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A fungal monooxygenase-derived jasmonate attenuates host innate immunity

Nature Chemical Biology volume 11, pages 733–740 (2015)Cite this article

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Abstract

Distinct modifications fine-tune the activity of jasmonic acid (JA) in regulating plant growth and immunity. Hydroxylated JA (12OH-JA) promotes flower and tuber development but prevents induction of JA signaling, plant defense or both. However, biosynthesis of 12OH-JA has remained elusive. We report here an antibiotic biosynthesis monooxygenase (Abm) that converts endogenous free JA into 12OH-JA in the model rice blast fungus Magnaporthe oryzae. Such fungal 12OH-JA is secreted during host penetration and helps evade the defense response. Loss of Abm in M. oryzae led to accumulation of methyl JA (MeJA), which induces host defense and blocks invasive growth. Exogenously added 12OH-JA markedly attenuated abmΔ-induced immunity in rice. Notably, Abm itself is secreted after invasion and most likely converts plant JA into 12OH-JA to facilitate host colonization. This study sheds light on the chemical arms race during plant-pathogen interaction, reveals Abm as an antifungal target and outlines a synthetic strategy for transformation of a versatile small-molecule phytohormone.

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Figure 1: M. oryzae uses the Abm monooxygenase to evade host innate immunity.
Figure 2: Abm is involved in the biosynthesis of 12OH-JA from JA.
Figure 3: JA derivatives show distinct effects on the host defense response against the blast fungus.
Figure 4: 12OH-JA blocks the induction of JA signaling.
Figure 5: Abm associates partially with the endoplasmic reticulum in M. oryzae and is secreted during invasive growth.
Figure 6: Abm-based hydroxylation of endogenous JA by M. oryzae overcomes the innate immunity in rice.

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Acknowledgements

We thank P. Staswick (University of Nebraska) for the chemically synthesized 12OH-JA and L. Laplaze (Institut de recherche pour le développement, France) for sharing Jas9-VENUS plasmids and transgenic Arabidopsis seeds. We thank L. Yixin and Z. Bo for help with ChemDraw. We also thank the Fungal Patho-Biology group for helpful discussions and suggestions. We are grateful to M. Calvert for help in spinning-disk confocal microscopy. This research was carried out using funds from the Temasek Life Sciences Laboratory (Singapore) and the National Research Foundation (Prime Minister's Office; NRF-CRP7-2010-02), Singapore.

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Author notes

  1. Yuan Yi Constance Chen

    Present address: Present address: Duke-NUS Graduate Medical School, Singapore.,

Authors and Affiliations

  1. Temasek Life Sciences Laboratory, Singapore

    Rajesh N Patkar, Ziwei Qu, Yuan Yi Constance Chen, Fan Yang & Naweed I Naqvi

  2. Department of Biological Sciences, National University of Singapore, Singapore

    Peter I Benke, Ziwei Qu, Sanjay Swarup & Naweed I Naqvi

  3. Singapore Centre for Environmental Life Sciences Engineering, Singapore

    Peter I Benke & Sanjay Swarup

  4. NUS Environmental Research Institute, National University of Singapore, Singapore

    Peter I Benke & Sanjay Swarup

  5. School of Biological Sciences, Nanyang Technological University, Singapore

    Naweed I Naqvi

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Contributions

R.N.P. conceived, designed and performed the experiment, analyzed the data and co-wrote the manuscript. P.I.B. performed the chemical analyses and interpreted the data. Z.Q. performed the experiments. Y.Y.C.C. performed the initial gene-deletion analysis. F.Y. performed the experiments. S.S. contributed the analysis tools and interpreted and analyzed the data. N.I.N. conceived and designed the experiments; provided reagents, materials and analysis tools; analyzed and interpreted the data; and co-wrote the manuscript.

Corresponding authors

Correspondence to Rajesh N Patkar or Naweed I Naqvi.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Results, Supplementary Table 1 and Supplementary Figures 1–15. (PDF 19870 kb)

41589_2015_BFnchembio1885_MOESM249_ESM.mov

Dynamics of Jas9-VENUS and H2B-RFP over a 30 min period in transgenic Arabidopsis roots treated with 1% ethanol (MOV 1649 kb)

41589_2015_BFnchembio1885_MOESM250_ESM.mov

Dynamics of Jas9-VENUS and H2B-RFP over a 30 min period in transgenic Arabidopsis roots treated with 50 μM JA (MOV 1528 kb)

41589_2015_BFnchembio1885_MOESM251_ESM.mov

Dynamics of Jas9-VENUS and H2B-RFP over a 30 min period in transgenic Arabidopsis roots treated with 50 μM MeJA (MOV 1156 kb)

41589_2015_BFnchembio1885_MOESM252_ESM.mov

Dynamics of Jas9-VENUS and H2B-RFP over a 30 min period in transgenic Arabidopsis roots treated with 50 μM 12OH-JA (MOV 1484 kb)

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Patkar, R., Benke, P., Qu, Z. et al. A fungal monooxygenase-derived jasmonate attenuates host innate immunity. Nat Chem Biol 11, 733–740 (2015). https://doi.org/10.1038/nchembio.1885

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