Abstract
Localized attack by a necrotizing pathogen induces systemic acquired resistance (SAR) to subsequent attack by a broad range of normally virulent pathogens. Salicylic acid accumulation is required for activation of local defenses, such as pathogenesis-related protein accumulation, at the initial site of attack, and for subsequent expression of SAR upon secondary, distant challenge1,2. Although salicylic acid moves through the plant, it is apparently not an essential mobile signal2. We screened Agrobacterium tumefaciens transfer DNA (tDNA) tagged lines of Arabidopsis thaliana for mutants specifically compromized in SAR. Here we show that Defective in induced resistance 1-1 (dir1-1) exhibits wild-type local resistance to avirulent and virulent Pseudomonas syringae, but that pathogenesis-related gene expression is abolished in uninoculated distant leaves and dir1-1 fails to develop SAR to virulent Pseudomonas or Peronospora parasitica. Petiole exudate experiments indicate that dir1-1 is defective in the production or transmission from the inoculated leaf of an essential mobile signal. DIR1 encodes a putative apoplastic lipid transfer protein and we propose that DIR1 interacts with a lipid-derived molecule to promote long distance signalling.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Hammerschmidt, R. Induced resistance: how do induced plants stop pathogens? Physiol. Mol. Plant Pathol. 55, 77–84 (1999)
Mauch-Mani, B. & Métraux, J-P. Salicylic acid and systemic acquired resistance to pathogen attack. Ann. Bot. 82, 535–540 (1998)
Feys, B. J. & Parker, J. E. Interplay of signaling in plant disease resistance. Trends Genet. 16, 449–455 (2000)
Feldman, K. A. in Methods in Arabidopsis Research (eds Koncz, C., Chua, N. H. & Schell, J.) 274–289 (World Scientific, Singapore/New Jersey/London/Hong Kong, 1992)
Wolfe, J., Hutcheon, C., Higgins, V. J. & Cameron, R. A functional gene-for-gene interaction is required for the production of an oxidative burst in response to infection with avirulent Pseudomonas syringae pv. tomato in Arabidopsis thaliana. Physiol. Mol. Plant Pathol. 56, 253–261 (2000)
Vernooij, B. et al. 2,6-dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 8, 228–234 (1995)
Liu, Y-G., Mitsukawa, N., Oosumi, T. & Whittier, R. F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457–463 (1995)
D'Alessio, J. M., Bebee, R., Hartley, J. L., Noon, M. C. & Polayes, D. Lambda Ziplox: Automatic subcloning of cDNA. Focus 14, 76 (1992)
Kader, J-C. Lipid-transfer proteins: a puzzling family of plant proteins. Trends Plant Sci. 2, 66–70 (1997)
Cao, H., Bowling, S. A., Gordon, A. S. & Dong, X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583–1592 (1994)
Delaney, T. P., Friedrich, L. & Ryals, J. A. An Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl Acad. Sci. USA 92, 6602–6606 (1995)
Parker, J. E. et al. Characterization of eds1, a mutation in Arabidopsis which suppresses resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8, 2033–2046 (1996)
Zhou, N., Tootle, T., Tsui, F., Klessig, D. & Glazebrook, J. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10, 1021–1030 (1998)
Shirasu, K., Nakajima, H., Rajasekhar, V. K., Dixon, R. A. & Lamb, C. J. Salicylic acid potentiates an agoinst-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261–270 (1997)
Conrath, U., Pieterse, C. M. J. & Mauch-Mani, B. Priming in plant-pathogen interactions. Trends Plant Sci. 7, 210–216 (2002)
Cameron, R. K., Paiva, N. L., Lamb, C. J. & Dixon, R. A. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, 121–130 (1999)
Nawrath, C. & Métraux, J. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen infection. Plant Cell 11, 1393–1404 (1999)
Arondel, V., Vergnolle, C., Cantrel, C. & Kader, J. Lipid transfer proteins are encoded by a small multigene family in Arabidopsis thaliana. Plant Sci. 157, 1–12 (2000)
Wirtz, K. W. Phospholipid transfer proteins revisited. Biochem. J. 324, 353–360 (1997)
Gomar, J. et al. Comparison of solution and crystal structures of maize nonspecific lipid transfer protein: a model for a potential in vivo lipid carrier protein. Proteins 31, 160–171 (1998)
Thoma, S., Kaneko, Y. & Somerville, C. A non-specific lipid transfer protein from Arabidopsis thaliana is a cell wall protein. Plant J. 3, 427–436 (1993)
Garcia-Olmedo, F., Molina, A., Segura, A. & Moreno, M. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol. 3, 72–74 (1995)
Wasternack, C. & Parthier, B. Jasmonate-signalled plant gene expression. Trends Plant Sci. 2, 302–307 (1997)
Chapman, K. D. Emerging physiological roles for N-acylphosphatidylethanolamine metabolism in plants: signal transduction and membrane protection. Chem. Phys. Lipids 108, 221–230 (2000)
Munnik, T. Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci. 6, 227–233 (2001)
Jirage, D. et al. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl Acad. Sci. USA 96, 13583–13588 (1999)
Falk, A. et al. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl Acad. Sci. USA 96, 3292–3297 (1999)
Church, G. M. & Gilbert, W. Genomic sequencing. Proc. Natl Acad. Sci. USA 81, 1991–1995 (1984)
King, R. W. & Zeevaart, J. A. D. Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol. 53, 96–103 (1974)
Chen, S., Petersen, B. L., Olsen, C. E., Schulz, A. & Halkier, B. A. Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol. 127, 194–201 (2001)
Blein, J.-P., Coutos-Thévenot, P., Marion, D. & Ponchet, M. From elicitins to lipid transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci. 7, 293–296 (2002)
Acknowledgements
We thank colleagues for plasmids and bacterial strains (see Methods), J. McDowell for providing Arabidopsis/P. parasitica-infected leaves, C. Hutcheon for analysing the oxidative burst, and N. Paiva and J. Blount for help with salicylic acid determinations. This work was supported by grants from the Noble Foundation (R.A.D. and C.J.L.), Agritope (C.J.L.), the Natural Sciences and Engineering Research Council of Canada (R.K.C.) and the Canada Foundation for Innovation (R.K.C.) and by the UK Biotechnology and Biological Sciences Research Council (C.J.L.). A.M.M. was supported by post-doctoral fellowships from the Ministerio de Educacion y Cultura de Espana and Gobierno Vasco.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
C.J.L. was on the Scientific Advisory Board of Agritope from 1997–99.
Rights and permissions
About this article
Cite this article
Maldonado, A., Doerner, P., Dixon, R. et al. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403 (2002). https://doi.org/10.1038/nature00962
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature00962
This article is cited by
-
The revealing of a novel lipid transfer protein lineage in green algae
BMC Plant Biology (2023)
-
N-hydroxypipecolic acid triggers systemic acquired resistance through extracellular NAD(P)
Nature Communications (2023)
-
Lipid transfer proteins: structure, classification and prospects of genetic engineering for improved disease resistance in plants
Plant Cell, Tissue and Organ Culture (PCTOC) (2023)
-
An Overview of Molecular Basis and Genetic Modification of Floral Organs Genes: Impact of Next-Generation Sequencing
Molecular Biotechnology (2023)
-
Characterization of non-specific lipid transfer protein (nsLtp) gene families in the Brassica napus pangenome reveals abundance variation
BMC Plant Biology (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.