Abstract
Caseinolytic protease (Clp)/Hsp100 proteins are members of the AAA+ (ATPase associated with a variety of cellular activities) family of proteins present in lower life forms and plants. These proteins represent a unique chaperone system that performs the crucial role of retrieving functional proteins from the aggregated state and are thus also referred to as disaggregases. Clp/Hsp100s were originally discovered in bacteria and yeast cells in late 1980s and early 1990s. Arabidopsis thaliana, in particular after the completion of its genome sequencing in the year 2000, has served as an excellent experimental system for investigating this important chaperone machine in plants. From the reverse and forward genetic analysis carried out with Arabidopsis Hsp101, it emerged that this protein is a powerful candidate gene in conferring heat tolerance. Importantly, this protein is implicated with heat tolerance both in vegetative and reproductive stages of the growth and development of Arabidopsis plants. In the data on genetic polymorphism in the amino acid sequence of Arabidopsis Hsp101 across diverse A. thaliana accessions sequenced in 1001 Arabidopsis genome sequencing project, we find that that there are sixty-three distinct AtHsp101 sequence types with variations in N-terminus, nucleotide binding and C-terminus domains in 855 analyzed Arabidopsis accessions. The in-depth analysis with these variant allelic forms may yield invaluable information on genetic variations in the regulatory regions which control the Hsp101 expression as well as those affecting Hsp101 disaggregase activity. Arabidopsis Hsp101 protein has turned out to be a prototype in search for homolog proteins and mechanisms of heat stress tolerance in rice as well as across diverse crops. Herein, we present the status of our understanding on the Arabidopsis Hsp101 genes, proteins, and their functional relevance.
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Abbreviations
- Clp:
-
Caseinolytic proteases
- NTD:
-
N-terminal domain
- Hsp:
-
Heat shock protein
- WT:
-
Wild type
- Hsf:
-
Heat shock factor
- HSE:
-
Heat shock element
- AAA:
-
ATPase associated with a variety of cellular activities
- NBD:
-
Nucleotide binding domain
- HS:
-
Heat stress
- TAIR:
-
The Arabidopsis information resource
- SNP:
-
Single nucleotide polymorphism
References
Agarwal M, Katiyar-Agarwal S, Sahi C, Gallie DR, Grover A (2001) Arabidopsis thaliana Hsp100 proteins: kith and kin. Cell Stress Chaperones 6:219. https://doi.org/10.1379/1466-1268(2001)006%3c0219:ATHPKA
Agarwal M, Katiyar-Agarwal S, Grover A (2002) Plant Hsp100 proteins: structure, function and regulation. Plant Sci 163:397–405. https://doi.org/10.1016/S0168-9452(02)00209-1
Agarwal M, Sahi C, Katiyar-Agarwal S, Agarwal S, Young T, Gallie DR, Sharma VM, Ganesan K, Grover A (2003) Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol Biol 51:543–553
Agarwal M, Singh A, Mittal D, Sahi C, Grover A (2011) Cycloheximide-mediated superinduction of genes involves both native and foreign transcripts in rice (Oryza sativa L.). Plant Physiol Biochem 49:9–12. https://doi.org/10.1016/j.plaphy.2010.09.010
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657. https://doi.org/10.1126/science.1086391
Barah P, Jayavelu ND, Mundy J, Bones AM (2013) Genome scale transcriptional response diversity among ten ecotypes of arabidopsis thaliana during heat stress. Front Plant Sci 4:1–10. https://doi.org/10.3389/fpls.2013.00532
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. https://doi.org/10.1074/jbc.M505653200<
Batra G, Chauhan VS, Singh A, Sarkar NK, Grover A (2007) Complexity of rice Hsp100 gene family: lessons from rice genome sequence data. J Biosci 32:611–619. https://doi.org/10.1007/s12038-007-0060-x
Beinker P, Schlee S, Groemping Y, Seidel R, Reinstein J (2002) The N terminus of ClpB from thermus thermophilus is not essential for the chaperone activity. J Biol Chem 277:47160–47166. https://doi.org/10.1074/jbc.M207853200
Burke JJ, Chen J (2015) Enhancement of reproductive heat tolerance in plants. PLoS ONE 10:e0122933. https://doi.org/10.1371/journal.pone.0122933
Busch W, Wunderlich M, Schöffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41:1–14. https://doi.org/10.1111/j.1365-313X.2004.02272.x
Cagliari TC, da Silva VCH, Borges JC, Prando A, Tasic L, Ramos CHI (2011) Sugarcane Hsp101 is a hexameric chaperone that binds nucleotides. Int J Biol Macromol 49:1022–1030. https://doi.org/10.1016/j.ijbiom
Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R, Leisse A, Steinhauser D, Fernie AR, Willmitzer L, Hannah MA (2011) High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant J 67:869–884
Campbell JL, Klueva NY, Zheng H, Nieto-Sotelo J, Ho T-H, Nguyen HT (2001) Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA. Biochim Biophys Acta Gene Struct Expr 1517:270–277. https://doi.org/10.1016/S0167-4781(00)00292-X
Chang CC, Huang PS, Lin HR, Lu CH (2007) Transactivation of protein expression by rice HSP101 in planta and using Hsp101 as a selection marker for transformation. Plant Cell Physiol 48:1098–1107. https://doi.org/10.1093/pcp/pcm080
Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262. https://doi.org/10.1104/pp.106.091322
Danekar P, Tyagi A, Mahto A, Krishna KG, Singh A, Raje RS, Gaikwad K, Singh NK (2014) Genome wide characterization of hsp 100 family genes from pigeonpea. Indian J Genet Plant Breed 74:325–334. https://doi.org/10.5958/0975-6906.2014.00850.5
Dinkova TD, Zepeda H, Martínez-Salas E, Martínez LM, Nieto-Sotelo J, Sánchez De Jiménez E (2005) Cap-independent translation of maize Hsp101. Plant J 41:722–731. https://doi.org/10.1111/j.1365-313X.2005.023
Doyle SM, Hoskins JR, Wickner S (2012) DnaK chaperone-dependent disaggregation by caseinolytic peptidase B (ClpB) mutants reveals functional overlap in the N-terminal domain and nucleotide-binding domain-1 pore tyrosine. J Biol Chem 287:28470–28479
Doyle SM, Shastry S, Kravats AN, Shih YH, Miot M, Hoskins JR, Stan G, Wickner S (2015) Interplay between E. coli DnaK, ClpB and GrpE during protein disaggregation. J Mol Biol 427:312–327. https://doi.org/10.1016/j.jmb.2014.10.013
Echevarría-Zomeño S, Fernández-Calvino L, Castro-Sanz AB, López JA, Vázquez J, Castellano MM (2016) Dissecting the proteome dynamics of the early heat stress response leading to plant survival or death in Arabidopsis. Plant, Cell Environ 39:1264–1278
Erdayani E, Nagarajan R, Grant NP, Gill KS (2020) Genome-wide analysis of the HSP101/CLPB gene family for heat tolerance in hexaploid wheat. Sci Rep 10:1–17. https://doi.org/10.1038/s41598-020-60673-4
Eriksson MJ, Clarke AK (1996) The heat shock protein ClpB mediates the development of thermotolerance in the cyanobacterium synechococcus sp. strain PCC 7942. J Bacteriol 178:4839–4846. https://doi.org/10.1128/jb.178.16.4839-4846.1996
Gottesman S, Squires C, Pichersky E, Carrington M, Mattick JS, Dalrymple B, Kuramitsu H, Shiroza T, Clark WP, Ross B, Squires CL, Maurizi MR (1990) Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc Natl Acad Sci (USA) 87:3513–3517
Gullì M, Corradi M, Rampino P, Marmiroli N, Perrotta C (2007) Four members of the HSP101 gene family are differently regulated in Triticum durum Desf. FEBS Lett 581:4841–4849. https://doi.org/10.1016/j.febslet.2007.09.010
Guo L, Chen S, Liu K, Liu Y, Ni L, Zhang K, Zhang L (2008) Isolation of heat shock factor HsfA1a-binding sites in vivo revealed variations of heat shock elements in Arabidopsis Thaliana. Plant Cell Physiol 49:1306–1315. https://doi.org/10.1093/pcp/pcn105
Heuck A, Schitter-Sollner S, Józef Suskiewicz M, Kurzbauer R, Kley J, Schleiffer A, Rombaut P, Herzog F, Clausen T (2016) Structural basis for the disaggregase activity and regulation of Hsp104. Elife 5:1–23. https://doi.org/10.7554/eLife.21516
Hill JE, Hemmingsen SM (2001) Arabidopsis thaliana type I and II chaperonins. Cell Stress Chaperones 6:190–200. https://doi.org/10.1379/1466-1268(2001)006%3c0190:attiai%3e2.0.co;2
Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392–4397. https://doi.org/10.1073/pnas.97.8.4392
Hong S, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27:25–35
Hong SW, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132:757–767. https://doi.org/10.1104/pp.102.017145
Hwang BJ, Park WJ, Chung CH, Goldberg AL (1987) Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proc Natl Acad Sci USA 84:5550–5554. https://doi.org/10.1073/pnas.84.16.5550
Ikeda M, Mitsuda N, Ohme-Takagi M (2011) Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157:1243–1254. https://doi.org/10.1104/pp.111.179036
Jackrel ME, Shorter J (2015) Engineering enhanced protein disaggregases for neurodegenerative disease. Prion 9:90–109. https://doi.org/10.1080/19336896.2015.1020277
Kannan TR, Musatovova O, Gowda P, Baseman JB (2008) Characterization of a unique ClpB protein of Mycoplasma pneumoniae and its impact on growth. Infect Immun 76:5082–5092. https://doi.org/10.1128/IAI.00698-08
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168. https://doi.org/10.1104/pp.104.052142.1
Katayama-Fujimura Y, Gottesman S, Maurizi MR (1987) A multiple-component, ATP-dependent protease from Escherichia coli. J Biol Chem 262:4477–4485
Katiyar-Agarwal S, Agarwal M, Gallie DR, Grover A (2001) Search for the cellular functions of plant Hsp100/Clp family proteins. CRC Crit Rev Plant Sci 20:277–295. https://doi.org/10.1080/20013591099236
Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677–686. https://doi.org/10.1023/A:1022561926676
Keeler SJ, Boettger CM, Haynes JG, Kuches KA, Johnson MM, Thureen DL, Keeler CL, Kitto SL (2000) Acquired thermotolerance and expression of the HSP100/ClpB genes of lima bean. Plant Physiol 123:1121–1132
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of cDNA for a dehydration-inducible gene that encodes a CLP a, b-like protein in arabidopsis thaliana L. Biochem Biophys Res Commun 196:1214–1220
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203
Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246. https://doi.org/10.1379/1466-1268(2001)006%3c0238:THFOPI%3e2.0.CO;2
Lavania D, Dhingra A, Grover A (2018) Analysis of transactivation potential of rice (Oryza sativa L.) heat shock factors. Planta 247:1267–1276. https://doi.org/10.1007/s00425-018-2865-2
Lázaro-Mixteco PE, Nieto-Sotelo J, Swatek KN, Houston NL, Mendoza-Hernández G, Thelen JJ, Dinkova TD (2012) The absence of heat shock protein HSP101 affects the proteome of mature and germinating maize embryos. J Proteome Res 11:3246–3258
Lee YR, Nagao RT, Key JL (1994) A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. Plant Cell 6:1889–1897. https://doi.org/10.1105/tpc.6.12.1889
Lee JH, Hübel A, Schöffl F (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J 8:603–612. https://doi.org/10.1046/j.1365-313X.1995.8040603.x
Lee U, Wie C, Escobar M, Williams B, Hong S, Vierling E (2005) Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell 17:559–571. https://doi.org/10.1105/tpc.104.027540.1
Lee U, Rioflorido I, Hong SW, Larkindale J, Waters ER, Vierling E (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49:115–127. https://doi.org/10.1111/j.1365-313X.2006.02940.x
Lee J, Kim J-H, Biter AB, Sielaff B, Lee S, Tsai FTF (2013) Heat shock protein (Hsp) 70 is an activator of the Hsp104 motor. Proc Natl Acad Sci USA 110:8513–8518. https://doi.org/10.1073/pnas.1217988110
Li M, Berendzen KW, Schöffl F (2010) Promoter specificity and interactions between early and late Arabidopsis heat shock factors. Plant Mol Biol 73:559–567. https://doi.org/10.1007/s11103-010-9643-2
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 6:201–208. https://doi.org/10.1379/1466-1268(2001)006%3c0201:gaoths%3e2.0.co;2
Lin M-Y, Chai K-H, Ko S-S, Kuang L-Y, Lur H-S, Charng Y-Y (2014) A Positive Feedback Loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol 164:2045–2053
Liu HC, Charng YY (2012) Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signal Behav 7:1–5. https://doi.org/10.4161/psb.19803
Liu HC, Charng YY (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol 163:276–290. https://doi.org/10.1104/pp.113.221168
Liu Z, Tek V, Akoev V, Zolkiewski M (2002) Conserved amino acid residues within the amino-terminal domain of ClpB are essential for the chaperone activity. J Mol Biol 321:111–120. https://doi.org/10.1016/S0022-2836(02)00591-0
Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant, Cell Environ 34:738–751. https://doi.org/10.1111/j.1365-3040
Lukoszek R, Feist P, Ignatova Z (2016) Insights into the adaptive response of Arabidopsis thaliana to prolonged thermal stress by ribosomal profiling and RNA-Seq. BMC Plant Biol 16:1–13. https://doi.org/10.1186/s12870-016-0915-0
McLoughlin F, Basha E, Fowler ME, Kim M, Bordowitz J, Katiyar-Agarwal S, Vierling E (2016) Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiol 172:1221–1236. https://doi.org/10.1104/pp.16.00536
McLoughlin F, Kim M, Marshall RS, Vierstra RD, Vierling E (2019) HSP101 interacts with the proteasome and promotes the clearance of ubiquitylated protein aggregates. Plant Physiol 180:1829–1847
Merret R, Carpentier MC, Favory JJ, Picart C, Descombin J, Bousquet-Antonelli C, Tillard P, Lejay L, Deragon JM, Charng YY (2017) Heat shock protein HSP101 affects the release of ribosomal protein mRNAs for recovery after heat shock. Plant Physiol 174:1216–1225
Miernyk JA (2001) The J-domain proteins of Arabidopsis thaliana: an unexpectedly large and diverse family of chaperones. Cell Stress Chaperones 6:209–218. https://doi.org/10.1379/1466-1268(2001)006%3c0209
Mishra RC, Grover A (2014) Intergenic sequence between arabidopsis caseinolytic protease B-cytoplasmic/heat shock protein100 and choline kinase genes functions as a heat-inducible bidirectional promoter. Plant Physiol 166:1646–1658
Mishra RC, Grover A (2016) ClpB/Hsp100 proteins and heat stress tolerance in plants. Crit Rev Biotechnol 36:862–874. https://doi.org/10.3109/07388551.2015.1051942
Mishra RC, Grover A (2019) Voyaging around ClpB/Hsp100 proteins and plant heat tolerance. Proc Indian Natl Sci Acad 85:791–802. https://doi.org/10.16943/ptinsa/2019/49592
Mishra RC, Richa SinghA, Tiwari LD, Grover A (2016) Characterization of 5′UTR of rice ClpB-C/Hsp100 gene: evidence of its involvement in post-transcriptional regulation. Cell Stress Chaperones 21:271–283. https://doi.org/10.1007/s12192-015-0657-1
Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 47:785–795. https://doi.org/10.1016/j.plaphy.2009.05.003
Mittal D, Enoki Y, Lavania D, Singh A, Sakurai H, Grover A (2011) Binding affinities and interactions among different heat shock element types and heat shock factors in rice (Oryza sativa L.). FEBS J 278:3076–3085. https://doi.org/10.1111/j.1742-4658.2011.08229.x
Mittal D, Madhyastha DA, Grover A (2012a) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7:e40899. https://doi.org/10.1371/journal.pone.0040899
Mittal D, Madhyastha DA, Grover A (2012b) Gene expression analysis in response to low and high temperature and oxidative stresses in rice: combination of stresses evokes different transcriptional changes as against stresses applied individually. Plant Sci 197:102–113. https://doi.org/10.1016/j.plantsci.2012.09.008
Mizuno S, Nakazaki Y, Yoshida M, Watanabe YH (2012) Orientation of the amino-terminal domain of ClpB affects the disaggregation of the protein. FEBS J 279:1474–1484. https://doi.org/10.1111/j.1742-4658.2012
Mogk A, Schlieker C, Strub C, Rist W, Weibezahn J, Bukau B (2003) Roles of individual domains and conserved motifs of the AAA + chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J Biol Chem 278:17615–17624
Mohapatra C, Kumar Jagdev M, Vasudevan D (2017) Crystal structures reveal N-terminal domain of Arabidopsis thaliana ClpD to be highly divergent from that of ClpC1. Sci Rep 7:1–11. https://doi.org/10.1038/srep44366
Mokry DZ, da Silva VCH, Abrahão J, Ramos CHI (2017) Characterization of the Hsp100 disaggregase from sugarcane (SHsp101) for chaperone like activity in a yeast system. J Plant Biochem Biotechnol 26:478–487. https://doi.org/10.1007/s13562-017-0409-7
Moore T, Keegstra K (1993) Characterization of a cDNA clone encoding a chloroplast-targeted Clp homologue. Plant Mol Biol 21:525–537. https://doi.org/10.1007/BF00028809
Muthusamy SK, Dalal M, Chinnusamy V, Bansal KC (2016) Differential regulation of genes coding for organelle and cytosolic ClpATPases under biotic and abiotic stresses in Wheat. Front Plant Sci 7:1–15
Myouga F, Motohashi R, Kuromori T, Nagata N, Shinozaki K (2006) An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. Plant J 48:249–260. https://doi.org/10.1111/j.1365-313X.2006.02873.x
Nakabayashi K, Ito M, Kiyosue T, Shinozaki K, Watanabe A (1999) Identification of clp genes expressed in senescing Arabidopsis leaves. Plant Cell Physiol 40:504–514. https://doi.org/10.1093/oxfordjournals.p
Nieto-Sotelo J, Kannan KB, Martínez LM, Segal C (1999) Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp 100 protein homologue. Gene 230:187–195. https://doi.org/10.1016/S0378-1119(99)00060-8
Nieto-Sotelo J, Martínez LM, Ponce G, Cassab GI, Alagón A, Meeley RB, Ribaut JM, Yang R (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell 14:1621–1633. https://doi.org/10.1105/tpc.010487
Oguchi Y, Kummer E, Seyffer F, Berynskyy M, Anstett B, Zahn R, Wade RC, Mogk A, Bukau B (2012) A tightly regulated molecular toggle controls AAA + disaggregase. Nat Struct Mol Biol 19:1338–1346. https://doi.org/10.1038/nsmb.2441
Ohama N, Kusakabe K, Mizoi J, Zhao H, Kidokoro S, Koizumi S (2016) The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of transcription factor expression. Plant Cell 28:181–201. https://doi.org/10.1105/tpc.15.00435
Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65. https://doi.org/10.1016/j.tplants.2016.08.015
Palmblad M, Mills DJ, Bindschedler LV (2008) Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. J Proteome Res 7:780–785
Panzade KP, Vishwakarma H, Padaria JC (2020) Heat stress inducible cytoplasmic isoform of ClpB1 from Z. nummularia exhibits enhanced thermotolerance in transgenic tobacco. Mol Biol Rep 47:3821–3831
Pareek A, Singla SL, Grover A (1995) Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stress in rice and in response to high temperature stress in rice and in response to high temperature stress in diverse plant genera. Plant Mol Biol 29:293–301
Parsell DA, Sanchez Y, Stitzel JD, Lindquist S (1991) Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature 353:270–273
Parsell DA, Kowal AS, Singer MA, Lindquist S (1994) Protein disaggregation. Nature 372:475–478
Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492. https://doi.org/10.1105/tpc.12.4.479
Radhamony RN, Prasad AM, Srinivasan R (2005) T-DNA insertional mutagenesis in Arabidopsis: a tool for functional genomics. Electron J Biotechnol 8:82–106
Rajan VBV, D’Silva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genomics 9:433–446. https://doi.org/10.1007/s10142-009-0132-0
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
Rosenzweig R, Moradi S, Zarrine-Afsar A, Glover JR, Kay LE (2013) Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339:1080–1083. https://doi.org/10.1126/science.1233066
Rosenzweig R, Farber P, Velyvis A, Rennella E, Latham MP, Kay LE (2015) ClpB N-terminal domain plays a regulatory role in protein disaggregation. Proc Natl Acad Sci USA 112:E6872–E6881. https://doi.org/10.1073/pnas.1512783112
Rosenzweig R, Sekhar A, Nagesh J, Kay LE (2017) Promiscuous binding by Hsp70 results in conformational heterogeneity and fuzzy chaperone-substrate ensembles. Elife 6:1–22. https://doi.org/10.7554/eLife.28030
Sanchez Y, Lindquist SL (1990) HSP104 required for induced thermotolerance. Science 80(248):1112–1115. https://doi.org/10.1126/science.2188365
Sanchez Y, Taulien J, Borkovich KA, Lindquist S (1992) Hsp104 is required for tolerance to many forms of stress. EMBO J 11:2357–2364. https://doi.org/10.1002/j.1460-2075.1992.tb05295.x
Sarkar NK, Kim Y-K, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genom 10:393. https://doi.org/10.1186/1471-2164-10-393
Sarkar NK, Kundnani P, Grover A (2013a) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18:427–437. https://doi.org/10.1007/s12192-012-0395-6
Sarkar NK, Thapar U, Kundnani P, Panwar P, Grover A (2013b) Functional relevance of J-protein family of rice (Oryza sativa). Cell Stress Chaperones 18:321–331. https://doi.org/10.1007/s12192-012-0384-9
Sarkar NK, Kim YK, Grover A (2014) Coexpression network analysis associated with call of rice seedlings for encountering heat stress. Plant Mol Biol 84:125–143. https://doi.org/10.1007/s11103-013-0123-3
Sarkar NK, Kotak S, Agarwal M, Kim Y-K, Grover A (2020) Silencing of class I small heat shock proteins affects seed—related attributes and thermotolerance in rice seedlings. Planta 251:1–16
Scharf K-D, 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. https://doi.org/10.1379/1466-1268(2001)006%3c0225:TEFOAT%3e2.0.CO;2
Schirmer EC, Lindquist S, Vierling E (1994) An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. Plant Cell 6:1899–1909
Serrano N, Ling Y, Bahieldin A, Mahfouz MM (2019) Thermopriming reprograms metabolic homeostasis to confer heat tolerance. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-018-36484-z
Seyffer F, Kummer E, Oguchi Y, Winkler J, Kumar M, Zahn R, Sourjik V, Bukau B, Mogk A (2012) Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA + disaggregase at aggregate surfaces. Nat Struct Mol Biol 19:1347–1355. https://doi.org/10.1038/nsmb.2442
Shorter J, Southworth DR (2019) Spiraling in control: structures and mechanisms of the Hsp104 disaggregase. Cold Spring Harb Perspect Biol 11(8):a034033. https://doi.org/10.1101/cshperspect.a034033
Singh A, Grover A (2010) Plant Hsp100/ClpB-like proteins: poorly-analyzed cousins of yeast ClpB machine. Plant Mol Biol 74:395–404. https://doi.org/10.1007/s11103-010-9682-8
Singh A, Singh U, Mittal D, Grover A (2010) Genome-wide analysis of rice ClpB/HSP100. ClpC and ClpD genes. BMC Genom 11:95. https://doi.org/10.1186/1471-2164-11-95
Singh A, Mittal D, Lavania D, Agarwal M, Mishra RC, Grover A (2012) OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress Chaperones 17:243–254
Singh G, Sarkar NK, Grover A (2018) Mapping of domains of heat stress transcription factor OsHsfA6a responsible for its transactivation activity. Plant Sci 274:80–90. https://doi.org/10.1016/j.plantsci.2018.05.010
Singla SL (1991) Gene expression in higher plants in response to environmental stresses. MSc Thesis, Dept Plant Mol Biol, Delhi Univ
Singla SL, Grover A (1993) Antibodies raised against yeast HSP 104 cross-react with a heat-and abscisic acid-regulated polypeptide in rice. Plant Mol Biol 22:1177–1180. https://doi.org/10.1007/BF00028989%3c/p
Singla SL, Grover A (1994) Detection and quantitation of a rapidly accumulating and predominant 104 kDa heat shock polypeptide in rice. Plant Sci 97:23–30. https://doi.org/10.1016/0168-9452(94)90103-1
Singla SL, Pareek A, Grover A (1997) Yeast HSP104 homologue rice HSP110 is developmentally- and stress-regulated. Plant Sci 125:211–219. https://doi.org/10.1016/S0168-9452(97)00073-3
Singla SL, Pareek A, Kush AK, Grover A (1998) Distribution patterns of 104 kDa stress-associated protein in rice. Plant Mol Biol 37:911–919. https://doi.org/10.1023/A:1006099715375
Squires CL, Pedersen S, Ross BM, Squires C (1991) ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol 173:4254–4262. https://doi.org/10.1128/jb.173.14.4254-4262.1991
Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for Pleiotropic Consequences. Plant Physiol 132:979–987. https://doi.org/10.1104/pp.10
Tanaka N, Tani Y, Hattori H, Tada T, Kunugi S (2004) Interaction of the N-terminal domain of Escherichia coli heat shock protein ClpB and protein aggregates during chaperone activity. Protein Sci 13:3214–3322
Tariq A, Lin JB, Noll MM, Torrente MP, Mack KL, Murillo OH, Jackrel ME, Shorter J (2018) Potentiating Hsp104 activity via phosphomimetic mutations in the middle domain. FEMS Yeast Res 18:1–14
Tiwari LD, Khungar L, Grover A (2020) AtHsc70-1 negatively regulates the basal heat tolerance in Arabidopsis thaliana through affecting the activity of HsfAs and Hsp101. Plant J. https://doi.org/10.1111/tpj.14883
Tomoyasu T, Mogk A, Langen H, Goloubinoff P, Bukau B (2001) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40:397–413. https://doi.org/10.1046/j.1365-2958.2001.02383.x
Tonsor SJ, Scott C, Boumaza I, Liss TR, Brodsky JL, Vierling E (2008) Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Mol Ecol 17:1–7. https://doi.org/10.1038/jid.2014.371
Wang L, Ma KB, Lu ZG, Ren SX, Jiang HR, Cui JW, Chen G, Teng NJ, Lam HM, Jin B (2020) Differential physiological, transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock. BMC Plant Biol 20:86. https://doi.org/10.1186/s12870-020-2292-y
Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403. https://doi.org/10.1093/jxb/ers355
Wells DR, Tanguay RL, Le H, Gallie DR (1998) HSP101 functions as a specific translational regulatory protein whose activity is regulated by nutrient status. Genes Dev 12:3236–3251. https://doi.org/10.1101/gad.12.20.3236
Wendler P, Shorter J, Snead D, Plisson C, Clare DK, Lindquist S, Saibil HR (2009) Motor mechanism for protein threading through Hsp104. Mol Cell 34:81–92. https://doi.org/10.1016/j.molcel.2009.02.026
Wu TY, Juan YT, Hsu YH, Wu SH, Liao HT, Fung RWM, Charng YY (2013) Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis. Plant Physiol 161:2075–2084. https://doi.org/10.1104/pp.112.212589
Young TE, Ling J, Geisler-lee CJ, Tanguay RL, Caldwell C, Gallie DR (2008) Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant Physiol 58:489–496. https://doi.org/10.1104/pp.010160.1
Zhang N, Belsterling B, Raszewski J, Tonsor SJ (2015) Natural populations of Arabidopsis thaliana differ in seedling responses to high temperature stress. AoB Plants 7:plv101. https://doi.org/10.1093/aobpla/plv101
Zhang SS, Yang H, Ding L, Song ZT, Ma H, Chang F, Liu JX (2017) Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in arabidopsis. Plant Cell 29:1007–1023. https://doi.org/10.1105/tpc.16.00916
Zinta G, Abdelgawad H, Peshev D, Weedon JT, Van Den Ende W, Nijs I, Janssens IA, Beemster GTS, Asard H (2018) Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2. J Exp Bot 69:2159–2170. https://doi.org/10.1093/jxb/ery055
Acknowledgements
AG is thankful to all his former students who have contributed to research on Hsp100 in his laboratory. Special thanks are due to Sneh Lata Singla-Pareek, Ashwani Pareek, Deepika Minhas, Himanshu Dubey, Sangeeta Agarwal, Chandan Sahi, Amanjot Singh, Dheeraj Mittal, Ratnesh Chandra Mishra, Dhruv Lavania, Richa Babbar and Garima Singh who worked on Hsp100 proteins or related aspects in their Ph.D. thesis and scores of students who did Masters or were post-doctoral and/or short-term fellows in the laboratory. The research funding received from DBT, DST and NASF (ICAR), Government of India, to AG are gratefully acknowledged. AG is thankful to SERB, DST for the award of J.C. Bose fellowship.
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We wish to honor the long-standing efforts put by Professor Elizabeth Vierling, University of Massachusetts, USA for the characterization of Hsp101 and sHsps of Arabidopsis. One of us (SK-A) had the privilege of working in her laboratory as a post-doctoral fellow during 2002–2003 which is thankfully acknowledged. In a recent mail to one of us (AG), she writes, “…… from my side I feel that I have worked on these proteins for over 35 years and will retire before I know what they really do!”.
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Kumar, R., Khungar, L., Shimphrui, R. et al. AtHsp101 research sets course of action for the genetic improvement of crops against heat stress. J. Plant Biochem. Biotechnol. 29, 715–732 (2020). https://doi.org/10.1007/s13562-020-00624-2
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DOI: https://doi.org/10.1007/s13562-020-00624-2