Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

被引:12
作者
Wan, Chen [1 ,2 ]
Zhang, Hui [1 ]
Cheng, Hongying [1 ,2 ]
Sowden, Robert G. [3 ,4 ]
Cai, Wenjuan [5 ]
Jarvis, R. Paul [3 ,4 ]
Ling, Qihua [1 ,2 ,6 ]
机构
[1] Chinese Acad Sci, Inst Plant Physiol & Ecol, CAS Ctr Excellence Mol Plant Sci, Natl Key Lab Plant Mol Genet, Shanghai, Peoples R China
[2] Univ Chinese Acad Sci, Beijing, Peoples R China
[3] Univ Oxford, Dept Plant Sci, Dept Biol, Oxford, England
[4] Univ Oxford, Dept Biol, Sect Mol Plant Biol, Oxford, England
[5] Chinese Acad Sci, Core Facil Ctr, CAS Ctr Excellence Mol Plant Sci, Shanghai, Peoples R China
[6] Chinese Acad Sci, Inst Plant Physiol & Ecol, CAS JIC Ctr Excellence Plant & Microbial Sci CEPAM, Shanghai, Peoples R China
基金
英国科研创新办公室; 中国国家自然科学基金; 英国生物技术与生命科学研究理事会;
关键词
autophagy; chloroplast; NBR1; protein import; stress response; UBIQUITIN-26S PROTEASOME SYSTEM; QUALITY-CONTROL; IN-VIVO; DEGRADATION; BIOGENESIS; MACHINERY; RECEPTOR; PLASTIDS; GROWTH; PHOSPHORYLATION;
D O I
10.15252/embj.2022112534
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the translocon at the outer envelope membrane of chloroplasts (TOC). Previous work has shown that TOC components are regulated by the ubiquitin-proteasome system (UPS) to control the chloroplast proteome, which is crucial for the organelle's function and plant development. Here, we demonstrate that the TOC apparatus is also subject to K63-linked polyubiquitination and regulation by selective autophagy, potentially promoting plant stress tolerance. We identify NBR1 as a selective autophagy adaptor targeting TOC components, and mediating their relocation into vacuoles for autophagic degradation. Such selective autophagy is shown to control TOC protein levels and chloroplast protein import and to influence photosynthetic activity as well as tolerance to UV-B irradiation and heat stress in Arabidopsis plants. These findings uncover the vital role of selective autophagy in the proteolytic regulation of specific chloroplast proteins, and how dynamic control of chloroplast protein import is critically important for plants to cope with challenging environments.
引用
收藏
页数:22
相关论文
共 92 条
  • [1] Acland A, 2013, NUCLEIC ACIDS RES, V41, pD8, DOI [10.1093/nar/gks1189, 10.1093/nar/gkx1095, 10.1093/nar/gkq1172]
  • [2] The Acidic A-Domain of Arabidopsis Toc159 Occurs as a Hyperphosphorylated Protein
    Agne, Birgit
    Andres, Charles
    Montandon, Cyril
    Christ, Bastien
    Ertan, Anouk
    Jung, Friederike
    Infanger, Sibylle
    Bischof, Sylvain
    Baginsky, Sacha
    Kessler, Felix
    [J]. PLANT PHYSIOLOGY, 2010, 153 (03) : 1016 - 1030
  • [3] UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii
    Allorent, Guillaume
    Lefebvre-Legendre, Linnka
    Chappuis, Richard
    Kuntz, Marcel
    Truong, Thuy B.
    Niyogi, Krishna K.
    Ulm, Roman
    Goldschmidt-Clermont, Michel
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2016, 113 (51) : 14864 - 14869
  • [4] Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells
    Andersen, Tonni Grube
    Naseer, Sadaf
    Ursache, Robertas
    Wybouw, Brecht
    Smet, Wouter
    De Rybel, Bert
    Vermeer, Joop E. M.
    Geldner, Niko
    [J]. NATURE, 2018, 555 (7697) : 529 - +
  • [5] Detecting sequence signals in targeting peptides using deep learning
    Armenteros, Jose Juan Almagro
    Salvatore, Marco
    Emanuelsson, Olof
    Winther, Ole
    von Heijne, Gunnar
    Elofsson, Arne
    Nielsen, Henrik
    [J]. LIFE SCIENCE ALLIANCE, 2019, 2 (05)
  • [6] Unusual nucleotide-binding properties of the chloroplast protein import receptor, atToc33
    Aronsson, H
    Combe, J
    Jarvis, P
    [J]. FEBS LETTERS, 2003, 544 (1-3) : 79 - 85
  • [7] A simple method for isolating import-competent Arabidopsis chloroplasts
    Aronsson, H
    Jarvis, P
    [J]. FEBS LETTERS, 2002, 529 (2-3): : 215 - 220
  • [8] Autophagy, plant senescence, and nutrient recycling
    Avila-Ospina, Liliana
    Moison, Michael
    Yoshimoto, Kohki
    Masclaux-Daubresse, Celine
    [J]. JOURNAL OF EXPERIMENTAL BOTANY, 2014, 65 (14) : 3799 - 3811
  • [9] ATI1, a newly identified atg8-interacting protein, binds two different Atg8 homologs
    Avin-Wittenberg, Tamar
    Michaeli, Simon
    Honig, Arik
    Galili, Gad
    [J]. PLANT SIGNALING & BEHAVIOR, 2012, 7 (06) : 685 - 687
  • [10] UniProt: the universal protein knowledgebase in 2021
    Bateman, Alex
    Martin, Maria-Jesus
    Orchard, Sandra
    Magrane, Michele
    Agivetova, Rahat
    Ahmad, Shadab
    Alpi, Emanuele
    Bowler-Barnett, Emily H.
    Britto, Ramona
    Bursteinas, Borisas
    Bye-A-Jee, Hema
    Coetzee, Ray
    Cukura, Austra
    Da Silva, Alan
    Denny, Paul
    Dogan, Tunca
    Ebenezer, ThankGod
    Fan, Jun
    Castro, Leyla Garcia
    Garmiri, Penelope
    Georghiou, George
    Gonzales, Leonardo
    Hatton-Ellis, Emma
    Hussein, Abdulrahman
    Ignatchenko, Alexandr
    Insana, Giuseppe
    Ishtiaq, Rizwan
    Jokinen, Petteri
    Joshi, Vishal
    Jyothi, Dushyanth
    Lock, Antonia
    Lopez, Rodrigo
    Luciani, Aurelien
    Luo, Jie
    Lussi, Yvonne
    Mac-Dougall, Alistair
    Madeira, Fabio
    Mahmoudy, Mahdi
    Menchi, Manuela
    Mishra, Alok
    Moulang, Katie
    Nightingale, Andrew
    Oliveira, Carla Susana
    Pundir, Sangya
    Qi, Guoying
    Raj, Shriya
    Rice, Daniel
    Lopez, Milagros Rodriguez
    Saidi, Rabie
    Sampson, Joseph
    [J]. NUCLEIC ACIDS RESEARCH, 2021, 49 (D1) : D480 - D489