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Heat Shock Proteins and Plants pp 245–282Cite as

Molecular Chaperones and HSPs in Sugarcane and Eucalyptus

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Part of the book series: Heat Shock Proteins ((HESP,volume 10))

Abstract

The sessile existence of plants makes these organisms more exposed to unfavorable environmental changes than animals and more likely to have evolved sophisticated ways to combat stresses. Therefore, knowledge about the network of molecular chaperones and heat shock proteins (HSPs) in plants is of great interest not only to improve agricultural production but also to enhance our understanding of the cellular protein-folding process. In this chapter we will review the use of bioinformatics to identify and annotate 5′EST-contigs belonging to molecular chaperones within plant genomes, with an emphasis on sugarcane and eucalyptus. The chapter will show that information concerning the diversity and quantity of expressed mRNAs under diverse developmental and environmental conditions has led to new insights on specific proteins’ importance and activities in response to environmental conditions sensed by these organisms. The general findings are as follows: Chaperone and stress-related protein genes are abundantly expressed and have ample diversity. Cytoplasmic chaperones have both higher expression and greater diversity than those from other cellular compartments. Findings regarding cDNA cloning and protein purification and characterization will also be discussed.

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Abbreviations

AUC:

analytical ultracentrifugation

CD:

circular dichroism

HSP:

heat shock protein

SEC-MALS:

size exclusion chromatography coupled to multi-angle light scattering

References

  • Abravaya K, Myers MP, Murphy SP, Morimoto RI (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6:1153–1164

    Article  CAS  PubMed  Google Scholar 

  • Agarwal M, Katiyar-Agarwal S, Sahi C, Gallie DR, Grover A (2001) Arabidopsis thaliana Hsp100 proteins: kith and kin. Cell Stress Chaperones 6:219–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali MM, Roe SM, Vaughan CK, Meyer P, Panaretou B, Piper PW, Prodromou C, Pearl LH (2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440:1013–1017

    Article  CAS  PubMed  Google Scholar 

  • Anckar J, Sistonen L (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80:1089–1115

    Article  CAS  PubMed  Google Scholar 

  • Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230

    Article  CAS  PubMed  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Bakthisaran R, Tangirala R, Rao Ch M (2015) Small heat shock proteins: role in cellular functions and pathology. Biochim Biophys Acta 1854:291–319

    Article  CAS  PubMed  Google Scholar 

  • Baldwin RL (1995) The nature of protein-folding pathways – the classical versus the new view. J Biomol NMR 5:103–109

    Article  CAS  PubMed  Google Scholar 

  • Baldwin RL, Rose GD (2013) Molten globules, entropy-driven conformational change and protein folding. Curr Opin Struct Biol 23:4–10

    Article  CAS  PubMed  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Döring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcriptions factors. J Biosci 29:471–487

    Article  CAS  PubMed  Google Scholar 

  • Barnett ME, Nagy M, Kedzierska S, Zolkiewski M (2005) The amino-terminal domain of ClpB supports binding to strongly aggregated proteins. J Biol Chem 280:34940–34945

    Article  CAS  PubMed  Google Scholar 

  • Barraclough R, Ellis RJ (1980) Protein synthesis in chloroplasts. IX. Assembly of newly- synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts. Biochim Biophys Acta 608:19–31

    Article  CAS  PubMed  Google Scholar 

  • Basha GJ, Friedrich KL, Vierling E (2006) The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J Biol Chem 281:39943–39952

    Article  CAS  PubMed  Google Scholar 

  • Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117

    Article  CAS  PubMed  Google Scholar 

  • Basha E, Jones C, Blackwell AE, Cheng G, Waters ER, Samsel KA, Siddique M, Pett V, Wysocki V, Vierling E (2013) An unusual dimeric small heat shock protein provides insight into the mechanism of this class of chaperones. J Mol Biol 425:1683–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batista FA, Gava LM, Pinheiro GM, Ramos CH, Borges JC (2015) From conformation to interaction: techniques to explore the Hsp70/Hsp90 network. Curr Protein Pept Sci 16:735–753

    Article  CAS  PubMed  Google Scholar 

  • Borges JC, Ramos CH. (2005) Protein folding assisted by chaperones. Protein Pept Lett. 12(3):257–61.

    Google Scholar 

  • Borges JC, Ramos CH (2006) Spectroscopic and thermodynamic measurements of nucleotide-induced changes in the human 70-kDa heat shock cognate protein. Arch Biochem Biophys 452:46–54

    Article  CAS  PubMed  Google Scholar 

  • Borges JC, Ramos CH (2011) Analysis of molecular targets of Mycobacterium tuberculosis by analytical ultracentrifugation. Curr Med Chem 18:1276–1285

    Article  CAS  PubMed  Google Scholar 

  • Borges JC, Peroto MC, Ramos CH (2001) Molecular chaperone genes in the sugarcane expressed sequence database (SUCEST). Genet Mol Biol 24:85–92

    Article  CAS  Google Scholar 

  • Borges JC, Cagliari TC, Ramos CH (2007) Expression and variability of molecular chaperones in the sugarcane expressome. J Plant Physiol 164:505–513

    Article  CAS  PubMed  Google Scholar 

  • Boshoff A (2015) Chaperonin-co-chaperonin interactions. Subcell Biochem 78:153–178

    Article  CAS  PubMed  Google Scholar 

  • Bösl B, Grimminger V, Walter S (2006) The molecular chaperone Hsp104 – a molecular machine for protein disaggregation. J Struct Biol 156:139–148

    Article  PubMed  CAS  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    Article  CAS  PubMed  Google Scholar 

  • Bracher A, Verghese J (2015) GrpE, Hsp110/Grp170, HspBP1/Sil1 and BAG domain proteins: nucleotide exchange factors for Hsp70 molecular chaperones. Subcell Biochem 78:1–33

    Article  CAS  PubMed  Google Scholar 

  • Brandvold KR, Morimoto RI (2015) The chemical biology of molecular chaperones–implications for modulation of proteostasis. J Mol Biol 427:2931–2947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchner J (1999) Hsp90 and co. – a holding for folding. Trends Biochem Sci 24:136–141

    Article  CAS  PubMed  Google Scholar 

  • Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366

    Article  CAS  PubMed  Google Scholar 

  • Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443–451

    Article  CAS  PubMed  Google Scholar 

  • Cagliari TC, Tiroli AO, Borges JC, Ramos CH (2005) Identification and in silico pattern analysis of Eucalyptus expressed sequencing tags (ESTs) enconding molecular chaperones. Genet Mol Biol 28:520–528

    Article  CAS  Google Scholar 

  • Cagliari TC, da Silva VC, Borges JC, Prando A, Tasic L, Ramos CH (2011) Sugarcane Hsp101 is a hexameric chaperone that binds nucleotides. Int J Biol Macromol 49:1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Carroni M, Kummer E, Oguchi Y, Wendler P, Clare DK, Sinning I, Kopp J, Mogk A, Bukau B, Saibil HR (2014) Head-to-tail interactions of the coiled-coil domains regulate ClpB activity and cooperation with Hsp70 in protein disaggregation. Elife 3:e02481

    Article  PubMed  PubMed Central  Google Scholar 

  • Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat shock protein family and structure predictions of the conserved “α-crystallin-domain”. J Mol Evol 40:238–248

    Article  CAS  PubMed  Google Scholar 

  • Chadli A, Bouhouche I, Sullivan W, Stensgard B, McMahon N, Catelli MG, Toft DO (2000) Dimerization and N-terminal domain proximity underlie the function of molecular chaperone heat shock protein 90. Proc Natl Acad Sci U S A 97:12524–12529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clerico EM, Tilitsky JM, Meng W, Gierasch LM (2015) How HSP70 molecular machines interact with their substrates to mediate diverse physiological functions. J Mol Biol 427:1575–1588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa DHA, Ramos CH (2009) The use of circular dichroism spectroscopy to study protein folding, form and function. Afr J Biochem Res 3:164–173

    CAS  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163

    Article  PubMed  PubMed Central  Google Scholar 

  • Cyr DM, Ramos CH (2015) Specification of Hsp70 function by type I and type II Hsp40. Subcell Biochem 78:91–102

    Article  CAS  PubMed  Google Scholar 

  • da Silva KP, Borges JC (2011) The molecular chaperone Hsp70 family members function by a bidirectional heterotrophic allosteric mechanism. Protein Pept Lett 18:132–142

    Article  PubMed  Google Scholar 

  • da Silva VC, Ramos CH (2012) The network interaction of human 90 kDa heat shock protein Hsp90: A target for cancer therapeutics. J Proteome 75:2790–2802

    Article  CAS  Google Scholar 

  • da Silva VC, Cagliari TC, Lima TB, Gozzo FC, Ramos CH (2013) Conformational and functional studies of a cytosolic 90 kDa heat shock protein Hsp90 from sugarcane. Plant Physiol Biochem 68:16–22

    Article  PubMed  CAS  Google Scholar 

  • Douglas PM, Summers DW, Cyr DM (2009) Molecular chaperones antagonize proteotoxicity by differentially modulating protein aggregation pathways. Prion 3:51–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle SM, Genest O, Wickner S (2013) Protein rescue from aggregates by powerful molecular chaperone machines. Nat Rev Mol Cell Biol 14:617–629

    Article  CAS  PubMed  Google Scholar 

  • Duncan EJ, Cheetham ME, Chapple JP, van der Spuy J (2015) The role of HSP70 and its co- chaperones in protein misfolding, aggregation and disease. Subcell Biochem 78:243–273

    Article  CAS  PubMed  Google Scholar 

  • Edward JT (1970) Molecular volumes and the Stokes-Einstein Equation. J Chem Educ 47:261–270

    Article  CAS  Google Scholar 

  • Ferreira ST, De Felice FG (2001) PABMB lecture. Protein dynamics, folding and misfolding: from basic physical chemistry to human conformational diseases. FEBS Lett 498:129–134

    Article  CAS  PubMed  Google Scholar 

  • Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346:623–628

    Article  CAS  PubMed  Google Scholar 

  • Fleckenstein T, Kastenmüller A, Stein ML, Peters C, Daake M, Krause M, Weinfurtner D, Haslbeck M, Weinkauf S, Groll M, Buchner J (2015) The chaperone activity of the development small heat shock protein Sip1 is regulated by pH-dependent conformational changes. Mol Cell 58:1067–1078

    Article  CAS  PubMed  Google Scholar 

  • Freeman BC, Morimoto RI (1996) The human cytosolic molecular chaperones HSP90, HSP70 (HSC70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 15:2969–2979

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujimoto M, Nakai A (2010) The heat shock factor family and adaptation to proteotoxic stress. FEBS J 277:4112–4125

    Article  CAS  PubMed  Google Scholar 

  • Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44:1588–1592

    Article  CAS  PubMed  Google Scholar 

  • Gava L, Ramos CH (2009) Human 90 kDa heat shock protein Hsp90 as a target for cancer therapeutics. Curr Chem Biol 3:330–341

    Article  CAS  Google Scholar 

  • Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73–82

    Article  CAS  PubMed  Google Scholar 

  • Goloubinoff P (2014) Recent and future grand challenges in protein folding, misfolding, and degradation. Front Mol Biosci 1:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gusev NB, Bogatcheva NV, Marston SB (2002) Structure and properties of small heat shock proteins (sHsp) and their interaction with cytoskeleton proteins. Biochemistry (Mosc) 67:511–519

    Article  CAS  Google Scholar 

  • Haley DA, Horwitz J, Stewart PL (1998) The small heat-shock protein, alphaB-crystallin, has a variable quaternary structure. J Mol Biol 277:27–35

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574–581

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Martin J, Neupert W (1992) Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Biophys Biomol Struct 21:293–322

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck M, Vierling E (2015) A first of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427:1537–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Buchner J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18:6744–6751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haslbeck M, Braun N, Stromer T, Richter B, Model N, Weinkauf S, Buchner J (2004) Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23:638–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haslbeck M, Miess A, Stromer T, Walter S, Buchner J (2005) Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem 280:23861–23868

    Article  CAS  PubMed  Google Scholar 

  • Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:49–384

    Article  Google Scholar 

  • Hietakangas V, Ahlskog JK, Jakobsson AM, Hellesuo M, Sahlberg NM, Holmberg CI, Mikhailov A, Palvimo JJ, Pirkkala L, Sistonen L (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol Cell Biol 23:2953–2968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill JE, Hemmingsen SM (2001) Arabidopsis thaliana type I and II chaperonins. Cell Stress Chaperones 6:190–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodson S, Marshall JJ, Burston SG (2012) Mapping the road to recovery: the ClpB/Hsp104 molecular chaperone. J Struct Biol 179:161–171

    Article  CAS  PubMed  Google Scholar 

  • Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Article  CAS  PubMed  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Jackson SE (2013) Hsp90: structure and function. Top Curr Chem 328:155–240

    Article  CAS  PubMed  Google Scholar 

  • Jakob U, Lilie H, Meyer I, Buchner J (1995) Transient interaction of Hsp90 with early unfolding intermediates of citrate synthaseeimplications for heat shock in vivo. J Biol Chem 270:7288–7294

    Article  CAS  PubMed  Google Scholar 

  • Kakkar VV, Prins LC, Kampinga HH (2012) DNAJ proteins and protein aggregation diseases. Curr Top Med Chem 12:2479–2490

    Article  CAS  PubMed  Google Scholar 

  • Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394:595–599

    Article  CAS  PubMed  Google Scholar 

  • Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82:323–355

    Article  CAS  PubMed  Google Scholar 

  • Knowles TP, Vendruscolo M, Dobson CM (2014) The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 15:384–396

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landreh M, Rising A, Presto J, Jörnvall H, Johansson J (2015) Specific chaperones and regulatory domains in control of amyloid formation. J Biol Chem 290:26430–26436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122:189–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M, Tsai FT (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115:229–240

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Sowa ME, Choi JM, Tsai FT (2004) The ClpB/Hsp104 molecular chaperone – a protein disaggregation machine. J Struct Biol 146:99–105

    Article  CAS  PubMed  Google Scholar 

  • Levitt M, Warshel A (1975) Computer simulation of protein folding. Nature 253:694–698

    Article  CAS  PubMed  Google Scholar 

  • Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 3:201–208

    Article  Google Scholar 

  • Liu L, Chen J, Yang B, Wang Y (2015) Oligomer-dependent and –independent chaperone activity of sHsps in different stressed conditions. FEBS Open Bio 5:155–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Löw D, Brändle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.1 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211:575–582

    Article  PubMed  Google Scholar 

  • Lu Z, Cyr DM (1998) Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 273:27824–27830

    Article  CAS  PubMed  Google Scholar 

  • Luheshi LM, Crowther DC, Dobson CM (2008) Protein misfolding and disease: from the test tube to the organism. Curr Opin Chem Biol 12:25–31

    Article  CAS  PubMed  Google Scholar 

  • Mackay RG, Helsen CW, Tkach JM, Glover JR (2008) The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry 47:1918–1927

    Article  CAS  PubMed  Google Scholar 

  • Makhnevych T, Houry WA (2012) The role of Hsp90 in protein complex assembly. Biochim Biophys Acta 1823:674–682

    Article  CAS  PubMed  Google Scholar 

  • Mani N, Ramakrishna K, Suguna K (2015) Characterization of rice small heat shock proteins targeted to different cellular organelles. Cell Stress Chaperones 20:451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matoo RU, Sharma SK, Priya S, Finka A, Goloubinoff P (2013) Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates. J Biol Chem 288:21399–21411

    Article  CAS  Google Scholar 

  • Mayer MP (2010) Gymnastics of molecular chaperones. Mol Cell 39:321–331

    Article  CAS  PubMed  Google Scholar 

  • Mayer MP, Kityk R (2015) Insights into the molecular mechanism of allostery in Hsp70s. Front Mol Biosci 20:58

    Article  Google Scholar 

  • Mayer MP, Le Breton L (2015) Hsp90: breaking the symmetry. Mol Cell 58:8–20

    Article  CAS  PubMed  Google Scholar 

  • Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, Fraenkel E, Ince TA, Whitesell L, Lindquist S (2012) HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150:549–562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendonça YA, Ramos CH (2012) Cloning, purification and characterization of a 90 kDa heat shock protein from Citrus sinensis (sweet orange). Plant Physiol Biochem 50:87–94

    Article  PubMed  CAS  Google Scholar 

  • Miernyk JA (2001) The J-domain proteins of Arabidopsis thaliana: an unexpectedly large and diverse family of chaperones. Cell Stress Chaperones 6:209–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miozzo F, Sabéran-Djoneidi D, Mezger V (2015) HSFs, stress sensors and sculptors of transcription compartments and epigenetic landscapes. J Mol Biol 427:3793–3816

    Article  CAS  PubMed  Google Scholar 

  • Mogk A, Kummer E, Bukau B (2015) Cooperation of Hsp70 and Hsp100 chaperone machines in protein disaggregation. Front Mol Biosci 19:22

    Google Scholar 

  • Mokry DZ, Abrahao J, Ramos CH (2015) Disaggregases, molecular chaperones that resolubilize protein aggregates. An Acad Bras Cienc 87:1273–1292

    Article  PubMed  Google Scholar 

  • Montgomery DL, Morimoto RI, Giesrasch LM (1999) Mutations in the substrate binding domain of the Escherichia coli 70 kDa affinity or interdomain coupling. J Mol Biol 286:915–932

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI (2011) The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb Symp Quant Biol 76:91–99

    Article  CAS  PubMed  Google Scholar 

  • Morrow G, Hightower LE, Tanguay RM (2015) Small heat shock proteins: big folding machines. Cell Stress Chaperones 20:207–212

    Article  CAS  PubMed  Google Scholar 

  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan AR, Hussey SG, Pinard D, van der Merwe K, Singh P, van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye CY, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van de Peer Y, Rokhsar DS, Schmutz J (2014) The genome of Eucalyptus grandis. Nature 510:356–362

    CAS  PubMed  Google Scholar 

  • Nillegoda NB, Bukau B (2015) Metazoan Hsp70-based protein disaggregases: emergence and mechanisms. Front Mol Biosci 2:57

    Article  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 

  • Nover L, Miernyk JA (2001) A genomics approach to the chaperone network of Arabidopsis thaliana. Cell Stress Chaperones 6:175–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 143:901–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Driscoll J, Clare D, Saibil H (2015) Prion aggregate structure in yeast cells is determined by the Hsp104-Hsp110 disaggregase machinery. J Cell Biol 211:145–158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patel S, Vierling E, Tama F (2014) Replica exchange molecular dynamics simulations provide insight into substrate recognition by small heat shock proteins. Biophys J 106:2644–2655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pesce ER, Blatch GL (2014) Plasmodial Hsp40 and Hsp70 chaperones: current and future perspectives. Parasitology 141:1167–1176

    Article  CAS  PubMed  Google Scholar 

  • Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    Article  CAS  PubMed  Google Scholar 

  • Priya S, Sharma SK, Goloubinoff P (2013) Molecular chaperones as enzymes that catalytically unfold misfolded polypeptides. FEBS Lett 587:1981–1987

    Article  CAS  PubMed  Google Scholar 

  • Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    Article  CAS  PubMed  Google Scholar 

  • Ramos CH (2008) In: O’Doherty CB, Byrne, AC (eds) Protein misfolding. Nova Science Publishers, New York. ISBN: 978-1-60456-881-3

    Google Scholar 

  • Ramos CH, Ferreira ST (2005) Protein folding, misfolding and aggregation: evolving concepts and conformational diseases. Protein Pept Lett 12:213–222

    Article  CAS  PubMed  Google Scholar 

  • Rampelt H, Kirstein-Miles J, Nillegoda NB, Chi K, Scholz SR, Morimoto RI, Bukau B (2012) Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J 31:4221–4235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saibil H (2013) Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 14:630–642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 24:393

    Article  CAS  Google Scholar 

  • Sarkar NK, Thapar U, Kundnani P, Panwar P, Grover A (2013) Functional importance of J- protein family of rice (Oryza sativa). Cell Stress Chaperones 18:321–331

    Article  CAS  PubMed  Google Scholar 

  • Sauer RT, Bolon DN, Burton BM, Burton RE, Flynn JM, Grant RA, Hersch GL, Joshi SA, Kenniston JA, Levchenko I, Neher SB, Oakes ES, Siddiqui SM, Wah DA, Baker TA (2004) Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119:9–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2001) Structure of TPR domainpeptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199–210

    Article  Google Scholar 

  • Schirmer EC, Glover JR, Lindquist S (1996) Hsp100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Mosser DD, Morimoto RI (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12:654–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shorter J (2011) The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 6:e26319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple aligments using Clustal Omega. Mol Syst Biol 11:7–539

    Google Scholar 

  • Slepenkov SV, Witt SN (2002) The unfolding story of the Escherichia coli Hsp70 DnaK: is DnaK a holdase or an unfoldase? Mol Microbiol 45:1197–1206

    Article  CAS  PubMed  Google Scholar 

  • Snider J, Houry WA (2008) AAA+ proteins: diversity in function, similarity in structure. Biochem Soc Trans 36:72–77

    Article  CAS  PubMed  Google Scholar 

  • Sorger PK, Pelham HR (1998) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864

    Article  Google Scholar 

  • Sóti C, Csermely P (2000) Molecular chaperones and the aging process. Biogerontology 1:225–233

    Article  PubMed  Google Scholar 

  • Stein L (2001) Genome annotation: from sequence to biology. Nat Rev Genet 2:493–503

    Article  CAS  PubMed  Google Scholar 

  • Stryer L (1965) The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of nonpolar binding sites. J Mol Biol 13:482–495

    Article  CAS  PubMed  Google Scholar 

  • Summers DW, Douglas PM, Ramos CH, Cyr DM (2009) Polypeptide transfer from Hsp40 to Hsp70 molecular chaperones. Trends Biochem Sci 34:230–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and trancription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tipping KW, van Oosten-Hawle P, Hewitt EW, Radford SE (2015) Amyloid fibres: inert end- stage aggregates or key players in disease? Trends Biochem Sci 40:719–727

    Article  CAS  PubMed  Google Scholar 

  • Tiroli AO, Ramos CH (2007) Biochemical and biophysical characterization of small heat shock proteins from sugarcane. Involvement of a specific region located at the N-terminus with substrate specificity. Int J Biochem Cell Biol 39:818–831

    Article  CAS  PubMed  Google Scholar 

  • Tiroli-Cepeda AO, Ramos CH (2010) Heat causes oligomeric disassembly and increases the chaperone activity of small heat shock proteins from sugarcane. Plant Physiol Biochem 48:108–116

    Article  CAS  PubMed  Google Scholar 

  • Tiroli-Cepeda AO, Ramos CH (2011) An overview of the role of molecular chaperones in protein homeostasis. Protein Pept Lett 18:101–109

    Article  CAS  PubMed  Google Scholar 

  • Tiroli-Cepeda AO, Lima TB, Balbuena TS, Gozzo FC, Ramos CH (2014) Structural and functional characterization of the chaperone Hsp70 from sugarcane. Insights into conformational changes during cycling from cross-linking/mass spectrometry assays. J Proteome 104:48–56

    Article  CAS  Google Scholar 

  • Torrente MP, Shorter J (2013) The metazoan protein disaggregase and amyloid depolymerase system: Hsp110, Hsp70, Hsp40 and small heat shock proteins. Prion 7:457–463

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN (2015) Functional roles of transiently and intrinsically disordered regions within proteins. FEBS J 282:1182–1189

    Article  CAS  PubMed  Google Scholar 

  • van Montfort R, Slingsby C, Vierling E (2001a) Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv Protein Chem 59:105–156

    Article  PubMed  Google Scholar 

  • van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001b) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8:1025–1030

    Article  PubMed  CAS  Google Scholar 

  • Vettore AL, da Silva FR, Kemper EL, Souza GM, da Silva AM, Ferro MI, Henrique-Silva F, Giglioti EA, Lemos MV, Coutinho LL, Nobrega MP, Carrer H, França SC, Bacci JM, Goldman MH, Gomes SL, Nunes LR, Camargo LE, Siqueira WJ, Van Sluys MA, Thiemann OH, Kuramae EE, Santelli RV, Marino CL, Targon ML, Ferro JA, Silveira HC, Marini DC, Lemos EG, Monteiro-Vitorello CB, Tambor JH, Carraro DM, Roberto PG, Martins VG, Goldman GH, de Oliveira RC, Truffi D, Colombo CA, Rossi M, de Araujo PG, Sculaccio SA, Angella A, Lima MM, de Rosa JVE, Siviero F, Coscrato VE, Machado MA, Grivet L, Di Mauro SM, Nobrega FG, Menck CF, Braga MD, Telles GP, Cara FA, Pedrosa G, Meidanis J, Arruda P (2003) Analysis and functional annotation of an expressed sequence tag collection for tropical crop sugarcane. Genome Res 13:2725–2735

    Article  PubMed  PubMed Central  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Voet D, Voet J (2011) Biochemistry, 4th edn. Wiley, Hoboken

    Google Scholar 

  • Wandinger SK, Richter K, Buchner J (2008) The Hsp90 chaperone machinery. J Biol Chem 283:18473–18477

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Waters ER (2013) The evolution, function, structure and expression of the plant sHSPs. J Exp Bot 64:391–403

    Article  CAS  PubMed  Google Scholar 

  • Wegele H, Müller L, Buchner J (2004) Hsp70 and Hsp90 – a relay team for protein folding. Rev Physiol Biochem Pharmacol 151:1–44

    CAS  PubMed  Google Scholar 

  • Westerheide SD, Anckar J, Stevens SMJ, Sistonen L, Morimoto RI (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323:1063–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winkler J, Tyedmers J, Bukau B, Mogk A (2012) Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 179:152–160

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER suite: protein structure and function prediction. Nat Methods 12:7–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yonehara M, Minami Y, Kawata Y, Nagai J, Yahara I (1996) Heat-induced chaperone activity of HSP90. J Biol Chem 271:2641–2645

    Article  CAS  PubMed  Google Scholar 

  • Young JC (2010) Mechanisms of the Hsp70 chaperone system. Biochem Cell Biol 88:291–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154:267–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zettlmeissl G, Rudolph R, Jaenicke R (1979) Reconstitution of lactic dehydrogenase. Noncovalent aggregation vs. reactivation 1. Physical properties and kinetics of aggregation. Biochemistry 18:5567–5571

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization and heat stress responses. BMC Genomics 14:532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Liu B, Li J, Zhang L, Wang Y, Zheng H, Lu M, Chen J (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics 16:181

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606–1614

    Article  CAS  PubMed  Google Scholar 

  • Zietkiewicz S, Krzewska J, Liberek K (2004) Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J Biol Chem 279:44376–44383

    Article  CAS  PubMed  Google Scholar 

  • Zolkiewski M (2006) A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61:1094–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zolkiewski M, Kessel M, Ginsburg A, Maurizi MR (1999) Nucleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci 9:1899–1903

    Article  Google Scholar 

  • Zolkiewski M, Zhang T, Nagy M (2012) Aggregate reactivation mediated by the Hsp100 chaperones. Arch Biochem Biophys 520:1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors wish to apologize to the authors of all the studies that we did not have space to include. Research in the laboratory of CHIR is supported by grants from Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP, 2012/50161-8) and Ministério da Ciência e Tecnologia/Conselho Nacional de Pesquisa e Desenvolvimento (MCT/CNPq). CCG thanks FAPESP for fellowship.

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  1. Department of Organic Chemistry, Institute of Chemistry, University of Campinas – UNICAMP, Campinas, SP, 13083-970, Brazil

    Conrado C. Gonçalves & Carlos H. I. Ramos

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  1. Conrado C. Gonçalves
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Correspondence to Carlos H. I. Ramos .

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  1. Department of Neuroscience, University of Dammam, Damman, Saudi Arabia

    Alexzander A. A. Asea

  2. Division of Molecular and Cellular Biology Department of Radiation Oncology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, USA

    Punit Kaur

  3. Department of Radiation Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA

    Stuart K. Calderwood

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Gonçalves, C.C., Ramos, C.H.I. (2016). Molecular Chaperones and HSPs in Sugarcane and Eucalyptus. In: Asea, A., Kaur, P., Calderwood, S. (eds) Heat Shock Proteins and Plants. Heat Shock Proteins, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-46340-7_13

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