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J-like protein family of Arabidopsis thaliana: the enigmatic cousins of J-domain proteins

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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.

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References

  • Ajit Tamadaddi C, Sahi C (2016) J domain independent functions of J proteins. Cell Stress Chaperones 21:563–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Blatch GL, Lässle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21:932–939

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Goodacre NF, Gerloff DL, Uetz P (2013) Protein domains of unknown function are essential in bacteria. Mbio 5:e00744-00713

    Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Rossi P, Kalodimos CG (2019) Structural basis for client recognition and activity of Hsp40 chaperones. Science 365:1313–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kufareva I, Abagyan R (2012) Methods of protein structure comparison. Methods Mol Biol 857:231–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493-d496

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Liang C, Zhou L (2020) Structural and functional analysis of the Hsp70/Hsp40 chaperone system. Protein Sci 29:378–390

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Martin JL (1995) Thioredoxin—a fold for all reasons. Structure 3:245–250

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pulido P, Leister D (2018) Novel DNAJ-related proteins in Arabidopsis thaliana. New Phytol 217:480–490

    Article  CAS  PubMed  Google Scholar 

  • Rajan VB, D’Silva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genomics 9:433–446

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We sincerely thank all the laboratory members for their valuable discussions on this manuscript. CT and AV thank the Department of Science and Technology (DST) INSPIRE fellowship for Ph.D. and Kishore Vaigyanik Protsahan Yojana (KVPY) scholarship for undergraduate study and, respectively.

Funding

This work was supported by the Science and Engineering Research Board (SERB-EMR/2015/001213) and Department of Biotechnology, Government of India (BT/PR12149/BRB/10/1348/2014), and intramural funds from IISER Bhopal to CS.

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Authors and Affiliations

  1. Department of Biological Sciences, Indian Institute of Science Education and Research, Bhopal, India

    Chetana Tamadaddi, Amit K. Verma, Avanti Vairagkar, Danish Diwan & Chandan Sahi

  2. Department of Biology, Eberly College of Science, The Pennsylvania State University, University Park, PA, USA

    Chetana Tamadaddi

  3. Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, USA

    Amit K. Verma

  4. School of Biotechnology and Bioinformatics, D Y Patil Deemed to be University, Navi Mumbai, India

    Vyankatesh Zambare

  5. Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Vyankatesh Zambare

  6. Department of Biology, University of Alabama, Birmingham, AL, USA

    Danish Diwan

  7. IISER Bhopal, Room Number 117, AB3, Bhopal Bypass Road, Bhopal, 462066, MP, India

    Chandan Sahi

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  1. Chetana Tamadaddi
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  2. Amit K. Verma
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  3. Vyankatesh Zambare
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  4. Avanti Vairagkar
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  5. Danish Diwan
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  6. Chandan Sahi
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Contributions

CT, AKV, and CS conceived the idea; CT and DD performed the qRT-PCR experiments and analysed the data. AKV, CT, VZ, and AV performed the bioinformatics studies. CT, AKV, VZ, and CS wrote the manuscript.

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Correspondence to Chandan Sahi.

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Communicated by Wusheng Liu.

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Tamadaddi, C., Verma, A.K., Zambare, V. et al. J-like protein family of Arabidopsis thaliana: the enigmatic cousins of J-domain proteins. Plant Cell Rep 41, 1343–1355 (2022). https://doi.org/10.1007/s00299-022-02857-y

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