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Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants

Nature Genetics volume 43, pages 421–427 (2011)Cite this article

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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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Figure 1: Impaired SAR in gly1 and gli1 plants correlates with a defect in G3P metabolism but not fatty acid (FA) or lipid flux.
Figure 2: G3P levels increase in response to pathogen inoculation.
Figure 3: Exogenous application of G3P restores defective SAR in gly1 and gli1 plants, and G3P-conferred SAR is dependent on SID2.
Figure 4: G3P-conferred SAR is dependent on DIR1.
Figure 5: G3P and DIR1 are dependent on each other for translocation into distal tissues.

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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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Author notes

  1. Ken‐Taro Sekine

    Present address: Present address: Iwate Biotechnology Research Center, Iwate, Japan.,

  2. Bidisha Chanda and Ye Xia: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA

    Bidisha Chanda, Ye Xia, Mihir Kumar Mandal, Keshun Yu, Ken‐Taro Sekine, Qing-ming Gao, Devarshi Selote, Aardra Kachroo & Pradeep Kachroo

  2. Department of Statistics, University of Kentucky, Lexington, Kentucky, USA

    Yanling Hu & Arnold Stromberg

  3. US Department of Agriculture, Agricultural Research Service, Washington State University, Prosser, Washington, USA

    Duroy Navarre

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Contributions

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.

Corresponding author

Correspondence to Pradeep Kachroo.

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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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