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Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery

Nature Plants volume 4, pages 157–164 (2018)Cite this article

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Abstract

Virus-induced diseases cause severe damage to cultivated plants, resulting in crop losses. Certain plant–virus interactions allow disease recovery at later stages of infection and have the potential to reveal important molecular targets for achieving disease control. Although recovery is known to involve antiviral RNA silencing1,2, the specific components of the many plant RNA silencing pathways3 required for recovery are not known. We found that Arabidopsis thaliana plants infected with oilseed rape mosaic virus (ORMV) undergo symptom recovery. The recovered leaves contain infectious, replicating virus, but exhibit a loss of viral suppressor of RNA silencing (VSR) protein activity. We demonstrate that recovery depends on the 21–22 nt siRNA-mediated post-transcriptional gene silencing (PTGS) pathway and on components of a transcriptional gene silencing (TGS) pathway that is known to facilitate non-cell-autonomous silencing signalling. Collectively, our observations indicate that recovery reflects the establishment of a tolerant state in infected tissues and occurs following robust delivery of antiviral secondary siRNAs from source to sink tissues, and establishment of a dosage able to block the VSR activity involved in the formation of disease symptoms.

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Fig. 1: Recovered leaves contain virus but have lost strong VSR activity.
Fig. 2: The role of PTGS and TGS genes in recovery.
Fig. 3

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Acknowledgements

This work was supported by funding from the Swiss National Science Foundation (SNF, grant 124940 and 144084 to MH, grant 126329 to FV), the Agence National de la Recherche Scientifique (ANR, grants ANR-08-BLAN-0244 and ANR-13-KBBE-005 to M.H.), the Région Alsace (PhD fellowship to N.P.) and the Centre National de la Recherche Scientifique (CNRS, grant PICS06702 to E.J.P. and M.H.). We would like to thank E. Bucher and T. Blevins for helpful discussions and suggestions, and P. Dunoyer and R. Stadler for providing the SUC:SUL and SUC:GFP Arabidopsis lines, respectively. We thank P. Dunoyer for also providing the Col-0 lines expressing the TBSV p19 and the BYV p21 VSRs. We are grateful to M. Pooggin (INRA, Montpellier) for the anti-P125/P182 antibody. Furthermore, we would like to thank M. Böhrer and T. Blevins for their support with RNA blotting and hybridization, and M. DiDonato, A. Niehl, K. Amari and D. Windels for other technical assistance, discussions and critical comments.

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Author notes

  1. Eduardo José Peña

    Present address: Instituto de Biotecnología y Biología Molecular, Facultad de Ciencias Exactas, UNLP-CONICET, La Plata, Buenos Aires, Argentina

  2. Franck Vazquez

    Present address: MDPI, Basel, Switzerland

Authors and Affiliations

  1. Zurich-Basel Plant Science Center, Department of Environmental Sciences, University of Basel, Basel, Switzerland

    Camilla Julie Kørner, Franck Vazquez & Manfred Heinlein

  2. Université de Strasbourg, CNRS, IBMP UPR 2357, Strasbourg, France

    Nicolas Pitzalis, Eduardo José Peña, Mathieu Erhardt & Manfred Heinlein

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  1. Camilla Julie Kørner
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Contributions

F.V. and M.H. conceived and designed the research; C.J.K., N.P., E.J.P., M.E. and M.H. performed the research; C.J.K., N. P., E.J.P., F.V. and M.H. analysed the data; M.E., F.V. and M.H. contributed reagents, materials and analysis tools; C.J.K., F.V. and M.H. wrote the paper; C.J.K, N. P., E.J.P., M.E., F.V. and M.H. read the manuscript and approved the final version of the manuscript.

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Correspondence to Manfred Heinlein.

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Supplementary Information

Supplementary Figures 1–14

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Supplementary Table 1

Occurrence and timing of recovery in hormone pathway mutants

Supplementary Table 2

Table of nucleic acid qPCR primers and northern blot hybridization probes

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Kørner, C.J., Pitzalis, N., Peña, E.J. et al. Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. Nature Plants 4, 157–164 (2018). https://doi.org/10.1038/s41477-018-0117-x

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