Abstract
Glycerol-3-phosphate (G3P) is an important metabolite that contributes to the growth and disease-related physiologies of prokaryotes, plants, animals and humans alike. Here we show that G3P serves as the inducer of an important form of broad-spectrum immunity in plants, termed systemic acquired resistance (SAR). SAR is induced upon primary infection and protects distal tissues from secondary infections. Genetic mutants defective in G3P biosynthesis cannot induce SAR but can be rescued when G3P is supplied exogenously. Radioactive tracer experiments show that a G3P derivative is translocated to distal tissues, and this requires the lipid transfer protein, DIR1. Conversely, G3P is required for the translocation of DIR1 to distal tissues, which occurs through the symplast. These observations, along with the fact that dir1 plants accumulate reduced levels of G3P in their petiole exudates, suggest that the cooperative interaction of DIR1 and G3P orchestrates the induction of SAR in plants.
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References
Durrant, W.E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).
Vlot, A.C., Klessig, D.F. & Park, S.-W. Systemic acquired resistance: the elusive signal(s). Curr. Opin. Plant Biol. 11, 436–442 (2008).
Iriti, M. & Faoro, F. Review of innate and specific immunity in plants and animals. Mycopathologia 164, 57–64 (2007).
Smith-Becker, J. et al. Accumulation of salicylic acid and 4-hydroxybenzoic acid in phloem of cucumber during systemic acquired resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant Physiol. 116, 231–238 (1998).
Rasmussen, J.B., Hammerschmidt, R. & Zook, M.N. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342–1347 (1991).
Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J. & Cameron, R.K. A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis. Nature 419, 399–403 (2002).
Vlot, A.C., Dempsey, D.A. & Klessig, D.F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177–206 (2009).
Park, S.-W., Kaimoyo, E., Kumar, D., Mosher, S. & Klessig, D. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116 (2007).
Jung, H.W., Tschaplinkski, T.J., Wang, L., Glazebrook, J. & Greenberg, J.T. Priming in systemic plant immunity. Science 324, 89–91 (2009).
Truman, W.M., Bennett, M.H., Turnbull, C.G. & Grant, M.R. Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 152, 1562–1573 (2010).
Truman, W., Bennett, M.H., Kubigsteltig, I., Turnbull, C. & Grant, M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA 104, 1075–1080 (2007).
Attaran, E., Zeier, T.E., Griebel, T. & Zeier, J. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21, 954–971 (2009).
Xia, Y. et al. An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe 5, 151–165 (2009).
Xia, Y. et al. The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol. 154, 833–846 (2010).
Nandi, A., Welti, R. & Shah, J. The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell 16, 465–477 (2004).
Miquel, M., Cassagne, C. & Browse, J. A new class of Arabidopsis mutants with reduced hexadecatrienoic acid fatty acid levels. Plant Physiol. 117, 923–930 (1998).
Kachroo, A. et al. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl. Acad. Sci. USA 101, 5152–5157 (2004).
Lu, M., Tang, X. & Zhou, J.-M. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13, 437–447 (2001).
Kang, L. et al. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc. Natl. Acad. Sci. USA 100, 3915–3924 (2003).
Kachroo, P., Venugopal, S.C., Navarre, D.A., Lapchyk, L. & Kachroo, A. Role of salicylic acid and fatty acid desaturation pathways in ssi2-mediated signaling. Plant Physiol. 139, 1717–1735 (2005).
Chaturvedi, R. et al. Plastid omega-3-fatty acid desaturase-dependent accumulation of systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54, 106–117 (2008).
Wei, Y., Periappuram, C., Datla, R., Selvaraj, G. & Zou, J. Molecular and biochemical characterization of a plastidic glycerol-3-phosphate dehydrogenase from Arabidopsis. Plant Physiol. Biochem. 39, 841–848 (2001).
Shen, W., Wei, Y., Dauk, M., Zheng, Z. & Zou, J. Identification of a mitochondrial glycerol-3-phosphate dehydrogenase from Arabidopsis thaliana: evidence for a mitochondrial glycerol-3-phosphate shuttle in plants. FEBS Lett. 536, 92–96 (2003).
Shen, W. et al. Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18, 422–441 (2006).
Quettier, A.-L., Shaw, E. & Eastmond, P.J. SUGAR-DEPENDENT6 encodes a mitochondrial flavin adenine dinucleotide-dependent glycerol-3-P dehdrogenase, which is required for glycerol catabolism and postgerminative seedling growth in Arabidopsis. Plant Physiol. 148, 519–528 (2008).
Fillinger, S. et al. Molecular and physiological characterization of the NAD-dependent glycerol 3-phosphate dehydrogenase in the filamentous fungus Aspergilllus nidulans. Mol. Microbiol. 39, 145–157 (2001).
Venugopal, S.C., Chanda, B., Vaillancourt, L., Kachroo, A. & Kachroo, P. The common metabolite glycerol-3-phosphate is a novel regulator of defense signaling. Plant Signal. Behav. 4, 746–749 (2009).
Vlot, A.C. et al. Identification of likely orthologs of tobacco salicylic acid binding protein 2 and their role in systemic resistance in Arabidopsis thaliana. Plant J. 56, 445–456 (2008).
Liu, P.-P., Yang, Y., Pichersky, E. & Klessig, D.F. Altering expression of Benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in Arabidopsis. Mol. Plant Microbe Interact. 23, 82–90 (2010).
Wildermuth, M.C., Dewdney, J., Wu, G. & Ausubel, F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565 (2001).
Lascombe, M.-B. et al. The structure of “defective in induced resistance” protein of Arabidopsis thaliana, DIR1, reveals a new type of lipid transfer protein. Protein Sci. 17, 1522–1530 (2008).
Robert, H.S. & Friml, J. Auxin and other signals on the move in plants. Nat. Chem. Biol. 5, 325–332 (2009).
Chanda, B. et al. Glycerol-3-phosphate levels are associated with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis. Plant Physiol. 147, 2017–2029 (2008).
Argast, M. & Boos, W. Purification and properties of the sn-glycerol 3-phosphate-binding protein of Escherichia coli. J. Biol. Chem. 254, 10931–10935 (1979).
Chandra-Shekara, A.C. et al. Light-dependent hypersensitive response and resistance signaling to turnip crinkle virus in Arabidopsis. Plant J. 45, 320–334 (2006).
Selote, D. & Kachroo, A. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol. 153, 1199–1211 (2010).
Martin, K. et al. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 59, 150–162 (2009).
Acknowledgements
We thank D. Smith and J. Shanklin for useful discussions, M. Goodin for providing the pSITE-2NA and TMV-MP30-GFP vectors and GFP antibodies and J. Johnson for help with gas chromatography. We thank L. Lapchyk for technical help and A. Crume for managing the plant growth facility. This work was supported by grants from the National Science Foundation (IOS#0749731) to A.K. and P.K. and United Soybean Board (#9444) to A.K.
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B.C. and Y.X. carried out Arabidopsis SAR experiments in parallel with contributions from K.‐T.S. and Q.-m.G. Soybean SAR experiments were carried out by D.S. G3P estimations were carried out by B.C. with contributions from Y.X. Generation of G3Pdh knockout lines and their analysis was carried out by B.C. GLY1-GFP transgenic lines were generated by K.‐T.S. DIR1 protein purification, binding, translocation assays and confocal microscopy were carried out by M.K.M. with contributions from D.S. TLC and G3P translocation assays were carried out by B.C. and M.K.M. with contributions from P.K. RNA blot and RT-PCR analyses were carried out by B.C. and Q.-m.G. Y.H. and A.S. analyzed microarray data with contributions from M.K.M. D.N. estimated salicylic acid levels. K.Y., B.C. and P.K. analyzed azeliac acid and jasmonic acid levels. K.Y. developed GC-MS–based protocol for detection and quantification of glycerol. P.K. and A.K. supervised the project and wrote the manuscript.
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Chanda, B., Xia, Y., Mandal, M. et al. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43, 421–427 (2011). https://doi.org/10.1038/ng.798
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DOI: https://doi.org/10.1038/ng.798
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