google Scholar 

  • Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an ArabidopsisPhytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28:293–305

    Article  CAS  PubMed  Google Scholar 

  • Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121

    Article  CAS  PubMed  Google Scholar 

  • Ryan CA, Moura DS (2002) Systemic wound signaling in plants: a new perception. Proc Natl Acad Sci USA 99:6519–6520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan CA, Pearce G (2003) Systemins: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci USA 100:14577–14580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    Article  CAS  PubMed  Google Scholar 

  • Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorriza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant Microb Interact 12:1000–1007

    Article  CAS  Google Scholar 

  • Simmons CR (1994) The physiology and molecular biology of plant 1,3-β-d-glucanases and 1,3;1,4-β-d-glucanases. Crit Rev Plant Sci 13:325–387

    CAS  Google Scholar 

  • Slezak S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum root against Aphanomyces euteiches? Mol Plant Microb Interact 13:238–241

    Article  Google Scholar 

  • Smart CD, Myers KL, Restrepo S, Martin GB, Fry WE (2003) Partial resistance of tomato to Phytophthora infestans is not dependent upon ethylene, jasmonic acid, or salicylic acid signaling pathways. Mol Plant Microb Interact 16:141–148

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Smith FA, Smith SE (1997) Structural diversity in (vesicular)–arbuscular mycorrhizal symbiosis. New Phytol 108:305–314

    Google Scholar 

  • Stennis MJ, Chandra S, Ryan CA, Low PS (1998) Systemin potentiates the oxidative burst in cultures tomato cells. Plant Physiol 117:1031–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato-amplification in wound signaling. Plant J 33:577–589

    Article  CAS  PubMed  Google Scholar 

  • Tejeda-Sartorius M, Martínez-Gallardo N, Olalde-Portugal V, Délano-Frier JP (2007) Jasmonic acid accelerates the expression of a pathogen-specific lipoxygenase (POTLX-3) and delays foliar late blight development in potato (Solanum tuberosum L.). Rev Mex Fitopatol (in press)

  • Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236

    Article  CAS  PubMed  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue B, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BPHJ, Eggermont K, Broekaert WF, Cammue BPA (2000) Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol Biochem 38:421–427

    Article  CAS  Google Scholar 

  • Tipton K (1993) Principles of enzyme assays and kinetic studies. In: Eisenthal R, Danson MJ (eds) Enzyme assays: a practical approach. PAS series. Oxford Univ. Press, UK, pp 1–58

    Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • van Wees SCM, Chang H-S, Zhu T, Glazebrook J (2003) Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132:606–617

    Article  PubMed  PubMed Central  Google Scholar 

  • Vleeshouweres VGAA, van Dooijeweert W, Govers F, Kamoun S, Colon LT (2000) The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210:853–864

    Article  Google Scholar 

  • Yamamizo C, Kuchimura K, Kobayashi A, Katou S, Kawakita K, Jones JDG, Doke N, Yoshioka H (2006) Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol 140:681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JDG, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15:706–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Wozniak CA (1997) Adaptation of a β-1,3-glucanase assay to microplate format. Biotechniques 22:922–926

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Délano-Frier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de la Noval, B., Pérez, E., Martínez, B. et al. Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens. Mycorrhiza 17, 449–460 (2007). https://doi.org/10.1007/s00572-007-0122-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-007-0122-9

Keywords

Navigation