Abstract
Considering global warming, it is of critical interest to understand in detail how plants withstand elevated temperatures and drought. Heat shock proteins (HSP) are involved in cellular response to both factors. HSP70 and HSP90 are multigene families in plants that function as molecular chaperones throughout the organism's tolerance range. However, the roles of individual members under water deficit are much less understood compared to heat shock response. In this study, transcriptional profiling of 12 HSP70s and 7 HSP90s in Arabidopsis thaliana (L.) Heynh. seedlings within wide dose ranges of high temperature and dehydration was conducted by RT-PCR, and roles of distinct inducible and constitutive members in tolerance were evaluated using loss-of-function mutants. The cellular responses to both treatments included strong factor-specific induction of inducible members and mild up-regulation of most constitutive members of various subcellular compartments. Differences in their kinetics, including baseline, time course and magnitude of changes, indicate specific functions of individual members. A significant complement to the cytosolic HSP transcript pool was created through differential expression of three inducible genes: AtHSP70-4 was highly induced in both cases, whereas induction of AtHSP70-5 and AtHSP90-1 was strong at heat shock and barely detectable or absent during dehydration. Nevertheless, analysis of knockout plants showed that AtHSP70-5 and AtHSP90-1 not only significantly contributed to the seed and seedling thermotolerance, but also substantially supported the growth activity under water deficit, when their expression remained negligible. These results suggested that inducible HSP70 and HSP90 at different levels of their expression perform specialized functions in protecting cells under adverse conditions.
Similar content being viewed by others
Abbreviations
- ER:
-
Endoplasmic reticulum
- HSP:
-
Heat shock proteins
- MS:
-
Murashige and Skoog mineral salt complex
- SE:
-
Standard error
- WT:
-
Wild type
References
Alvim FC, Carolino SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126:1042–1054. https://doi.org/10.1104/pp.126.3.1042
Ambrosone A, Giacomo M, Leone A, Grillo MS, Costa A (2013) Identification of early induced genes upon water deficit in potato cell culture by cDNA-AFLP. J Plant Res 126:169–178. https://doi.org/10.1007/s10265-012-0505-7
Augustine SM, Narayan JA, Syamaladevi DP, Appunu C, Chakravarthi M, Ravichandran V (2015) Erianthus arundinaceus HSP70 (EaHSP70) overexpression increases drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Sci 232:23–34. https://doi.org/10.1016/j.plantsci.2014.12.012
Banti V, Loreti E, Novi G, Santaniello A, Alpi A, Perata P (2008) Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ 31:1029–1037. https://doi.org/10.1111/j.1365-3040.2008.01816.x
Bedulina DS, Evgenev MB, Timofeyev MA, Protopopova MV, Garbuz DG, Pavlichenko VV, Luckenbach T, Shatilina ZM, Axenov-Gribanov DV, Gurkov AN, Sokolova IM, Zatsepina OG (2013) Expression patterns and organization of the hsp70 genes correlate with thermotolerance in two congener endemic amphipod species (Eulimnogammarus cyaneus and E. verrucosus) from Lake Baikal. Mol Ecol 22:1416–1430. https://doi.org/10.1111/mec.12136
Bobrownyzky J (2006) A method for the imitation of drought stress in Arabidopsis thaliana (L.) Heynh. Plant Introd 1:98–105
Bowen J, Lay-Yee M, Plummer K, Ferguson I (2002) The heat shock response is involved in thermotolerance in suspension-cultured apple fruit cells. J Plant Physiol 159:599–606. https://doi.org/10.1078/0176-1617-0752
Cazalé AC, Clément M, Chiarenza S, Roncato MA, Pochon N, Creff A, Marin E, Leonhardt N, Noël LD (2009) Altered expression of cytosolic/nuclear HSC70-1 molecular chaperone affects development and abiotic stress tolerance in Arabidopsis thaliana. J Exp Bot 60(9):2653–2664. https://doi.org/10.1093/jxb/erp109
Chaudhary R, Baranwal VK, Kumar R, Sircar D, Chauhan H (2019) Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development. Funct Integr Genom 19:1007–1022. https://doi.org/10.1007/s10142-019-00695-y
Clément M, Leonhardt N, Droillard M, Reiter I, Montillet J, Genty B, Laurière C, Nussaume L, Noël LD (2011) The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiol 156:1481–1492. https://doi.org/10.1104/pp.111.174425
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. https://doi.org/10.1146/annurev.physiol.61.1.243
Feller U, Vaseva II (2014) Extreme climatic events: impacts of drought and high temperature on physiological processes in agronomically important plants. Front Environ Sci 2:39. https://doi.org/10.3389/fenvs.2014.00039
Grigorova B, Vaseva II, Demirevska K, Feller U (2011) Expression of selected heat shock proteins after individually applied and combined drought and heat stress. Acta Physiol Plant 33:2041–2049. https://doi.org/10.1007/s11738-011-0733-9
Haralampidis K, Miliony D, Rigas S, Hatzopoulos P (2002) Combinatorial interaction of cis elements specify the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129:1138–1149. https://doi.org/10.1104/pp.004044
Hoekstra LA, Montooth KL (2013) Inducing extra copies of the Hsp70 gene in Drosophila melanogaster increases energetic demand. BMC Evol Biol 13:68. https://doi.org/10.1186/1471-2148-13-68
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. https://doi.org/10.1016/j.plantsci.2009.01.016
Jungkunz I, Link K, Vogel F, Voll LM, Sonnewald S, Sonnewald U (2011) AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. Plant J 66:983–995. https://doi.org/10.1111/j.1365-313X.2011.04558.x
Korres NE, Norsworthy JK, Tehranchian P, Gitsopoulos TK, Loka DA, Oosterhuis DM, Gealy DR, Moss SR, Burgos NR, Miller MR, Palhano M (2016) Cultivars to face climate change effects on crops and weeds: a review. Agron Sustain Dev 36:1–22. https://doi.org/10.1007/s13593-016-0350-5
Kozeko LY (2014) Changes in heat-shock protein synthesis and thermotolerance of Arabidopsis thaliana seedlings resulting from Hsp90 inhibition by geldanamycin. Cell Tissue Biol 8(5):416–422. https://doi.org/10.1134/S1990519X14050046
Kozeko L (2019) The role of HSP90 chaperones in stability and plasticity of ontogenesis of plants under normal and stressful conditions (Arabidopsis thaliana). Cytol Genet 53(2):143–161. https://doi.org/10.3103/S0095452719020063
Kozeko LY, Buy DD, Pirko YV, Blume YB, Kordyum EL (2018) Clinorotation affects induction of the heat shock response in Arabidopsis thaliana seedlings. Gravit Space Res 6(1):2–9
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
Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147. https://doi.org/10.1016/j.cell.2009.11.006
Landi S, Capasso G, Ben Azaiez FE, Jallouli S, Ayadi S, Trifa Y, Esposito S (2019) Different roles of heat shock proteins (70 kDa) during abiotic stresses in barley (Hordeum vulgare) genotypes. Plants 8:248. https://doi.org/10.3390/plants8080248
Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761. https://doi.org/10.1104/pp.107.112060
Lee JH, Schöffl F (1996) An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol Gen Genet 252:11–19. https://doi.org/10.1007/s004389670002
Leng L, Liang Q, Jiang J, Zhang C, Hao Y, Wang X, Su W (2017) A subclass of HSP70s regulate development and abiotic stress responses in Arabidopsis thaliana. J Plant Res 130:349–363. https://doi.org/10.1007/s10265-016-0900-6
Li Z, Long R, Zhang T, Wang Z, Zhang F, Yang Q, Kang J (2017) Molecular cloning and functional analysis of the drought tolerance gene MsHSP70 from alfalfa (Medicago sativa L.). J Plant Res 130:387–396. https://doi.org/10.1007/s10265-017-0905-9
Lim CJ, Yang KA, Hong JK, Choi JS, Yun DJ, Hong JC, Chung WS, Lee SY, Cho MJ, Lim CO (2006) Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. J Plant Res 119:373–383. https://doi.org/10.1007/s10265-006-0285-z
Lin B, Wang J, Liu H, Chen R, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6(3):201–208. https://doi.org/10.1379/1466-1268(2001)006%3c0201:gaoths%3e2.0.co;2
Ludwig-Müller J, Krishna P, Forreiter C (2000) A glucosinolate mutant of Arabidopsis is thermosensitive and defective in cytosolic Hsp90 expression after heat stress. Plant Physiol 123(3):949–958. https://doi.org/10.1104/pp.123.3.949
Montero-Barrientos M, Hermosa R, Cardoza RE, Gutiérrez S, Nicolás C, Monte E (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol 167(8):659–665. https://doi.org/10.1016/j.fgb.2008.09.003
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. https://doi.org/10.1104/pp.103.033431
Rozenzvieg D, Elmaci C, Samach A, Lurie S, Porat R (2004) Isolation of four heat shock protein cDNAs from grapefruit peel tissue and characterization of their expression in response to heat and chilling temperature stresses. Physiol Plant 121:421–428. https://doi.org/10.1111/j.1399-3054.2004.00334.x
Samakovli D, Thanou A, Valmas C, Hatzopoulos P (2007) Hsp90 canalizes developmental perturbation. J Exp Bot 58:3515–3524. https://doi.org/10.1093/jxb/erm191
Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS ONE 7:1–15. https://doi.org/10.1371/journal.pone.0000648
Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochimica et Biophisica Acta 1819:104–119. https://doi.org/10.1016/j.bbagrm.2011.10.002
Schumann W (2001) Heat shock response. eLS. https://doi.org/10.1038/npg.els.0000395
Silva-Correia J, Freitas S, Tavares RM, Lino-Neto T, Azevedo H (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10:7. https://doi.org/10.1186/1746-4811-10-7
Song A, Zhu X, Chen F, Gao H, Jiang J, Chen S (2014) A chrysanthemum heat shock protein confers tolerance to abiotic stress. Int J Mol Sci 15(3):5063–5078. https://doi.org/10.3390/ijms15035063
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037. https://doi.org/10.1146/annurev.physiol.61.1.243
Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol 132(2):979–987. https://doi.org/10.1104/pp.102.019398
Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126:789–800. https://doi.org/10.1104/pp.126.2.789
Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genom 8:125. https://doi.org/10.1186/1471-2164-8-125
Taipale M, Jarosz D, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528. https://doi.org/10.1038/nrm2918
Tichá T, Samakovli D, Kuchařová A, Vavrdová T, Šamaj J (2020) Multifaceted roles of HEAT SHOCK PROTEIN 90 molecular chaperones in plant development. J Exp Bot 71(14):3966–3985. https://doi.org/10.1093/jxb/eraa177
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 103:2069–2083. https://doi.org/10.1111/tpj.14883
Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiol Biochem Zool 73(2):249–256. https://doi.org/10.1086/316740
Valente MA, Faria JA, Soares-Ramos JR, Reis PA, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MA, Fietto LG, Loureiro ME, Aragão FJ, Fontes EP (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J Exp Bot 60(2):533–546. https://doi.org/10.1093/jxb/ern296
Wang X, Yan B, Min S, Wei Z, Zekria D, Wang H, Kai G (2015) Overexpression of a Brassica campestris HSP70 in tobacco confers enhanced tolerance to heat stress. Protoplasma 253:1–9. https://doi.org/10.1007/s00709-015-0867-5
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” Browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2(8):e718. https://doi.org/10.1371/journal.pone.0000718
Yamada K, Fukao Y, Hayashi M, Fukazawa M, Suzuki I, Nishimura M (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J Biol Chem 282(52):37794–37804. https://doi.org/10.1074/jbc.M707168200
Yer EN, Baloglu MC, Ziplar UT, Ayan S, Unver T (2016) Drought-responsive Hsp70 gene analysis in Populus at genome-wide level. Plant Mol Biol Rep 34:483–500. https://doi.org/10.1007/s11105-015-0933-3
Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, Zhang X (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166:851–861. https://doi.org/10.1016/j.jplph.2008.11.007
Acknowledgements
This work was funded by the National Academy of Sciences of Ukraine (Project 0112U000059). The author thanks Prof. Elizabeth Kordyum for support and invaluable discussion and Dr. J. Bobrownyzky for providing the characteristics of the drought simulation model.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Esposito.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kozeko, L. Different roles of inducible and constitutive HSP70 and HSP90 in tolerance of Arabidopsis thaliana to high temperature and water deficit. Acta Physiol Plant 43, 58 (2021). https://doi.org/10.1007/s11738-021-03229-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-021-03229-x