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Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants

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Abstract

Small heat shock proteins (sHSPs) are chaperones that play an important role in stress tolerance. They consist of an alpha-crystallin domain (ACD) flanked by N- and C-terminal regions. However, not all proteins that contain an ACD, hereafter referred to as ACD proteins, are sHSPs because certain ACD proteins are known to have different functions. Furthermore, since not all ACD proteins have been identified yet, current classifications are incomplete. A total of 17 complete plant proteomes were screened for the presence of ACD proteins by HMMER profiling and the identified ACD protein sequences were classified by maximum likelihood phylogeny. Differences among and within groups were analysed, and levels of functional constraint were determined. There are 29 different classes of ACD proteins, eight of which contain classical sHSPs and five likely chaperones. The other classes contain proteins with uncharacterised or poorly characterised functions. N- and C-terminal sequences are conserved within the phylogenetic classes. Phylogenetics suggests a single duplication of the CI sHSP ancestor that occurred prior to the speciation of mono- and dicotyledons. This was followed by a number of more recent duplications that resulted in the presence of many paralogues. The results suggest that N- and C-terminal sequences of sHSPs play a role in class-specific functionality and that non-sHSP ACD proteins have conserved but unexplored functions, which are mainly determined by subsequences other than that of the ACD.

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Abbreviations

ACD:

Alpha-crystallin domain

CAM:

C-terminal anchoring module

MC:

Monophyletic clades

MSA:

Multiple sequence alignment

NaLi:

Sodium–lithium tolerance

sHSPs:

Small heat shock proteins

UAP:

Uncharacterised ACD protein

References

  • Abyzov A, Errami M, Leslin CM, Ilyin VA (2005) Friend, an integrated analytical front-end application for bioinformatics. Bioinformatics 21:3677–3678

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  • Bagnéris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep N, Slingsby C (2009) Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J Mol Biol 392:1242–1252

    Article  PubMed  Google Scholar 

  • Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylidès C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13:519–527

    Article  PubMed  CAS  Google Scholar 

  • Basha E, 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  PubMed  CAS  Google Scholar 

  • Basha E, Jones C, Wysocki V, Vierling E (2010) Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J Biol Chem 285:11489–11497

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Chang H, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:1667–1675

    Article  PubMed  CAS  Google Scholar 

  • de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin—small heat-shock protein superfamily. Int J Biol Macromol 22:151–162

    Article  PubMed  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (2010) HMMER3: a new generation of sequence homology search software. http://hmmer.janelia.org/

  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  PubMed  CAS  Google Scholar 

  • Giese KC, Vierling E (2004) Mutants in a small heat shock protein that affect the oligomeric state. Analysis and allele-specific suppression. J Biol Chem 279:32674–32683

    Article  PubMed  CAS  Google Scholar 

  • Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313:903–919

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Dufayard J, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  PubMed  CAS  Google Scholar 

  • Hanson RM (2010) Jmol: an open-source Java viewer for chemical structures in 3D. http://www.jmol.org/

  • 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  PubMed  CAS  Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    Article  PubMed  CAS  Google Scholar 

  • Hilario E, Teixeira EC, Pedroso GA, Bertolini MC, Medrano FJ (2006) Crystallization and preliminary X-ray diffraction analysis of XAC1151, a small heat-shock protein from Xanthomonas axonopodis pv. citri belonging to the alpha-crystallin family. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:446–448

    Article  PubMed  Google Scholar 

  • Horton P, Park K, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed  Google Scholar 

  • Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    Article  PubMed  CAS  Google Scholar 

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008:420747

    PubMed  Google Scholar 

  • Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460

    Article  PubMed  Google Scholar 

  • Jaya N, Garcia V, Vierling E (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci USA 106:15604–15609

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kirschner M, Winkelhaus S, Thierfelder JM, Nover L (2000) Transient expression and heat-stress-induced co-aggregation of endogenous and heterologous small heat-stress proteins in tobacco protoplasts. Plant J 24:397–411

    Article  PubMed  CAS  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Ma C, Haslbeck M, Babujee L, Jahn O, Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141:47–60

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto TK, Pardo JM, Takeda S, Bressan RA, Hasegawa PM (2001) Tobacco and Arabidopsis SLT1 mediate salt tolerance of yeast. Plant Mol Biol 45:489–500

    Article  PubMed  CAS  Google Scholar 

  • Mintseris J, Weng Z (2005) Structure, function, and evolution of transient and obligate protein–protein interactions. Proc Natl Acad Sci USA 102:10930–10935

    Article  PubMed  CAS  Google Scholar 

  • Morrow G, Inaguma Y, Kato K, Tanguay RM (2000) The small heat shock protein Hsp22 of Drosophila melanogaster is a mitochondrial protein displaying oligomeric organization. J Biol Chem 275:31204–31210

    Article  PubMed  CAS  Google Scholar 

  • Mueller LA, Solow TH, Taylor N, Skwarecki B, Buels R, Binns J, Lin C, Wright MH, Ahrens R, Wang Y et al (2005) The SOL genomics network: a comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317

    Article  PubMed  CAS  Google Scholar 

  • Murakami T, Matsuba S, Funatsuki H, Kawaguchi K, Saruyama H, Tanida M, Sato Y (2004) Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol Breed 13:165–175

    Article  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Ann Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Nikolaidis N, Nei M (2004) Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol 21:498–505

    Article  PubMed  CAS  Google Scholar 

  • Notredame C, Abergel C (2003) Using multiple alignment methods to assess the quality of genomic data analysis. In: Andrade M (ed) Bioinformatics and genomes: current perspectives. Horizon Scientific Press, Wymondham, pp 30–50

    Google Scholar 

  • Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217

    Article  PubMed  CAS  Google Scholar 

  • Orosz F, Ovádi J (2011) Proteins without 3D structure: definition, detection and beyond. Bioinformatics 27:1449–1454

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L et al (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  CAS  Google Scholar 

  • Ouyang Y, Chen J, Xie W, Wang L, Zhang Q (2009) Comprehensive sequence and expression profile analysis of Hsp20 gene family in rice. Plant Mol Biol 70:341–357

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Poulain P, Gelly J, Flatters D (2010) Detection and architecture of small heat shock protein monomers. PLoS One 5:e9990

    Article  PubMed  Google Scholar 

  • Rampino P, Mita G, Assab E, De Pascali M, Giangrande E, Treglia AS, Perrotta C (2010) Two sunflower 17.6HSP genes, arranged in tandem and highly homologous, are induced differently by various elicitors. Plant Biol 12:13–22

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P, Lindquist EA, Kamisugi Y et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    Article  PubMed  CAS  Google Scholar 

  • Reumann S, Weber APM (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled—others remain. Biochim Biophys Acta 1763:1496–1510

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP, Piontkivska H, Nei M (2002) Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family. Mol Biol Evol 19:68–75

    Article  PubMed  CAS  Google Scholar 

  • Sarkar NK, Kim Y, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10:393

    Article  PubMed  Google Scholar 

  • Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep 27:329–334

    Article  PubMed  CAS  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis, available at http://www.math.wustl.edu/~sawyer

  • Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Federhen S et al (2011) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 39:D38–D51

    Article  PubMed  Google Scholar 

  • Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66:361–378

    Article  PubMed  CAS  Google Scholar 

  • Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225–237

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  PubMed  CAS  Google Scholar 

  • Siddique M, Port M, Tripp J, Weber C, Zielinski D, Calligaris R, Winkelhaus S, Scharf K (2003) Tomato heat stress protein Hsp16.1-CIII represents a member of a new class of nucleocytoplasmic small heat stress proteins in plants. Cell Stress Chaperones 8:381–394

    Article  PubMed  CAS  Google Scholar 

  • Sluijs A, Schouten S, Pagani M, Woltering M, Brinkhuis H, Sinninghe Damsté JS, Dickens GR, Huber M, Reichart G, Stein R et al (2006) Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum. Nature 441:610–613

    Article  PubMed  CAS  Google Scholar 

  • Stamler R, Kappé G, Boelens W, Slingsby C (2005) Wrapping the alpha-crystallin domain fold in a chaperone assembly. J Mol Biol 353:68–79

    Article  PubMed  CAS  Google Scholar 

  • Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    PubMed  CAS  Google Scholar 

  • Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L et al (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014

    Article  PubMed  CAS  Google Scholar 

  • Swigonová Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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 

  • 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  PubMed  CAS  Google Scholar 

  • Waters ER (1995) The molecular evolution of the small heat-shock proteins in plants. Genetics 141:785–795

    PubMed  CAS  Google Scholar 

  • Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13:127–142

    Article  PubMed  CAS  Google Scholar 

  • Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC (2000) Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12:569–582

    Article  PubMed  CAS  Google Scholar 

  • Zhu H, Chen T, Zhu M, Fang Q, Kang H, Hong Z, Zhang Z (2008) A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148:337–347

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Financial resources: Universidad Nacional de Mar del Plata, project EXA468/09; HGB is a postdoctoral fellow at CONICET; EMV and AtH are members of CONICET research career.

A. lyrata, B. distachyon, C. papaya, C. sativus, M. esculenta, M. guttatus, M. truncatula, P. persica, R. communis, V. vinifera and Z. mays sequence data were produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/) in collaboration with the user community (Phytozome v5).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Biológicas (IIB-CONICET-UNMdP), Universidad Nacional de Mar del Plata, CC 1245, 7600, Mar del Plata, Argentina

    Hernán Gabriel Bondino & Arjen ten Have

  2. Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Universidad Nacional de Rosario, Suipacha 531, S2002LRK, Rosario, Argentina

    Estela Marta Valle

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  1. Hernán Gabriel Bondino
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Correspondence to Arjen ten Have.

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Supplemental Data file S1 Complete Sequences of 824 ACD proteins (FASTA format). The first two letters of the accession codes correspond to the plant species: AL, A. lyrata; AT, A. thaliana; BD, B. distachyon; CP, C. papaya; CS, C. sativus; GM, G. max; ME, M. esculenta; MG, M. guttatus; MT, M. truncatula; OS, O. sativa; PP, P. persica; PT, P. trichocarpa; RC, R. communis; SB, S. bicolor; SL, S. lycopersicum; VV, V. vinifera; ZM, Z. mays

Supplemental Data file S2 Truncated MSA (Clustal format). The first two letters of the accession codes correspond to the plant species: AL, A. lyrata; AT, A. thaliana; BD, B. distachyon; CP, C. papaya; CS, C. sativus; GM, G. max; ME, M. esculenta; MG, M. guttatus; MT, M. truncatula; OS, O. sativa; PP, P. persica; PT, P. trichocarpa; RC, R. communis; SB, S. bicolor; SL, S. lycopersicum; VV, V. vinifera; ZM, Z. mays

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Bondino, H.G., Valle, E.M. & ten Have, A. Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants. Planta 235, 1299–1313 (2012). https://doi.org/10.1007/s00425-011-1575-9

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