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NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors

Nature Plants volume 4, pages 811–823 (2018)Cite this article

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Abstract

NON-EXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1) is a master regulator of plant response to pathogens that confers immunity through a transcriptional cascade mediated by salicylic acid and TGA transcription factors. Little is known, however, about its implication in plant response to abiotic stress. Here, we provide genetic and molecular evidence supporting the fact that Arabidopsis NPR1 plays an essential role in cold acclimation by regulating cold-induced gene expression independently of salicylic acid and TGA factors. Our results demonstrate that, in response to low temperature, cytoplasmic NPR1 oligomers release monomers that translocate to the nucleus where they interact with heat shock transcription factor 1 (HSFA1) to promote the induction of HSFA1-regulated genes and cold acclimation. These findings unveil an unexpected function for NPR1 in plant response to low temperature, reveal a new regulatory pathway for cold acclimation mediated by NPR1 and HSFA1 factors, and place NPR1 as a central hub integrating cold and pathogen signalling for a better adaptation of plants to an ever-changing environment.

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Fig. 1: NPR1 accumulates in response to low temperature and positively regulates cold acclimation in Arabidopsis.
Fig. 2: Monomerisation and nuclear localization of NPR1 depends on TRXH3, TRXH5 and SnRK2.8, and are required for cold acclimation.
Fig. 3: NPR1 activates the cold-induction of HSFA1-regulated genes.
Fig. 4: HSFA1 factors promote cold acclimation by inducing heat stress-responsive gene expression under low-temperature conditions.
Fig. 5: NPR1 interacts with HSFA1 factors to activate cold-induced heat stress-responsive gene expression.
Fig. 6: Proposed model for the function of NPR1 in cold acclimation response.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request. All primers used in this study are described in Supplementary Table 4. Sequence data from the genes mentioned in this article can be found in the GenBank/EMBL data libraries under the accession numbers listed in Supplementary Table 6. The full names of these genes are also included in Supplementary Table 6. The RNAseq data from this article have been submitted to the Gene Expression Omnibus database (www.ncbi.nlm.nih.gov/geo) and assigned the identifier accession GSE101483.

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Acknowledgements

We thank all our colleagues who kindly provided us with the mutants and transgenic plants used in this work (see Methods section for details). Furthermore, we thank J.J. Sanchez-Serrano, R. Solano, J. Barrero-Gil and R. Catalá for helpful discussions and comments. This research was supported by grants BIO2013-47788-R from MINECO and BIO2016-79187-R from AEI/FEDER, UE to J.S. and grants 1141202 from FONDECYT and NC130030 from the Millennium Science Initiative to L.H. E.O. was the recipient of a PhD fellowship from CONICYT and an I-COOP + scholarship from the CSIC.

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Authors and Affiliations

  1. Departamento de Biotecnología Microbiana y de Plantas, Centro Investigaciones Biológicas, CSIC, Madrid, Spain

    Ema Olate & Julio Salinas

  2. Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

    Ema Olate & Loreto Holuigue

  3. Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay , Versailles Cedex, France

    José M. Jiménez-Gómez

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  1. Ema Olate
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  2. José M. Jiménez-Gómez
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Contributions

E.O., L.H. and J.S. conceived and designed the experiments. E.O. performed the experiments. E.O., J.M.M. and J.S. analysed the data. J.S. wrote the paper.

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Correspondence to Julio Salinas.

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Supplementary Information

Supplementary Figures 1–9, Supplementary Methods, Supplementary References and Supplementary Table legends.

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Olate, E., Jiménez-Gómez, J.M., Holuigue, L. et al. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nature Plants 4, 811–823 (2018). https://doi.org/10.1038/s41477-018-0254-2

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