Abstract
Plant heat shock transcription factors (Hsfs) are commonly found to be involved in various stress responses. Several Hsfs displayed dwarf phenotype while conferred stress tolerance when over-expressed. However, the underlying mechanisms were not fully understood. Here we report the cloning and characterization of an Hsf (BhHsf1) from the resurrection plant Boea hygrometrica. Drought, heat and wound can induce BhHsf1 expression. The over-expression of BhHsf1 conferred growth retardation and stress tolerance in both Arabidopsis and tobacco. Evidence was presented to show that the growth retardation of aerial organs in the transgenic plants was resulted from the reduction of cell proliferation. Gene expression profiling using microarray hybridization and pathway analysis showed that Hsps and stress-associated genes were induced whereas the genes related to DNA replication and mitotic cell cycle were down-regulated in BhHsf1 over-expression Arabidopsis, which was in consistence with the observation of the impaired nuclear endoreduplication. Taking together, our results suggest that BhHsf1 may play dual roles in mediating the processes in heat stress tolerance and growth retardation via regulation of target genes related to stress protection and mitotic cell cycle.
Similar content being viewed by others
References
Anastasiou E, Lenhard M (2007) Growing up to one’s standard. Curr Opin Plant Biol 10:63–69. doi:10.1016/j.pbi.2006.11.002
Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Doring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58. doi:10.1080/07352680590910410
Bertrand C, Bergounioux C, Domenichini S, Delarue M, Zhou DX (2003) Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J Biol Chem 278:28246–28251. doi:10.1074/jbc.M302787200
Bockel C (2001) Isolation of genes expressed during early dehydration and detailed molecular analysis of Cp-Hsf1, a new Hsf-homologue, from the resurrection plant Craterostigma plantagineum. Dissertation, University of Cologne
Breuer C, Stacey NJ, West CE, Zhao Y, Chory J, Tsukaya H, Azumi Y, Maxwell A, Roberts K, Sugimoto-Shirasu K (2007) Bin4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell 19:3655–3668. doi:10.1105/tpc.107.054833
Chang CC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499–511. doi:10.1111/j.1365-313X.2004.02066.x
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. doi:10.1104/pp.106.091322
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x
Cockcroft CE, den Boer BG, Healy JM, Murray JA (2000) Cyclin D control of growth rate in plants. Nature 405:575–579. doi:10.1038/35014621
Collett H, Shen A, Gardner M, Farrant JM, Denby KJ, Illing N (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiol Plant 122:39–53. doi:10.1111/j.1399-3054.2004.00381.x
Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508. doi:10.1046/j.1365-313x.1999.00620.x
De Almeida ERR, Gossele V, Muller CG, Dockx J, Reynaerts A, Botterman J, Krebbers E, Timko MP (1989) Transgenic expression of two marker genes under the control of an Arabidopsis RBCS promoter: sequences encoding the Rubisco transit peptide increase expression levels. Mol Gen Genet 218:78–86. doi:10.1007/BF00330568
De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668. doi:10.1105/tpc.13.7.1653
Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870. doi:10.1038/sj.embor.7401043
Fleury D, Himanen K, Cnops G, Nelissen H, Boccardi TM, Maere S, Beemster GT, Neyt P, Anami S, Robles P, Micol JL, Inze D, Van Lijsebettens M (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19:417–432. doi:10.1105/tpc.106.041319
Frisch DA, Harris-Haller LW, Yokubaitis NT, Thomas TL, Hardin SH, Hall TC (1995) Complete sequence of the binary vector Bin 19. Plant Mol Biol 27:405–409. doi:10.1007/BF00020193
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993. doi:10.1073/pnas.0505667103
Gaff DF (1971) Desiccation-tolerant flowering plants in Southern Africa. Science 174:1033–1034. doi:10.1126/science.174.4013.1033
Gaitanaris GA, Papavassiliou AG, Rubock P, Silverstein SJ, Gottesman ME (1990) Renaturation of denatured lambda repressor requires heat shock proteins. Cell 61:1013–1020. doi:10.1016/0092-8674(90)90066-N
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051
Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA 96:13732–13737
Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351. doi:10.1105/tpc.004960
Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78. doi:10.1111/j.1365-313X.2005.02429.x
Hu Y, Bao F, Li J (2000) Promotive effect of brassinosteroids on cell division involves a distinct cycd3-induction pathway in Arabidopsis. Plant J 24:693–701. doi:10.1111/j.1365-313X.2000.00915.x
Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci 115:973–982
Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-della signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470. doi:10.1104/pp.107.103788
Jing Y, Cui D, Bao F, Hu Z, Qin Z, Hu Y (2009) Tryptophan deficiency affects organ growth by retarding cell expansion in Arabidopsis. Plant J 57:511–521. doi:10.1111/j.1365-313X.2008.03706.x
Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357. doi:10.1105/tpc.010362
Kapila J, De Rycke R, Van Montagu M, Angenon G (1997) An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122:101–108
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291. doi:10.1038/7036
Kotak S, Vierling E, Baumlein H, von Koskull-Doring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19:182–195. doi:10.1105/tpc.106.048165
Li C, Chen Q, Gao X, Qi B, Chen N, Xu S, Chen J, Wang X (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China C Life Sci 48:540–550. doi:10.1360/062005-119
Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463. doi:10.1046/j.1365-313X.1995.08030457.x
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Mansour KS, Hallet JN (2001) Effect of desiccation on DNA synthesis and the cell cycle of the moss polytrichum formosum. New Phytol 87:315–324. doi:10.1111/j.1469-8137.1981.tb03202.x
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16:1555–1567. doi:10.1101/gad.228802
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. doi:10.1016/j.tplants.2004.08.009
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539. doi:10.1016/S1369-5266(00)00212-0
Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14:110–117. doi:10.1016/j.tplants.2008.11.007
Neale AD, Blomstedt CK, Bronson P, Le T-N, Guthridge K, Evans J, Gaff DF, Hamill JD (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell Environ 23:265–277. doi:10.1046/j.1365-3040.2000.00548.x
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547. doi:10.1111/j.1365-313X.2006.02889.x
Nover L, Scharf KD, Gagliardi D, Vergne P, Czarnecka-Verner E, Gurley WB (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1:215–223
Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189
Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383. doi:10.1093/jxb/erm184
Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100. doi:10.1023/A:1026550808557
Osorio J, Osorio ML, Chaves MM, Pereira JS (1998) Water deficits are more important in delaying growth than in changing patterns of carbon allocation in Eucalyptus globulus. Tree Physiol 18:363–373. doi:10.1093/treephys/18.6.363
Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schoffl F (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136:3148–3158. doi:10.1104/pp.104.042606
Prieto-Dapena P, Castano R, Almoguera C, Jordano J (2008) The ectopic overexpression of a seed-specific transcription factor, HaHsfA9, confers tolerance to severe dehydration in vegetative organs. Plant J 54:1004–1014. doi:10.1111/j.1365-313X.2008.03465.x
Randall HC, Sinclair TR (1988) Sensitivity of soybean leaf development to water deficits. Plant Cell Environ 11:835–839. doi:10.1111/j.1365-3040.1988.tb01909.x
Rose AB, Elfersi T, Parra G, Korfa I (2008) Promoter-proximal introns in Arabidopsis thaliana are enriched in dispersed signals that elevate gene expression. Plant Cell 20:543–551. doi:10.1105/tpc.107.057190
Schnittger A, Weinl C, Bouyer D, Schobinger U, Hu lskamp M (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15:303–315. doi:10.1105/tpc.008342
Setter TL, Flannigan BA (2001) Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J Exp Bot 52:1401–1408. doi:10.1093/jexbot/52.360.1401
Shao HB, Liang ZS, Shao MA (2005) LEA proteins in higher plants: structure, function, gene expression and regulation. Colloids Surf B 45:131–135. doi:10.1016/j.colsurfb.2005.07.017
Sheffield WP, Shore GC, Randall SK (1990) Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence. J Biol Chem 265:11069–11076
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426. doi:10.1046/j.0960-7412.2001.01227.x
Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496. doi:10.1146/annurev.arplant.57.032905.105320
Tsukaya H (2008) Controlling size in multicellular organs: focus on the leaf. PLoS Biol 6:e174. doi:10.1371/journal.pbio.0060174
Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812. doi:10.1007/s00114-007-0254-y
von Koskull-Doring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12:452–457. doi:10.1016/j.tplants.2007.08.014
Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15:501–510. doi:10.1046/j.1365-313X.1998.00231.x
Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 24:613–623. doi:10.1111/j.1365-313X.2000.00899.x
Wang LL, Shang HH, Liu YX, Zheng MZ, Wu RH, Phillips J, Bartels D, Deng X (2009) A role for a cell wall localized glycine-rich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol. Available via doi: 10.1111/j.1438-8677.2008.00187.x
West G, Inze D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058. doi:10.1104/pp.104.040022
Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139. doi:10.1046/j.1365-3040.2002.00782.x
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227:957–967. doi:10.1007/s00425-007-0670-4
Yoshida T, Sakuma Y, Todaka D, Maruyama K, Qin F, Mizoi J, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2008) Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem Biophys Res Commun 368:515–521. doi:10.1016/j.bbrc.2008.01.134
Acknowledgments
We thank Dr Takumi Nishiuchi, Division of Functional Genomics, Advanced Science Research Center, Kanazawa University for providing control seeds. This project was founded by National Natural Science Foundation of China (No. 30400027) and National High Technology Research and Development Program of China (863 Program) (No. 2007AA021403).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
11103_2009_9538_MOESM2_ESM.tif
Fig. S1 The promoter sequence of BhHsf1. Cis-elements predicted by PLACE software were shown shaded or underlined; start codon (ATG) was labelled with rectangle. (TIFF 816 kb)
Rights and permissions
About this article
Cite this article
Zhu, Y., Wang, Z., Jing, Y. et al. Ectopic over-expression of BhHsf1, a heat shock factor from the resurrection plant Boea hygrometrica, leads to increased thermotolerance and retarded growth in transgenic Arabidopsis and tobacco. Plant Mol Biol 71, 451 (2009). https://doi.org/10.1007/s11103-009-9538-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11103-009-9538-2