Conserved nematode signalling molecules elicit plant defenses and pathogen resistance
Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan. However, it remained unknown whether plants can detect conserved molecular patterns derived from plant-parasitic animals, including nematodes. Here we show that several genera of plant-parasitic nematodes produce small molecules called ascarosides, an evolutionarily conserved family of nematode pheromones. Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways. Ascr#18 perception increases resistance in Arabidopsis, tomato, potato and barley to viral, bacterial, oomycete, fungal and nematode infections. These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes. Using small-molecule signals such as ascarosides to activate plant immune responses has potential utility to improve economic and environmental sustainability of agriculture.
© 2015 Macmillan Publishers Limited. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 24 November 2014; Accepted 10 June 2015; Published 23 July 2015. We thank William E. Fry for providing P. infestans strains and laboratory space for P. infestans inoculations, Neelanjan Bose, Alexander Artyukhin and Sydney Campbell for assistance with HPLC-MS analyses, Anshu Kumari for the greenhouse support and Patrick Boyle for helpful discussions. This work was supported in part by the USDA (AFRI 2011-68004-30154 to D.F.K., AFRI 2013-02577 to V.M.W. and AFRI 2014-04823 to F.K.), the NSF (IOS-0820405, to D.F.K.), the Triad Foundation (D.F.K. and F.C.S.) and BASF SE. Contributions: P.M., M.M., D.F.K. and F.C.S. designed the research; P.M., M.M., A.K., S.H.v.R., F.K., and S.C. performed the research; F.K., A.C., and V.M.W. contributed reagents, S.H.v.R., F.K. and F.C.S. analyzed nematode metabolomes, R.J.M and S.H.v.R. synthesized ascarosides; P.M., M.M., S.H.v.R., D.F.K., A.K., S.C., X.W., K.-H.K. and F.C.S. analyzed the data; and D.F.K., P.M., M.M., F.K., V.M.W., and F.C.S. wrote the paper. The authors declare no competing financial interests.
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