title: Heat Shock Protein HSP101 Affects the Release of Ribosomal Protein mRNAs for Recovery after Heat Shock.
abstract: Heat shock (HS) is known to have a profound impact on gene expression at different levels, such as inhibition of protein synthesis, in which HS blocks translation initiation and induces the sequestration of mRNAs into stress granules (SGs) or P-bodies for storage and/or decay. SGs prevent the degradation of the stored mRNAs, which can be reengaged into translation in the recovery period. However, little is known on the mRNAs stored during the stress, how these mRNAs are released from SGs afterward, and what the functional importance is of this process. In this work, we report that ArabidopsisHEAT SHOCK PROTEIN101(HSP101) knockout mutant (hsp101) presented a defect in translation recovery and SG dissociation after HS Using RNA sequencing and RNA immunoprecipitation approaches, we show that mRNAs encoding ribosomal proteins (RPs) were preferentially stored during HS and that these mRNAs were released and translated in an HSP101-dependent manner during recovery. By15N incorporation and polysome profile analyses, we observed that these released mRNAs contributed to the production of new ribosomes to enhance translation. We propose that, after HS, HSP101 is required for the efficient release of RP mRNAs from SGs resulting in a rapid restoration of the translation machinery by producing new RPs.
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.) remy.merret@univ-perp.fr yycharng@sinica.edu.tw.
authors.forename: Rémy
authors.identifier: http://orcid.org/0000-0002-3790-1115
authors.initials: R
authors.lastname: Merret
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Marie-Christine
authors.initials: MC
authors.lastname: Carpentier
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Jean-Jacques
authors.initials: JJ
authors.lastname: Favory
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Claire
authors.initials: C
authors.lastname: Picart
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Julie
authors.initials: J
authors.lastname: Descombin
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Cécile
authors.initials: C
authors.lastname: Bousquet-Antonelli
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Pascal
authors.initials: P
authors.lastname: Tillard
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Laurence
authors.identifier: http://orcid.org/0000-0003-0785-3893
authors.initials: L
authors.lastname: Lejay
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.).|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.).|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.).
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Deragon
authors.affiliation: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan 11529, Republic of China (R.M., Y.-y.C.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|CNRS-LGDP UMR 5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Université de Perpignan Via Domitia, LGDP-UMR5096, 66860 Perpignan, France (R.M., M.-C.C., J.-J.F., C.P., J.D., C.B.-A., J.-M.D.); remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes 'Claude Grignon,' UMR CNRS/INRA/SupAgro/UM2, 34060 Montpellier cedex, France (P.T., L.L.); and remy.merret@univ-perp.fr yycharng@sinica.edu.tw.|Institut Universitaire de France, 1 rue Descartes, 75231 Paris cedex 05, France (J.-M.D.) remy.merret@univ-perp.fr yycharng@sinica.edu.tw.
authors.forename: Yee-Yung
authors.identifier: http://orcid.org/0000-0002-9107-3955
authors.initials: YY
authors.lastname: Charng
mesh_terms: D003594:Cytoplasmic Granules / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D055786:Gene Knockout Techniques; D018869:Heat-Shock Response / Q000235:genetics*; D009154:Mutation / Q000235:genetics; D010940:Plant Proteins / Q000378:metabolism*; D011132:Polyribosomes / Q000378:metabolism; D014176:Protein Biosynthesis; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012269:Ribosomal Proteins / Q000235:genetics* / Q000378:metabolism; D012270:Ribosomes / Q000378:metabolism; D014157:Transcription Factors / Q000378:metabolism*; D014158:Transcription, Genetic
chemical_list: C115569:HSP101 protein, plant; D010940:Plant Proteins; D012333:RNA, Messenger; D012269:Ribosomal Proteins; D014157:Transcription Factors