Control of retrograde signalling by protein import and cytosolic folding stress.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
05 2019
05 2019
Historique:
received:
02
07
2018
accepted:
22
03
2019
pubmed:
8
5
2019
medline:
14
6
2019
entrez:
8
5
2019
Statut:
ppublish
Résumé
Communication between organelles and the nucleus is essential for fitness and survival. Retrograde signals are cues emitted from the organelles to regulate nuclear gene expression. GENOMES UNCOUPLED1 (GUN1), a protein of unknown function, has emerged as a central integrator, participating in multiple retrograde signalling pathways that collectively regulate the nuclear transcriptome. Here, we show that GUN1 regulates chloroplast protein import through interaction with the import-related chaperone cpHSC70-1. We demonstrated that overaccumulation of unimported precursor proteins (preproteins) in the cytosol causes a GUN phenotype in the wild-type background and enhances the GUN phenotype of the gun1 mutant. Furthermore, we identified the cytosolic HSP90 chaperone complex, induced by overaccumulated preproteins, as a central regulator of photosynthetic gene expression that determines the expression of the GUN phenotype. Taken together, our results suggest a model in which protein import capacity, folding stress and the cytosolic HSP90 complex control retrograde communication.
Identifiants
pubmed: 31061535
doi: 10.1038/s41477-019-0415-y
pii: 10.1038/s41477-019-0415-y
doi:
Substances chimiques
Arabidopsis Proteins
0
DNA-Binding Proteins
0
GUN1 protein, Arabidopsis
0
HSC70 Heat-Shock Proteins
0
HSP90 Heat-Shock Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
525-538Références
Bradbeer, J. W., Atkinson, Y. E., Borner, T. & Hagemann, R. Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesized RNA. Nature 279, 816–817 (1979).
doi: 10.1038/279816a0
Ramel, F. et al. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc. Natl Acad. Sci. USA 109, 5535–5540 (2012).
doi: 10.1073/pnas.1115982109
Estavillo, G. M. et al. Evidence for a SAL1–PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23, 3992–4012 (2011).
doi: 10.1105/tpc.111.091033
Xiao, Y. M. et al. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149, 1525–1535 (2012).
doi: 10.1016/j.cell.2012.04.038
Woodson, J. D., Perez-Ruiz, J. M. & Chory, J. Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr. Biol. 21, 897–903 (2011).
doi: 10.1016/j.cub.2011.04.004
Fang, X. et al. Chloroplast-to-nucleus signaling regulates microRNA biogenesis in Arabidopsis. Dev. Cell 48, 371–382.e4 (2018).
doi: 10.1016/j.devcel.2018.11.046
Martin, G. et al. Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network. Nat. Commun. 7, 11431 (2016).
doi: 10.1038/ncomms11431
Jarvis, P. & Lopez-Juez, E. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14, 787–802 (2013).
doi: 10.1038/nrm3702
Singh, R., Singh, S., Parihar, P., Singh, V. P. & Prasad, S. M. Retrograde signaling between plastid and nucleus: a review. J. Plant Physiol. 181, 55–66 (2015).
doi: 10.1016/j.jplph.2015.04.001
Susek, R. E., Ausubel, F. M. & Chory, J. Signal-transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene-expression from chloroplast development. Cell 74, 787–799 (1993).
doi: 10.1016/0092-8674(93)90459-4
Koussevitzky, S. et al. Signals from chloroplasts converge to regulate nuclear gene expression. Science 316, 715–719 (2007).
doi: 10.1126/science. 1140516
Mochizuki, N., Brusslan, J. A., Larkin, R., Nagatani, A. & Chory, J. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl Acad. Sci. USA 98, 2053–2058 (2001).
doi: 10.1073/pnas.98.4.2053
Larkin, R. M., Alonso, J. M., Ecker, J. R. & Chory, J. GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299, 902–906 (2003).
doi: 10.1126/science.1079978
Strand, A., Asami, T., Alonso, J., Ecker, J. R. & Chory, J. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421, 79–83 (2003).
doi: 10.1038/nature01204
von Gromoff, E. D., Alawady, A., Meinecke, L., Grimm, B. & Beck, C. F. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell 20, 552–567 (2008).
doi: 10.1105/tpc.107.054650
Moulin, M., McCormac, A. C., Terry, M. J. & Smith, A. G. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc. Natl Acad. Sci. USA 105, 15178–15183 (2008).
doi: 10.1073/pnas.0803054105
La Rocca, N., Rascio, N., Oster, U. & Rudiger, W. Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 213, 101–108 (2001).
doi: 10.1007/s004250000477
Wu, G. Z. et al. Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED 1. Plant Physiol. 176, 2472–2495 (2018).
doi: 10.1104/pp.18.00009
Hernandez-Verdeja, T. & Strand, A. Retrograde signals navigate the path to chloroplast development. Plant Physiol. 176, 967–976 (2018).
doi: 10.1104/pp.17.01299
Ruckle, M. E., DeMarco, S. M. & Larkin, R. M. Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19, 3944–3960 (2007).
doi: 10.1105/tpc.107.054312
Waters, M. T. et al. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21, 1109–1128 (2009).
doi: 10.1105/tpc.108.065250
Kakizaki, T. et al. Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol. 151, 1339–1353 (2009).
doi: 10.1104/pp.109.145987
Tadini, L. et al. GUN1 controls accumulation of the plastid ribosomal protein S1 at the protein level and interacts with proteins involved in plastid protein homeostasis. Plant Physiol. 170, 1817–1830 (2016).
pubmed: 26823545
pmcid: 4775149
Colombo, M., Tadini, L., Peracchio, C., Ferrari, R. & Pesaresi, P. GUN1, a jack-of-all-trades in chloroplast protein homeostasis and signaling. Front. Plant Sci. 7, 1427 (2016).
doi: 10.3389/fpls.2016.01427
Llamas, E., Pulido, P. & Rodriguez-Concepcion, M. Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis. PLoS Genet. 13, e1007022 (2017).
doi: 10.1371/journal.pgen.1007022
Sun, X. et al. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat. Commun. 2, 477 (2011).
doi: 10.1038/ncomms1486
Page, M. T. et al. Seedlings lacking the PTM protein do not show a genomes uncoupled (gun) mutant phenotype. Plant Physiol. 174, 21–26 (2017).
doi: 10.1104/pp.16.01930
Mochizuki, N., Susek, R. & Chory, J. An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol. 112, 1465–1469 (1996).
doi: 10.1104/pp.112.4.1465
Su, P.-H. & Li, H.-M. Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22, 1516–1531 (2010).
doi: 10.1105/tpc.109.071415
Flores-Pérez, U. et al. Functional analysis of the Hsp93/ClpC chaperone at the chloroplast envelope. Plant Physiol. 170, 147–162 (2016).
doi: 10.1104/pp.15.01538
Shi, L. X. & Theg, S. M. A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22, 205–220 (2010).
doi: 10.1105/tpc.109.071464
Liu, L., McNeilage, R. T., Shi, L. X. & Theg, S. M. ATP requirement for chloroplast protein import is set by the Km for ATP hydrolysis of stromal Hsp70 in Physcomitrella patens. Plant Cell 26, 1246–1255 (2014).
doi: 10.1105/tpc.113.121822
Nielsen, E., Akita, M., Davila-Aponte, J. & Keegstra, K. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16, 935–946 (1997).
doi: 10.1093/emboj/16.5.935
Huang, P.-K., Chan, P.-T., Su, P.-H., Chen, L.-J. & Li, H.-M. Chloroplast Hsp93 directly binds to transit peptides at an early stage of the preprotein import process. Plant Physiol. 170, 857–866 (2016).
doi: 10.1104/pp.15.01830
Kubis, S. et al. The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 15, 1859–1871 (2003).
doi: 10.1105/tpc.012955
Lee, S. et al. Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin–26S proteasome system in Arabidopsis. Plant Cell 21, 3984–4001 (2009).
doi: 10.1105/tpc.109.071548
Fellerer, C., Schweiger, R., Schongruber, K., Soll, J. & Schwenkert, S. Cytosolic HSP90 cochaperones HOP and FKBP interact with freshly synthesized chloroplast preproteins of Arabidopsis. Mol. Plant 4, 1133–1145 (2011).
doi: 10.1093/mp/ssr037
Wrobel, L. et al. Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol. Nature 524, 485–488 (2015).
doi: 10.1038/nature14951
Weidberg, H. & Amon, A. MitoCPR-A surveillance pathway that protects mitochondria in response to protein import stress. Science 360, eaan4146 (2018).
doi: 10.1126/science.aan4146
Kovacheva, S., Bedard, J., Wardle, A., Patel, R. & Jarvis, P. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J. 50, 364–379 (2007).
doi: 10.1111/j.1365-313X.2007.03060.x
Zhao, X., Huang, J. & Chory, J. genome uncoupled1 mutants are hypersensitive to norflurazon and lincomycin. Plant Physiol. 178, 960–964 (2018).
doi: 10.1104/pp.18.00772
Kimura, Y., Yahara, I. & Lindquist, S. Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 268, 1362–1365 (1995).
doi: 10.1126/science.7761857
Cutforth, T. & Rubin, G. M. Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 77, 1027–1036 (1994).
doi: 10.1016/0092-8674(94)90442-1
Zhang, X. C., Millet, Y. A., Cheng, Z., Bush, J. & Ausubel, F. M. Jasmonate signalling in Arabidopsis involves SGT1b–HSP70–HSP90 chaperone complexes. Nat. Plants 1, 15049 (2015).
doi: 10.1038/nplants.2015.49
Wang, R. H. et al. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat. Commun. 7, 10269 (2016).
doi: 10.1038/ncomms10269
Kindgren, P., Noren, L., Lopez Jde, D., Shaikhali, J. & Strand, A. Interplay between heat shock protein 90 and HY5 controls PhANG expression in response to the GUN5 plastid signal. Mol. Plant 5, 901–913 (2012).
doi: 10.1093/mp/ssr112
Kindgren, P. et al. A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress. Physiol. Plant 141, 310–320 (2011).
doi: 10.1111/j.1399-3054.2010.01440.x
Cardamone, M. D. et al. Mitochondrial retrograde signaling in mammals is mediated by the transcriptional cofactor GPS2 via direct mitochondria-to-nucleus translocation. Mol. Cell 69, 757–772 (2018).
doi: 10.1016/j.molcel.2018.01.037
Quiros, P. M., Mottis, A. & Auwerx, J. Mitonuclear communication in homeostasis and stress. Nat. Rev. Mol. Cell Biol. 17, 213–226 (2016).
doi: 10.1038/nrm.2016.23
Chan, K. X., Phua, S. Y., Crisp, P., McQuinn, R. & Pogson, B. J. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67, 25–53 (2016).
doi: 10.1146/annurev-arplant-043015-111854
Wang, X. & Chen, X. J. A cytosolic network suppressing mitochondria-mediated proteostatic stress and cell death. Nature 524, 481–484 (2015).
doi: 10.1038/nature14859
Jarvis, P. et al. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282, 100–103 (1998).
doi: 10.1126/science.282.5386.100
Huang, W., Ling, Q., Bedard, J., Lilley, K. & Jarvis, P. In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol. 157, 147–159 (2011).
doi: 10.1104/pp.111.181891
Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant 15, 473–497 (1962).
doi: 10.1111/j.1399-3054.1962.tb08052.x
Azimzadeh, J. et al. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20, 2146–2159 (2008).
doi: 10.1105/tpc.107.056812
Grefen, C. et al. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355–365 (2010).
doi: 10.1111/j.1365-313X.2010.04322.x
Scharff, L. B. & Koop, H. U. Linear molecules of tobacco ptDNA end at known replication origins and additional loci. Plant Mol. Biol. 62, 611–621 (2006).
doi: 10.1007/s11103-006-9042-x
Zoschke, R., Watkins, K. P. & Barkan, A. A rapid ribosome profiling method elucidates chloroplast ribosome behavior in vivo. Plant Cell 25, 2265–2275 (2013).
doi: 10.1105/tpc.113.111567
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001).
doi: 10.1093/nar/29.9.e45
Cahoon, E. B., Shanklin, J. & Ohlrogge, J. B. Expression of a coriander desaturase results in petroselinic acid production in transgenic tobacco. Proc. Natl Acad. Sci. USA 89, 11184–11188 (1992).
doi: 10.1073/pnas.89.23.11184
Czarnecki, O. et al. An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23, 4476–4491 (2011).
doi: 10.1105/tpc.111.086421
Barkan, A. Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Methods Enzymol. 297, 38–57 (1998).
doi: 10.1016/S0076-6879(98)97006-9
Aronsson, H. & Jarvis, R. P. Rapid isolation of Arabidopsis chloroplasts and their use for in vitro protein import assays. Methods Mol. Biol. 774, 281–305 (2011).
doi: 10.1007/978-1-61779-234-2_17
Mou, Z., He, Y., Dai, Y., Liu, X. & Li, J. Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12, 405–418 (2000).
doi: 10.1105/tpc.12.3.405
Walz, C., Juenger, M., Schad, M. & Kehr, J. Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J. 31, 189–197 (2002).
doi: 10.1046/j.1365-313X.2002.01348.x
Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
doi: 10.1038/nbt.1511
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
doi: 10.1038/nmeth.3901
Patton, D. A. et al. An embryo-defective mutant of arabidopsis disrupted in the final step of biotin synthesis. Plant Physiol. 116, 935–946 (1998).
doi: 10.1104/pp.116.3.935
Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents: verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394 (1989).
doi: 10.1016/S0005-2728(89)80347-0
Moran, R. Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiol. 69, 1376–1381 (1982).
doi: 10.1104/pp.69.6.1376
Froehlich, J. Studying Arabidopsis envelope protein localization and topology using thermolysin and trypsin proteases. Methods Mol. Biol. 774, 351–367 (2011).
doi: 10.1007/978-1-61779-234-2_21
Queitsch, C., Sangster, T. A. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618–624 (2002).
doi: 10.1038/nature749
Stebbins, C. E. et al. Crystal structure of an Hsp90–geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239–250 (1997).
doi: 10.1016/S0092-8674(00)80203-2
Massey, A. J. et al. A novel, small molecule inhibitor of Hsc70/Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother. Pharmacol. 66, 535–545 (2010).
doi: 10.1007/s00280-009-1194-3
Balaburski, G. M. et al. A modified HSP70 inhibitor shows broad activity as an anticancer agent. Mol. Cancer Res. 11, 219–229 (2013).
doi: 10.1158/1541-7786.MCR-12-0547-T
Cho, H. J. et al. A small molecule that binds to an ATPase domain of Hsc70 promotes membrane trafficking of mutant cystic fibrosis transmembrane conductance regulator. J. Am. Chem. Soc. 133, 20267–20276 (2011).
doi: 10.1021/ja206762p