Voyaging around ClpB/Hsp100 proteins and plant heat tolerance
Keywords:
Aggregates, ClpB/Hsp100, plant, protein, renaturation, thermotolerance
Abstract
Temperature is one of the key physical parameters that fine tunes plant growth and development. However, above the optimal range, it can negatively affect the physiology of plants. Supraoptimal temperature brings incongruity in cellular proteostasis resulting in the build-up of insoluble toxic protein aggregates. To prevent protein misfolding and aggregation, cells deploy different strategies including synthesis of heat shock proteins (Hsp) belonging to different families, like sHsps, Hsp40, Hsp60, Hsp70. Once these aggregates are formed, their dissolution and recovery of the functional proteins occurs by the action of Caseinolytic Protease B (ClpB)/ Hsp100. ClpB/Hsp100 proteins are evolutionarily conserved in bacteria, fungi and plants. This highlights the extreme importance of ClpB function during heat stress (HS) in plants. ClpB system appears indispensable, as mutant bacteria, yeast as well as plants lacking ClpB protein fail to survive HS. Genetic expression of ClpB proteins is modulated both by high temperature as well as developmental cues. Plant contains three isoforms of ClpB/Hsp100, one each localized to cytoplasm (ClpB-C), chloroplast (ClpB-P) and mitochondria (ClpB-M), against one in bacteria and two in yeast. It is particularly the ClpB-C protein that governs the thermotolerance response in plants. This review introduces plant ClpB proteins, summarizes the knowledge gained hitherto in ClpB biology, critically analyzes the recent findings and brings forth the areas requiring thrust in the upcoming research on ClpBs.
References
Agarwal, M., Sahi, C., Katiyar-Agarwal, S., Agarwal, S., Young, T., Gallie, D.R., Sharma, V.M., Ganesan, K., and 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 molecular biology 51, 543-553.
Bita, C.E., and Gerats, T. (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in plant science 4, 273.
Campbell, J.L., Klueva, N.Y., Zheng, H.G., Nieto-Sotelo, J., Ho, T.D., and Nguyen, H.T. (2001). Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA(1). Biochimica et biophysica acta 1517, 270-277.
Carr, T., Wang, Y., Huang, Z., Yeakley, J.M., Fan, J.B., and Whitham, S.A. (2006). Tobamovirus infection is independent of HSP101 mRNA induction and protein expression. Virus research 121, 33-41.
Dinkova, T.D., Zepeda, H., Martinez-Salas, E., Martinez, L.M., Nieto-Sotelo, J., and de Jimenez, E.S. (2005). Cap-independent translation of maize Hsp101. The Plant journal : for cell and molecular biology 41, 722-731.
Echevarria-Zomeno, S., Yanguez, E., Fernandez-Bautista, N., Castro-Sanz, A.B., Ferrando, A., and Castellano, M.M. (2013). Regulation of Translation Initiation under Biotic and Abiotic Stresses. Int J Mol Sci 14, 4670-4683.
Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D.S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40, D1178-1186.
Gottesman, S., Clark, W.P., and Maurizi, M.R. (1990). The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clp-specific substrate. The Journal of biological chemistry 265, 7886-7893.
Hong, S.W., and Vierling, E. (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences of the United States of America 97, 4392-4397.
Hong, S.W., and Vierling, E. (2001). Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. The Plant journal : for cell and molecular biology 27, 25-35.
Hwang, B.J., Park, W.J., Chung, C.H., and Goldberg, A.L. (1987). Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proceedings of the National Academy of Sciences of the United States of America 84, 5550-5554.
Katayama-Fujimura, Y., Gottesman, S., and Maurizi, M.R. (1987). A multiple-component, ATP-dependent protease from Escherichia coli. The Journal of biological chemistry 262, 4477-4485.
Katiyar-Agarwal, S., Agarwal, M., and Grover, A. (2003). Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant molecular biology 51, 677-686.
Kim, M., Lee, U., Small, I., des Francs-Small, C.C., and Vierling, E. (2012). Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. The Plant cell 24, 3349-3365.
Kitagawa, M., Wada, C., Yoshioka, S., and Yura, T. (1991). Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). Journal of bacteriology 173, 4247-4253.
Konieczny, I., and Liberek, K. (2002). Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. The Journal of biological chemistry 277, 18483-18488.
Kotak, S., Vierling, E., Baumlein, H., and von Koskull-Doring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. The Plant cell 19, 182-195.
Krajewska, J., Arent, Z., Zolkiewski, M., and Kedzierska-Mieszkowska, S. (2018). Isolation and Identification of Putative Protein Substrates of the AAA+ Molecular Chaperone ClpB from the Pathogenic Spirochaete Leptospira interrogans. Int J Mol Sci 19.
Krzewska, J., Langer, T., and Liberek, K. (2001). Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS letters 489, 92-96.
Kumar, S.V., and Wigge, P.A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147.
Lavania, D., Dhingra, A., and Grover, A. (2018). Analysis of transactivation potential of rice (Oryza sativa L.) heat shock factors. Planta 247, 1267-1276.
Lavania, D., Dhingra, A., Siddiqui, M.H., Al-Whaibi, M.H., and Grover, A. (2015). Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86, 100-108.
Lazaro-Mixteco, P.E., Nieto-Sotelo, J., Swatek, K.N., Houston, N.L., Mendoza-Hernandez, G., Thelen, J.J., and Dinkova, T.D. (2012). The Absence of Heat Shock Protein HSP101 Affects the Proteome of Mature and Germinating Maize Embryos. Journal of proteome research 11, 3246-3258.
Lee, U., Wie, C., Escobar, M., Williams, B., Hong, S.W., and Vierling, E. (2005). Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. The Plant cell 17, 559-571.
Lee, U., Rioflorido, I., Hong, S.W., Larkindale, J., Waters, E.R., and Vierling, E. (2006). The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. The Plant journal : for cell and molecular biology 49, 115-127.
Lee, Y.R., Nagao, R.T., and Key, J.L. (1994). A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. The Plant cell 6, 1889-1897.
Lin, M.Y., Chai, K.H., Ko, S.S., Kuang, L.Y., Lur, H.S., and 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 physiology 164, 2045-2053.
Ling, J., Wells, D.R., Tanguay, R.L., Dickey, L.F., Thompson, W.F., and Gallie, D.R. (2000). Heat shock protein HSP101 binds to the Fed-1 internal light regulator y element and mediates its high translational activity. The Plant cell 12, 1213-1227.
Mishra, R.C., and 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 physiology 166, 1646-1658.
Mishra, R.C., and Grover, A. (2016). ClpB/Hsp100 proteins and heat stress tolerance in plants. Crit Rev Biotechnol 36, 862-874.
Mishra, R.C., Richa, Singh, A., Tiwari, L.D., and 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.
Mogk, A., Tomoyasu, T., Goloubinoff, P., Rudiger, S., Roder, D., Langen, H., and Bukau, B. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. The EMBO journal 18, 6934-6949.
Myouga, F., Motohashi, R., Kuromori, T., Nagata, N., and Shinozaki, K. (2006). An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. The Plant journal : for cell and molecular biology 48, 249-260.
Nieto-Sotelo, J., Kannan, K.B., Martinez, L.M., and Segal, C. (1999). Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene 230, 187-195.
Nieto-Sotelo, J., Martinez, L.M., Ponce, G., Cassab, G.I., Alagon, A., Meeley, R.B., Ribaut, J.M., and Yang, R. (2002). Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. The Plant cell 14, 1621-1633.
Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., and van Wijk, K.J. (2013). ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. The Plant cell 25, 2276-2301.
Parsell, D.A., Kowal, A.S., Singer, M.A., and Lindquist, S. (1994). Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478.
Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S., and Cassman, K.G. (2004). Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101, 9971-9975.
Pontis, E., Sun, X.Y., Jornvall, H., Krook, M., and Reichard, P. (1991). ClpB proteins copurify with the anaerobic Escherichia coli reductase. Biochemical and biophysical research communications 180, 1222-1226.
Queitsch, C., Hong, S.W., Vierling, E., and Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant cell 12, 479-492.
Sanchez, Y., and Lindquist, S.L. (1990). HSP104 required for induced thermotolerance. Science 248, 1112-1115.
Sanchez, Y., Taulien, J., Borkovich, K.A., and Lindquist, S. (1992). Hsp104 is required for tolerance to many forms of stress. The EMBO journal 11, 2357-2364.
Schelin, J., Lindmark, F., and Clarke, A.K. (2002). The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology 148, 2255-2265.
Schirmer, E.C., Lindquist, S., and Vierling, E. (1994). An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. The Plant cell 6, 1899-1909.
Schoffl, F., Rieping, M., Baumann, G., Bevan, M., and Angermuller, S. (1989). The function of plant heat shock promoter elements in the regulated expression of chimaeric genes in transgenic tobacco. Mol Gen Genet 217, 246-253.
Schroda, M. (2004). The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast. Photosynthesis research 82, 221-240.
Singh, A., and Grover, A. (2010). Plant Hsp100/ClpB-like proteins: poorly-analyzed cousins of yeast ClpB machine. Plant molecular biology 74, 395-404.
Singh, A., Singh, U., Mittal, D., and Grover, A. (2010). Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC genomics 11, 95.
Singh, A., Mittal, D., Lavania, D., Agarwal, M., Mishra, R.C., and 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, N.K., and Grover, A. (2018). Mapping of domains of heat stress transcription factor OsHsfA6a responsible for its transactivation activity. Plant science : an international journal of experimental plant biology 274, 80-90.
Singla, S.L., and Grover, A. (1993). Antibodies raised against yeast HSP 104 cross-react with a heat- and abscisic acid-regulated polypeptide in rice. Plant molecular biology 22, 1177-1180.
Singla, S.L., Pareek, A., Kush, A.K., and Grover, A. (1998). Distribution patterns of 104 kDa stress-associated protein in rice. Plant molecular biology 37, 911-919.
Squires, C.L., Pedersen, S., Ross, B.M., and Squires, C. (1991). ClpB is the Escherichia coli heat shock protein F84.1. Journal of bacteriology 173, 4254-4262.
Tkach, J.M., and Glover, J.R. (2008). Nucleocytoplasmic trafficking of the molecular chaperone Hsp104 in unstressed and heat-shocked cells. Traffic 9, 39-56.
Tonsor, S.J., Scott, C., Boumaza, I., Liss, T.R., Brodsky, J.L., and Vierling, E. (2008). Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Molecular ecology 17, 1614-1626.
Watanabe, Y.H., Motohashi, K., Taguchi, H., and Yoshida, M. (2000). Heat-inactivated proteins managed by DnaKJ-GrpE-ClpB chaperones are released as a chaperonin-recognizable non-native form. The Journal of biological chemistry 275, 12388-12392.
Wells, D.R., Tanguay, R.L., Le, H., and Gallie, D.R. (1998). HSP101 functions as a specific translational regulatory protein whose activity is regulated by nutrient status. Genes Dev 12, 3236-3251.
Yang, J.Y., Sun, Y., Sun, A.Q., Yi, S.Y., Qin, J., Li, M.H., and Liu, J. (2006). The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant molecular biology 62, 385-395.
Young, T.E., Ling, J., Geisler-Lee, C.J., Tanguay, R.L., Caldwell, C., and Gallie, D.R. (2001). Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant physiology 127, 777-791.
Zolkiewski, M. (2006). A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61, 1094-1100.
Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodriguez, V.R., Asakura, Y., Sun, Q., and van Wijk, K.J. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Molecular & cellular proteomics : MCP 8, 1789-1810.
Bita, C.E., and Gerats, T. (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in plant science 4, 273.
Campbell, J.L., Klueva, N.Y., Zheng, H.G., Nieto-Sotelo, J., Ho, T.D., and Nguyen, H.T. (2001). Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA(1). Biochimica et biophysica acta 1517, 270-277.
Carr, T., Wang, Y., Huang, Z., Yeakley, J.M., Fan, J.B., and Whitham, S.A. (2006). Tobamovirus infection is independent of HSP101 mRNA induction and protein expression. Virus research 121, 33-41.
Dinkova, T.D., Zepeda, H., Martinez-Salas, E., Martinez, L.M., Nieto-Sotelo, J., and de Jimenez, E.S. (2005). Cap-independent translation of maize Hsp101. The Plant journal : for cell and molecular biology 41, 722-731.
Echevarria-Zomeno, S., Yanguez, E., Fernandez-Bautista, N., Castro-Sanz, A.B., Ferrando, A., and Castellano, M.M. (2013). Regulation of Translation Initiation under Biotic and Abiotic Stresses. Int J Mol Sci 14, 4670-4683.
Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D.S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40, D1178-1186.
Gottesman, S., Clark, W.P., and Maurizi, M.R. (1990). The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clp-specific substrate. The Journal of biological chemistry 265, 7886-7893.
Hong, S.W., and Vierling, E. (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences of the United States of America 97, 4392-4397.
Hong, S.W., and Vierling, E. (2001). Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. The Plant journal : for cell and molecular biology 27, 25-35.
Hwang, B.J., Park, W.J., Chung, C.H., and Goldberg, A.L. (1987). Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proceedings of the National Academy of Sciences of the United States of America 84, 5550-5554.
Katayama-Fujimura, Y., Gottesman, S., and Maurizi, M.R. (1987). A multiple-component, ATP-dependent protease from Escherichia coli. The Journal of biological chemistry 262, 4477-4485.
Katiyar-Agarwal, S., Agarwal, M., and Grover, A. (2003). Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant molecular biology 51, 677-686.
Kim, M., Lee, U., Small, I., des Francs-Small, C.C., and Vierling, E. (2012). Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. The Plant cell 24, 3349-3365.
Kitagawa, M., Wada, C., Yoshioka, S., and Yura, T. (1991). Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). Journal of bacteriology 173, 4247-4253.
Konieczny, I., and Liberek, K. (2002). Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. The Journal of biological chemistry 277, 18483-18488.
Kotak, S., Vierling, E., Baumlein, H., and von Koskull-Doring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. The Plant cell 19, 182-195.
Krajewska, J., Arent, Z., Zolkiewski, M., and Kedzierska-Mieszkowska, S. (2018). Isolation and Identification of Putative Protein Substrates of the AAA+ Molecular Chaperone ClpB from the Pathogenic Spirochaete Leptospira interrogans. Int J Mol Sci 19.
Krzewska, J., Langer, T., and Liberek, K. (2001). Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS letters 489, 92-96.
Kumar, S.V., and Wigge, P.A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147.
Lavania, D., Dhingra, A., and Grover, A. (2018). Analysis of transactivation potential of rice (Oryza sativa L.) heat shock factors. Planta 247, 1267-1276.
Lavania, D., Dhingra, A., Siddiqui, M.H., Al-Whaibi, M.H., and Grover, A. (2015). Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86, 100-108.
Lazaro-Mixteco, P.E., Nieto-Sotelo, J., Swatek, K.N., Houston, N.L., Mendoza-Hernandez, G., Thelen, J.J., and Dinkova, T.D. (2012). The Absence of Heat Shock Protein HSP101 Affects the Proteome of Mature and Germinating Maize Embryos. Journal of proteome research 11, 3246-3258.
Lee, U., Wie, C., Escobar, M., Williams, B., Hong, S.W., and Vierling, E. (2005). Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. The Plant cell 17, 559-571.
Lee, U., Rioflorido, I., Hong, S.W., Larkindale, J., Waters, E.R., and Vierling, E. (2006). The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. The Plant journal : for cell and molecular biology 49, 115-127.
Lee, Y.R., Nagao, R.T., and Key, J.L. (1994). A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. The Plant cell 6, 1889-1897.
Lin, M.Y., Chai, K.H., Ko, S.S., Kuang, L.Y., Lur, H.S., and 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 physiology 164, 2045-2053.
Ling, J., Wells, D.R., Tanguay, R.L., Dickey, L.F., Thompson, W.F., and Gallie, D.R. (2000). Heat shock protein HSP101 binds to the Fed-1 internal light regulator y element and mediates its high translational activity. The Plant cell 12, 1213-1227.
Mishra, R.C., and 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 physiology 166, 1646-1658.
Mishra, R.C., and Grover, A. (2016). ClpB/Hsp100 proteins and heat stress tolerance in plants. Crit Rev Biotechnol 36, 862-874.
Mishra, R.C., Richa, Singh, A., Tiwari, L.D., and 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.
Mogk, A., Tomoyasu, T., Goloubinoff, P., Rudiger, S., Roder, D., Langen, H., and Bukau, B. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. The EMBO journal 18, 6934-6949.
Myouga, F., Motohashi, R., Kuromori, T., Nagata, N., and Shinozaki, K. (2006). An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. The Plant journal : for cell and molecular biology 48, 249-260.
Nieto-Sotelo, J., Kannan, K.B., Martinez, L.M., and Segal, C. (1999). Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene 230, 187-195.
Nieto-Sotelo, J., Martinez, L.M., Ponce, G., Cassab, G.I., Alagon, A., Meeley, R.B., Ribaut, J.M., and Yang, R. (2002). Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. The Plant cell 14, 1621-1633.
Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., and van Wijk, K.J. (2013). ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. The Plant cell 25, 2276-2301.
Parsell, D.A., Kowal, A.S., Singer, M.A., and Lindquist, S. (1994). Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478.
Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S., and Cassman, K.G. (2004). Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101, 9971-9975.
Pontis, E., Sun, X.Y., Jornvall, H., Krook, M., and Reichard, P. (1991). ClpB proteins copurify with the anaerobic Escherichia coli reductase. Biochemical and biophysical research communications 180, 1222-1226.
Queitsch, C., Hong, S.W., Vierling, E., and Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant cell 12, 479-492.
Sanchez, Y., and Lindquist, S.L. (1990). HSP104 required for induced thermotolerance. Science 248, 1112-1115.
Sanchez, Y., Taulien, J., Borkovich, K.A., and Lindquist, S. (1992). Hsp104 is required for tolerance to many forms of stress. The EMBO journal 11, 2357-2364.
Schelin, J., Lindmark, F., and Clarke, A.K. (2002). The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology 148, 2255-2265.
Schirmer, E.C., Lindquist, S., and Vierling, E. (1994). An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. The Plant cell 6, 1899-1909.
Schoffl, F., Rieping, M., Baumann, G., Bevan, M., and Angermuller, S. (1989). The function of plant heat shock promoter elements in the regulated expression of chimaeric genes in transgenic tobacco. Mol Gen Genet 217, 246-253.
Schroda, M. (2004). The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast. Photosynthesis research 82, 221-240.
Singh, A., and Grover, A. (2010). Plant Hsp100/ClpB-like proteins: poorly-analyzed cousins of yeast ClpB machine. Plant molecular biology 74, 395-404.
Singh, A., Singh, U., Mittal, D., and Grover, A. (2010). Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC genomics 11, 95.
Singh, A., Mittal, D., Lavania, D., Agarwal, M., Mishra, R.C., and 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, N.K., and Grover, A. (2018). Mapping of domains of heat stress transcription factor OsHsfA6a responsible for its transactivation activity. Plant science : an international journal of experimental plant biology 274, 80-90.
Singla, S.L., and Grover, A. (1993). Antibodies raised against yeast HSP 104 cross-react with a heat- and abscisic acid-regulated polypeptide in rice. Plant molecular biology 22, 1177-1180.
Singla, S.L., Pareek, A., Kush, A.K., and Grover, A. (1998). Distribution patterns of 104 kDa stress-associated protein in rice. Plant molecular biology 37, 911-919.
Squires, C.L., Pedersen, S., Ross, B.M., and Squires, C. (1991). ClpB is the Escherichia coli heat shock protein F84.1. Journal of bacteriology 173, 4254-4262.
Tkach, J.M., and Glover, J.R. (2008). Nucleocytoplasmic trafficking of the molecular chaperone Hsp104 in unstressed and heat-shocked cells. Traffic 9, 39-56.
Tonsor, S.J., Scott, C., Boumaza, I., Liss, T.R., Brodsky, J.L., and Vierling, E. (2008). Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Molecular ecology 17, 1614-1626.
Watanabe, Y.H., Motohashi, K., Taguchi, H., and Yoshida, M. (2000). Heat-inactivated proteins managed by DnaKJ-GrpE-ClpB chaperones are released as a chaperonin-recognizable non-native form. The Journal of biological chemistry 275, 12388-12392.
Wells, D.R., Tanguay, R.L., Le, H., and Gallie, D.R. (1998). HSP101 functions as a specific translational regulatory protein whose activity is regulated by nutrient status. Genes Dev 12, 3236-3251.
Yang, J.Y., Sun, Y., Sun, A.Q., Yi, S.Y., Qin, J., Li, M.H., and Liu, J. (2006). The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant molecular biology 62, 385-395.
Young, T.E., Ling, J., Geisler-Lee, C.J., Tanguay, R.L., Caldwell, C., and Gallie, D.R. (2001). Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant physiology 127, 777-791.
Zolkiewski, M. (2006). A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61, 1094-1100.
Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodriguez, V.R., Asakura, Y., Sun, Q., and van Wijk, K.J. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Molecular & cellular proteomics : MCP 8, 1789-1810.
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2020-01-21
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