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

Hongbo Li; Yingzhu Li; Qiong Zhao; Tingting Li; Juan Wei; Baiying Li; Wenjin Shen; Chao Yang; Yonglun Zeng; Pedro L. Rodriguez; Yunde Zhao; Liwen Jiang; Xiaojing Wang; Caiji Gao

doi:10.1038/s41477-019-0400-5

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

Hongbo Li, Yingzhu Li, Qiong Zhao, Tingting Li, Juan Wei, Baiying Li, Wenjin Shen, Chao Yang, Yonglun Zeng, Pedro L. Rodriguez, Yunde Zhao, Liwen Jiang^*, Xiaojing Wang^*, Caiji Gao^*

^*Corresponding author for this work

Department of Biology

Research output: Contribution to journal › Journal article › peer-review

68 Citations (Scopus)

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.

Original language	English
Pages (from-to)	512-524
Number of pages	13
Journal	Nature Plants
Volume	5
Issue number	5
Early online date	8 Apr 2019
DOIs	https://doi.org/10.1038/s41477-019-0400-5
Publication status	Published - 1 May 2019

Scopus Subject Areas

Plant Science

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41477-019-0400-5

Cite this

@article{9cf22829b7414d47a1724ab4f89a6039,

title = "The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling",

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.",

author = "Hongbo Li and Yingzhu Li and Qiong Zhao and Tingting Li and Juan Wei and Baiying Li and Wenjin Shen and Chao Yang and Yonglun Zeng and Rodriguez, {Pedro L.} and Yunde Zhao and Liwen Jiang and Xiaojing Wang and Caiji Gao",

note = "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. Publisher Copyright: {\textcopyright} 2019, The Author(s), under exclusive licence to Springer Nature Limited.",

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AU - Li, Hongbo

AU - Li, Yingzhu

AU - Zhao, Qiong

AU - Li, Tingting

AU - Wei, Juan

AU - Li, Baiying

AU - Shen, Wenjin

AU - Yang, Chao

AU - Zeng, Yonglun

AU - Rodriguez, Pedro L.

AU - Zhao, Yunde

AU - Jiang, Liwen

AU - Wang, Xiaojing

AU - Gao, Caiji

N1 - 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. Publisher Copyright: © 2019, The Author(s), under exclusive licence to Springer Nature Limited.

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Y1 - 2019/5/1

N2 - 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.

AB - 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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DO - 10.1038/s41477-019-0400-5

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SN - 2055-026X

VL - 5

SP - 512

EP - 524

JO - Nature Plants

JF - Nature Plants

IS - 5

ER -

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

Abstract

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