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Noncanonical ATG8–ABS3 interaction controls senescence in plants

Nature Plants volume 5, pages 212–224 (2019)Cite this article

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Abstract

Protein homeostasis is essential for cellular functions and longevity, and the loss of proteostasis is one of the hallmarks of senescence. Autophagy is an evolutionarily conserved cellular degradation pathway that is critical for the maintenance of proteostasis. Paradoxically, autophagy deficiency leads to accelerated protein loss by unknown mechanisms. We discover that the ABNORMAL SHOOT3 (ABS3) subfamily of multidrug and toxic compound extrusion transporters promote senescence under natural and carbon-deprivation conditions in Arabidopsis thaliana. The senescence-promoting ABS3 pathway functions in parallel with the longevity-promoting autophagy to balance plant senescence and survival. Surprisingly, ABS3 subfamily multidrug and toxic compound extrusion proteins interact with AUTOPHAGY-RELATED PROTEIN 8 (ATG8) at the late endosome to promote senescence and protein degradation without canonical cleavage and lipidation of ATG8. This non-autophagic ATG8–ABS3 interaction paradigm is probably conserved among dicots and monocots. Our findings uncover a previously unknown non-autophagic function of ATG8 and an unrecognized senescence regulatory pathway controlled by ATG8–ABS3-mediated proteostasis.

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Fig. 1: ABS3 subfamily MATEs promote plant senescence.
Fig. 2: Genetic interaction between abs3-1D, mateq and the autophagy mutant atg7-3.
Fig. 3: Physical interaction between ABS3 and ATG8e.
Fig. 4: The ATG8–ABS3 interaction is independent of ABS3 transporter activity or ATG8-PE conjugation.
Fig. 5: ABS3-mediated senescence requires ATG8–ABS3 interaction.
Fig. 6: Conserved ATG8–ABS3 interactions in wheat.
Fig. 7: Model for the ATG8–ABS3 interaction in controlling senescence in plants.

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Data availability

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

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31570267 to F.Y., 31770205 to X.L. and 31741010 to Y.Q.) and Northwest A&F University (2452016001 to F.Y.). Y.W., L.S. and J.S. were supported by US National Institute of Health grant R01GM06493. We thank the Teaching and Research Core Facility at the College of Life Sciences, NWAFU for support in this work. We thank members of the Sheen Laboratory and K. Mao of Massachusetts General Hospital and Harvard Medical School, USA for stimulating discussions and critical reading of the manuscript.

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Author notes

  1. Rui Wang

    Present address: Department of Molecular Genetics, Center for Applied Plant Science, Ohio State University, Columbus, OH, USA

  2. These authors contributed equally: Min Jia, Xiayan Liu.

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F University, Yangling, Shaanxi, China

    Min Jia, Xiayan Liu, Hui Xue, Rui Wang, Yu Chen, Ni Xu, Jun Zhao, Jingxia Shao, Yafei Qi, Lijun An & Fei Yu

  2. Department of Molecular Biology and Centre for Computational and Integrative Biology, Massachusetts General Hospital, Boston, MA, USA

    Yue Wu, Lin Shi & Jen Sheen

  3. Department of Genetics, Harvard Medical School, Boston, MA, USA

    Yue Wu, Lin Shi & Jen Sheen

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Contributions

X.L., J.Sheen and F.Y. conceived the study and designed the experiments. M.J., H.X, R.W., Y.C., N.X., J.Z., J.Shao and Y.Q. performed the experiments. M.J., X.L., Y.W., L.S. and L.A. analysed the data. M.J., X.L., J.Sheen and F.Y. wrote the manuscript with contributions from all authors.

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Correspondence to Fei Yu.

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Jia, M., Liu, X., Xue, H. et al. Noncanonical ATG8–ABS3 interaction controls senescence in plants. Nature Plants 5, 212–224 (2019). https://doi.org/10.1038/s41477-018-0348-x

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