The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling

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Abstract

The endosomal sorting complex required for transport (ESCRT) machinery has been well documented for its function in endosomal sorting in eukaryotes. Here, we demonstrate an up-to-now unknown and non-endosomal function of the ESCRT component in plants. We show that FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1 (FREE1), a recently identified plant-specific ESCRT component essential for multivesicular body biogenesis, plays additional functions in the nucleus in transcriptional inhibition of abscisic acid (ABA) signalling. Following ABA treatment, SNF1-related protein kinase 2 (SnRK2) kinases phosphorylate FREE1, a step requisite for ABA-induced FREE1 nuclear import. In the nucleus, FREE1 interacts with the basic leucine zipper transcription factors ABA-RESPONSIVE ELEMENTS BINDING FACTOR4 and ABA-INSENSITIVE5 to reduce their binding to the cis-regulatory sequences of downstream genes. Collectively, our study demonstrates the crosstalk between endomembrane trafficking and ABA signalling at the transcriptional level and highlights the moonlighting properties of the plant ESCRT subunit FREE1, which has evolved unique non-endosomal functions in the nucleus besides its roles in membrane trafficking in the cytoplasm.

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Fig. 1: free1-ctmut is a newly identified free1 weak allele and is hypersensitive to ABA treatment.
Fig. 2: ABA treatment induces nuclear shuttling of FREE1.
Fig. 3: SnRK2 kinases interact with and phosphorylate the FREE1 protein.
Fig. 4: Identification of the phosphorylation sites located in the C terminus of FREE1.
Fig. 5: FREE1 interacts with and supresses the transcriptional activation activities of ABF4 and ABI5.
Fig. 6: Genetic interactions between FREE1 and ABF4 or ABI5.

Data availability

The data that support the findings of this study are available from the corresponding authors on reasonable request.

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31671467 and 31870171), the China 1000-Talents Plan for young researchers (C83025) to C.G., the National Natural Science Foundation of China (31701246) to W.S., the China Postdoctoral Science Foundation (2018M630963) and the National Science Foundation of Guangdong Province (2018A030310505) to C.Y., the National Natural Science Foundation of China (91854201) and the Research Grants Council of Hong Kong (C4011-14R, C4012-16E, C4002-17G and AoE/M-05/12) to L.J. We thank H. Deng for her assistance on the EMSA experiments.

Author information

H.L., Y.L., Q.Z. and C.G. designed the project. H.L., Y.L., Q.Z., T.L., J.W., B.L. and Y.Z. performed the experiments. H.L., Y.L., Q.Z., W.S., C.Y., P.L.R., Y.Z., L.J., X.W. and C.G. analysed the results. H.L., Q.Z., R.L.R., L.J., X.W. and C.G. wrote the manuscript.

Correspondence to Liwen Jiang or Xiaojing Wang or Caiji Gao.

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Journal peer review information: Nature Plants thanks Masa Sato and other anonymous reviewers for their contribution to the peer review of this work.

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Li, H., Li, Y., Zhao, Q. et al. The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling. Nat. Plants 5, 512–524 (2019) doi:10.1038/s41477-019-0400-5

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