J-like protein family of Arabidopsis thaliana: the enigmatic cousins of J-domain proteins.
Abiotic and biotic stress
Arabidopsis thaliana
Hsp70:JDP machinery
J-domain proteins
J-like proteins
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
27
11
2021
accepted:
26
02
2022
pubmed:
16
3
2022
medline:
23
6
2022
entrez:
15
3
2022
Statut:
ppublish
Résumé
J-like proteins (JLPs) are emerging as ancillaries to the cellular chaperone network. They modulate functions of Hsp70:J-domain protein (JDP) systems in novel ways thereby having key roles in diverse plant processes. J-domain proteins (JDPs) form an obligate co-chaperone partnership with Hsp70s with their highly conserved J-domain to steer protein quality control processes in the cell. The HPD motif between helix II and helix III of the J-domain is crucial for JDP's interaction with Hsp70s. According to the most recent classification, J-like proteins (JLPs) form an extended class of the JDP family possessing a degenerate J-domain with the HPD motif non-conservatively replaced by other amino acid residues and hence are not able to interact with Hsp70s. Considering this most updated and acceptable JLP classification, we identified 21 JLPs in Arabidopsis thaliana that share a structurally conserved J-like domain (JLD), but lack the HPD motif. Analysis of publicly available gene expression data as well as real-time quantitative PCR performed for a few selected JLPs implicated some of these proteins in growth, development and stress response. Here, we summarize the current state of knowledge on plant JLPs and their involvement in vital plant cellular/metabolic processes, including chloroplast division, mitochondrial protein import and flowering. Finally, we propose possible modes of action for these highly elusive proteins and other DnaJ-related proteins (DNAJRs) in regulating the Hsp70 chaperone network.
Identifiants
pubmed: 35290497
doi: 10.1007/s00299-022-02857-y
pii: 10.1007/s00299-022-02857-y
doi:
Substances chimiques
Arabidopsis Proteins
0
HSP40 Heat-Shock Proteins
0
HSP70 Heat-Shock Proteins
0
Molecular Chaperones
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1343-1355Subventions
Organisme : Science and Engineering Research Board
ID : SERB-EMR/2015/001213
Organisme : Department of Biotechnology , Ministry of Science and Technology
ID : BT/PR12149/BRB/10/1348/2014
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Ajit Tamadaddi C, Sahi C (2016) J domain independent functions of J proteins. Cell Stress Chaperones 21:563–570
pubmed: 27145962
pmcid: 4908003
doi: 10.1007/s12192-016-0697-1
Ajjawi I, Coku A, Froehlich JE, Yang Y, Osteryoung KW, Benning C, Last RL (2011) A J-like protein influences fatty acid composition of chloroplast lipids in Arabidopsis. PLoS ONE 6:e25368
pubmed: 22028775
pmcid: 3196505
doi: 10.1371/journal.pone.0025368
Berardini TZ, Reiser L, Li D, Mezheritsky Y, Muller R, Strait E, Huala E (2015) The Arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis (new York, NY, 2000) 53:474–485
doi: 10.1002/dvg.22877
Blatch GL, Lässle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21:932–939
pubmed: 10517866
doi: 10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N
Cao M, Wei C, Zhao L, Wang J, Jia Q, Wang X, Jin Q, Deng T (2014) DnaJA1/Hsp40 is co-opted by influenza A virus to enhance its viral RNA polymerase activity. J Virol 88:14078–14089
pubmed: 25253355
pmcid: 4249161
doi: 10.1128/JVI.02475-14
Chen X, Ghazanfar B, Khan AR, Hayat S, Cheng Z (2013) Comparative analysis of putative orthologues of mitochondrial import motor subunit: Pam18 and Pam16 in plants. PLoS ONE 8:e78400
pubmed: 24194927
pmcid: 3806816
doi: 10.1371/journal.pone.0078400
Ciou HS, Tsai YL, Chiu CC (2020) Arabidopsis chloroplast J protein DJC75/CRRJ mediates nitrate-promoted seed germination in the dark. Ann Bot 125:1091–1099
pubmed: 32157271
pmcid: 7262469
doi: 10.1093/aob/mcaa040
Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890
pubmed: 2849754
pmcid: 338945
doi: 10.1093/nar/16.22.10881
D’Silva PR, Schilke B, Walter W, Craig EA (2005) Role of Pam16’s degenerate J domain in protein import across the mitochondrial inner membrane. Proc Natl Acad Sci USA 102:12419–12424
pubmed: 16105940
pmcid: 1194952
doi: 10.1073/pnas.0505969102
D’Silva PR, Schilke B, Hayashi M, Craig EA (2008) Interaction of the J-protein heterodimer Pam18/Pam16 of the mitochondrial import motor with the translocon of the inner membrane. Mol Biol Cell 19:424–432
pubmed: 18003975
pmcid: 2174176
doi: 10.1091/mbc.e07-08-0748
Ducett JK, Peterson FC, Hoover LA, Prunuske AJ, Volkman BF, Craig EA (2013) Unfolding of the C-terminal domain of the J-protein Zuo1 releases autoinhibition and activates Pdr1-dependent transcription. J Mol Biol 425:19–31
pubmed: 23036859
doi: 10.1016/j.jmb.2012.09.020
Feng P, Lin H, Chen W, Zuo Y (2014) Predicting the types of J-proteins using clustered amino acids. BioMed Res Int 2014:935719
pubmed: 24804260
pmcid: 3996952
Finka A, Mattoo RU, Goloubinoff P (2011) Meta-analysis of heat- and chemically upregulated chaperone genes in plant and human cells. Cell Stress Chaperones 16:15–31
pubmed: 20694844
doi: 10.1007/s12192-010-0216-8
Frazier AE, Dudek J, Guiard B, Voos W, Li Y, Lind M, Meisinger C, Geissler A, Sickmann A, Meyer HE, Bilanchone V, Cumsky MG, Truscott KN, Pfanner N, Rehling P (2004) Pam16 has an essential role in the mitochondrial protein import motor. Nat Struct Mol Biol 11:226–233
pubmed: 14981507
doi: 10.1038/nsmb735
Gillis J, Schipper-Krom S, Juenemann K, Gruber A, Coolen S, van den Nieuwendijk R, van Veen H, Overkleeft H, Goedhart J, Kampinga HH, Reits EA (2013) The DNAJB6 and DNAJB8 protein chaperones prevent intracellular aggregation of polyglutamine peptides. J Biol Chem 288:17225–17237
pubmed: 23612975
pmcid: 3682527
doi: 10.1074/jbc.M112.421685
Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470
pubmed: 18812496
pmcid: 2570736
doi: 10.1105/tpc.108.061440
Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711
pubmed: 19453460
doi: 10.1111/j.1365-313X.2009.03905.x
Goodacre NF, Gerloff DL, Uetz P (2013) Protein domains of unknown function are essential in bacteria. Mbio 5:e00744-00713
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723
pubmed: 9504803
doi: 10.1002/elps.1150181505
Hageman J, Kampinga HH (2009) Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library. Cell Stress Chaperones 14:1–21
pubmed: 18686016
doi: 10.1007/s12192-008-0060-2
Harris CJ, Scheibe M, Wongpalee SP, Liu W, Cornett EM, Vaughan RM, Li X, Chen W, Xue Y, Zhong Z, Yen L, Barshop WD, Rayatpisheh S, Gallego-Bartolome J, Groth M, Wang Z, Wohlschlegel JA, Du J, Rothbart SB, Butter F, Jacobsen SE (2018) A DNA methylation reader complex that enhances gene transcription. Science 362:1182–1186
pubmed: 30523112
pmcid: 6353633
doi: 10.1126/science.aar7854
Hennessy F, Cheetham ME, Dirr HW, Blatch GL (2000) Analysis of the levels of conservation of the J domain among the various types of DnaJ-like proteins. Cell Stress Chaperones 5:347–358
pubmed: 11048657
pmcid: 312864
doi: 10.1379/1466-1268(2000)005<0347:AOTLOC>2.0.CO;2
Hennessy F, Nicoll WS, Zimmermann R, Cheetham ME, Blatch GL (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci 14:1697–1709
pubmed: 15987899
pmcid: 2253343
doi: 10.1110/ps.051406805
Huang Y, Chen X, Liu Y, Roth C, Copeland C, McFarlane HE, Huang S, Lipka V, Wiermer M, Li X (2013) Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity. Nat Commun 4:2558
pubmed: 24153405
doi: 10.1038/ncomms3558
Jiang Y, Rossi P, Kalodimos CG (2019) Structural basis for client recognition and activity of Hsp40 chaperones. Science 365:1313–1319
pubmed: 31604242
pmcid: 7023980
doi: 10.1126/science.aax1280
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592
pubmed: 20651708
pmcid: 3003299
doi: 10.1038/nrm2941
Kampinga HH, Andreasson C, Barducci A, Cheetham ME, Cyr D, Emanuelsson C, Genevaux P, Gestwicki JE, Goloubinoff P, Huerta-Cepas J, Kirstein J, Liberek K, Mayer MP, Nagata K, Nillegoda NB, Pulido P, Ramos C, De Los RP, Rospert S, Rosenzweig R, Sahi C, Taipale M, Tomiczek B, Ushioda R, Young JC, Zimmermann R, Zylicz A, Zylicz M, Craig EA, Marszalek J (2019) Function, evolution, and structure of J-domain proteins. Cell Stress Chaperones 24:7–15
pubmed: 30478692
doi: 10.1007/s12192-018-0948-4
Kawai-Yamada M, Saito Y, Jin L, Ogawa T, Kim KM, Yu LH, Tone Y, Hirata A, Umeda M, Uchimiya H (2005) A novel Arabidopsis gene causes Bax-like lethality in Saccharomyces cerevisiae. J Biol Chem 280:39468–39473
pubmed: 16192270
doi: 10.1074/jbc.M509632200
Knox C, Luke GA, Blatch GL, Pesce E-R (2011) Heat shock protein 40 (Hsp40) plays a key role in the virus life cycle. Virus Res 160:15–24
pubmed: 21729725
doi: 10.1016/j.virusres.2011.06.013
Kradolfer D, Wolff P, Jiang H, Siretskiy A, Köhler C (2013) An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev Cell 26:525–535
pubmed: 24012484
doi: 10.1016/j.devcel.2013.08.006
Kufareva I, Abagyan R (2012) Methods of protein structure comparison. Methods Mol Biol 857:231–257
pubmed: 22323224
pmcid: 4321859
doi: 10.1007/978-1-61779-588-6_10
Lee JY, Lee HS, Song JY, Jung YJ, Reinbothe S, Park YI, Lee SY, Pai HS (2013) Cell growth defect factor1/chaperone-like protein of POR1 plays a role in stabilization of light-dependent protochlorophyllide oxidoreductase in Nicotiana benthamiana and Arabidopsis. Plant Cell 25:3944–3960
pubmed: 24151298
pmcid: 3877821
doi: 10.1105/tpc.113.111096
Lee H-S, Choi I, Jeon Y, Ahn H-K, Cho H, Kim J, Kim J-H, Lee J-M, Lee S, Bünting J, Seo DH, Lee T, Lee D-H, Lee I, Oh M-H, Kim T-W, Belkhadir Y, Pai H-S (2021) Chaperone-like protein DAY plays critical roles in photomorphogenesis. Nat Commun 12:4194
pubmed: 34234144
pmcid: 8263706
doi: 10.1038/s41467-021-24446-5
Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493-d496
pubmed: 29040681
doi: 10.1093/nar/gkx922
Li Y, Dudek J, Guiard B, Pfanner N, Rehling P, Voos W (2004) The presequence translocase-associated protein import motor of mitochondria. Pam16 functions in an antagonistic manner to Pam18. J Biol Chem 279:38047–38054
pubmed: 15218029
doi: 10.1074/jbc.M404319200
Liu Q, Liang C, Zhou L (2020) Structural and functional analysis of the Hsp70/Hsp40 chaperone system. Protein Sci 29:378–390
pubmed: 31509306
doi: 10.1002/pro.3725
Lu Z, Cyr DM (1998) The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J Biol Chem 273:5970–5978
pubmed: 9488737
doi: 10.1074/jbc.273.10.5970
Martin JL (1995) Thioredoxin—a fold for all reasons. Structure 3:245–250
pubmed: 7788290
doi: 10.1016/S0969-2126(01)00154-X
Mehawej C, Delahodde A, Legeai-Mallet L, Delague V, Kaci N, Desvignes JP, Kibar Z, Capo-Chichi JM, Chouery E, Munnich A, Cormier-Daire V, Mégarbané A (2014) The impairment of MAGMAS function in human is responsible for a severe skeletal dysplasia. PLoS Genet 10:e1004311
pubmed: 24786642
pmcid: 4006740
doi: 10.1371/journal.pgen.1004311
Mokranjac D, Sichting M, Popov-Celeketic D, Berg A, Hell K, Neupert W (2005) The import motor of the yeast mitochondrial TIM23 preprotein translocase contains two different J proteins, Tim14 and Mdj2. J Biol Chem 280:31608–31614
pubmed: 16027163
doi: 10.1074/jbc.M502397200
Mokranjac D, Bourenkov G, Hell K, Neupert W, Groll M (2006) Structure and function of Tim14 and Tim16, the J and J-like components of the mitochondrial protein import motor. EMBO J 25:4675–4685
pubmed: 16977310
pmcid: 1590002
doi: 10.1038/sj.emboj.7601334
Nillegoda NB, Kirstein J, Szlachcic A, Berynskyy M, Stank A, Stengel F, Arnsburg K, Gao X, Scior A, Aebersold R, Guilbride DL, Wade RC, Morimoto RI, Mayer MP, Bukau B (2015) Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation. Nature 524:247–251
pubmed: 26245380
pmcid: 4830470
doi: 10.1038/nature14884
Nillegoda NB, Stank A, Malinverni D, Alberts N, Szlachcic A, Barducci A, De Los RP, Wade RC, Bukau B (2017) Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes. Elife 6:e24560
pubmed: 28504929
pmcid: 5542770
doi: 10.7554/eLife.24560
Park HY, Lee SY, Seok HY, Kim SH, Sung ZR, Moon YH (2011) EMF1 interacts with EIP1, EIP6 or EIP9 involved in the regulation of flowering time in Arabidopsis. Plant Cell Physiol 52:1376–1388
pubmed: 21700722
doi: 10.1093/pcp/pcr084
Pulido P, Leister D (2018) Novel DNAJ-related proteins in Arabidopsis thaliana. New Phytol 217:480–490
pubmed: 29271039
doi: 10.1111/nph.14827
Rajan VB, D’Silva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genomics 9:433–446
pubmed: 19633874
doi: 10.1007/s10142-009-0132-0
Rebeaud ME, Mallik S, Goloubinoff P, Tawfik DS (2021) On the evolution of chaperones and cochaperones and the expansion of proteomes across the Tree of Life. Proc Natl Acad Sci 118:e2020885118
pubmed: 34001607
pmcid: 8166112
doi: 10.1073/pnas.2020885118
Ratheesh KR, Nagarajan NS, Arunraj SP, Sinha D, Rajan VBV, Esthaki VK, D’Silva P (2012) HSPIR: a manually annotated heat shock protein information resource. Bioinformatics 28:2853–2855
doi: 10.1093/bioinformatics/bts520
Sagarika P, Dobriyal N, Sahi C (2021) Dosage sensitivity of JDPs, a valuable tool for understanding their function: a case study on Caj1 overexpression-mediated filamentous growth in budding yeast. Curr Genet
Sahi C, Lee T, Inada M, Pleiss JA, Craig EA (2010) Cwc23, an essential J protein critical for pre-mRNA splicing with a dispensable J domain. Mol Cell Biol 30:33–42
pubmed: 19822657
doi: 10.1128/MCB.00842-09
Sha B, Lee S, Cyr DM (2000) The crystal structure of the peptide-binding fragment from the yeast Hsp40 protein Sis1. Structure 8:799–807
pubmed: 10997899
doi: 10.1016/S0969-2126(00)00170-2
Shen Y, Hendershot LM (2005) ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP’s interactions with unfolded substrates. Mol Biol Cell 16:40–50
pubmed: 15525676
pmcid: 539150
doi: 10.1091/mbc.e04-05-0434
Sinha D, Srivastava S, D’Silva P (2016) Functional diversity of human mitochondrial J-proteins is independent of their association with the inner membrane presequence translocase. J Biol Chem 291:17345–17359
pubmed: 27330077
pmcid: 5016132
doi: 10.1074/jbc.M116.738146
Szabo A, Korszun R, Hartl FU, Flanagan J (1996) A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J 15:408–417
pubmed: 8617216
pmcid: 449956
doi: 10.1002/j.1460-2075.1996.tb00371.x
Tamadaddi C, Sagar V, Verma AK, Afsal F, Sahi C (2021) Expansion of the evolutionarily conserved network of J-domain proteins in the Arabidopsis mitochondrial import complex. Plant Mol Biol 105:385–403
pubmed: 33206359
doi: 10.1007/s11103-020-01095-8
Verges E, Colomina N, Gari E, Gallego C, Aldea M (2007) Cyclin Cln3 is retained at the ER and released by the J chaperone Ydj1 in late G1 to trigger cell cycle entry. Mol Cell 26:649–662
pubmed: 17560371
doi: 10.1016/j.molcel.2007.04.023
Verma AK, Tamadaddi C, Tak Y, Lal SS, Cole SJ, Hines JK, Sahi C (2019) The expanding world of plant J-domain proteins. Crit Rev Plant Sci 38:382–400
pubmed: 33223602
doi: 10.1080/07352689.2019.1693716
Walsh P, Bursac D, Law YC, Cyr D, Lithgow T (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5:567–571
pubmed: 15170475
pmcid: 1299080
doi: 10.1038/sj.embor.7400172
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296-w303
pubmed: 29788355
pmcid: 6030848
doi: 10.1093/nar/gky427
Yamamoto H, Peng L, Fukao Y, Shikanai T (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23:1480–1493
pubmed: 21505067
pmcid: 3101538
doi: 10.1105/tpc.110.080291
Yang C, Compton MM, Yang P (2005) Dimeric novel HSP40 is incorporated into the radial spoke complex during the assembly process in flagella. Mol Biol Cell 16:637–648
pubmed: 15563613
pmcid: 545900
doi: 10.1091/mbc.e04-09-0787
Zhang B, Qiu HL, Qu DH, Ruan Y, Chen DH (2018) Phylogeny-dominant classification of J-proteins in Arabidopsis thaliana and Brassica oleracea. Genome 61:405–415
pubmed: 29620479
doi: 10.1139/gen-2017-0206
Zhou K, Ren Y, Lv J, Wang Y, Liu F, Zhou F, Zhao S, Chen S, Peng C, Zhang X, Guo X, Cheng Z, Wang J, Wu F, Jiang L, Wan J (2013) Young leaf chlorosis 1, a chloroplast-localized gene required for chlorophyll and lutein accumulation during early leaf development in rice. Planta 237:279–292
pubmed: 23053539
doi: 10.1007/s00425-012-1756-1