Skip to main content
Log in

Overexpression of C-Repeat Binding Factor1 (CBF1) Gene Enhances Heat Stress Tolerance in Arabidopsis

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

High temperature affects plant growth, development, and seed production. We generated Arabidopsis transgenic plants overexpressing abiotic stress-tolerance associated genes (CBF1, GolS1, NDPK2, YUC6, and PRE1) to investigate the effects of these genes on heat stress (HS) tolerance. We evaluated thermotolerance by assessing the survival rate of T2 seedlings under acute HS conditions. C-repeat binding factor 1-overexpressing (CBF1-OE) plants exhibited drastically improved HS tolerance, whereas overexpression of the other examined genes yielded marginal effects. Consistent with the ability of CBF1 to regulate transcription, we found that the transcription of several heat-shock inducible genes was remarkably increased in CBF1-OE plants under HS conditions. Furthermore, the expression of several reactive oxygen species (ROS)-responsive genes related to oxidative stress was notably upregulated in CBF1-OE plants. Thus, the thermotolerance of CBF1-OE plants is at least partly associated with the elevated expression of several HS-inducible and ROS-responsive genes. Our study showed that CBF1 plays a role in increasing HS tolerance in Arabidopsis in addition to its previously established roles in cold/drought tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of Data and Material

The authors confirm that data supporting the findings in this study are available within the article and its supplementary materials.

Code Availability

Not applicable.

References

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Begcy K, Nosenko T, Zhou LZ, Fragner L, Weckwerth W, Dresselhaus T (2019) Male sterility in maize after transient heat stress during the tetrad stage of pollen development. Plant Physiol 181:683–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Article  PubMed  PubMed Central  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    Article  CAS  PubMed  Google Scholar 

  • Cha JY, Kim WY, Kang SB, Kim JI, Baek D, Jung IJ, Kim MR, Li N, Kim HJ, Nakajima M, Asami T, Sabir JS, Park HC, Lee SY, Bohnert HJ, Bressan RA, Pardo JM, Yun DJ (2015) A novel thiol-reductase activity of Arabidopsis YUC6 confers drought tolerance independently of auxin biosynthesis. Nat Commun 6:8041

    Article  CAS  PubMed  Google Scholar 

  • Chauhan H, Khurana N, Agarwal P, Khurana JP, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. PLoS ONE 8:e79577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • de Pinto MC, Locato V, Paradiso A, De Gara L (2015) Role of redox homeostasis in thermo-tolerance under a climate change scenario. Ann Bot 116:487–496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dou H, Xv K, Meng Q, Li G, Yang X (2015) Potato plants ectopically expressing Arabidopsis thaliana CBF3 exhibit enhanced tolerance to high-temperature stress. Plant Cell Environ 38:61–72

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Al Mahmud J, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants-Basel 8:384

    Article  CAS  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong SW, Lee W, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132:757–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Lee S, Yang KY, Kim YM, Park SY, Kim SY, Soh MS (2006) Overexpression of PRE1 and its homologous genes activates Gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol 47:591–600

    Article  CAS  PubMed  Google Scholar 

  • Li XM, Chao DY, Wu Y et al (2015) Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47:827–833

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620

    Article  CAS  PubMed  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics 283:185–196

    Article  CAS  PubMed  Google Scholar 

  • Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358–363

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65

    Article  CAS  PubMed  Google Scholar 

  • Oh SA, Hoai TNT, Park HJ, Zhao M, Twell D, Honys D, Park SK (2020) MYB81, a microspore-specific GAMYB transcription factor, promotes pollen mitosis I and cell lineage formation in Arabidopsis. Plant J 101:590–603

    Article  CAS  PubMed  Google Scholar 

  • Panchuk II, Volkov RA, Schoffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101:9971–9975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thornashow MF, Chen THH (2007) Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J 5:591–604

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoffl F, Prandl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiol 117:1135–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schramm F, Larkindale J, Kiehlmann E, Ganguli A, Englich G, Vierling E, von Koskull-Doring P (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53:264–274

    Article  CAS  PubMed  Google Scholar 

  • Sgobba A, Paradiso A, Dipierro S, De Gara L, de Pinto MC (2015) Changes in antioxidants are critical in determining cell responses to short- and long-term heat stress. Physiol Plant 153:68–78

    Article  CAS  PubMed  Google Scholar 

  • Shen H, Zhong X, Zhao F et al (2015) Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat Biotechnol 33:996–1003

    Article  CAS  PubMed  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suo H, Ma Q, Ye K, Yang C, Tang Y, Hao J, Zhang ZJ, Chen M, Feng Y, Nian H (2012) Overexpression of AtDREB1A causes a severe dwarf phenotype by decreasing endogenous gibberellin levels in soybean [Glycine max (L.) Merr]. PLoS ONE 7:e45568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Miller G, Sejima H, Harper J, Mittler R (2013) Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2. J Exp Bot 64:253–263

    Article  CAS  PubMed  Google Scholar 

  • Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, De Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol 134:1100–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S, Ravanat JL, Hegie A, Triantaphylides C, Shulaev V, Van Montagu MC, Van Breusegem F, Mittler R (2011) Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci USA 108:1711–1716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkov RA, Panchuk II, Mullineaux PM, Schoffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhao CZ, Zhang ZJ, Xie SJ, Si T, Li YY, Zhu JK (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol 171:2744–2759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. Jian-Kang Zhu and Prof. Byeong-Ha Lee (Sogang University, South Korea) for providing the cbf1 mutant edited by the CRISPR/Cas9 system (Zhao et al. 2016). This research was supported by Kyungpook National University Development Project Research Fund, 2018.

Author information

Authors and Affiliations

Authors

Contributions

SDY and MHK performed the experiments and wrote the manuscript. SAO, MSS and SKP designed the experiment and analyzed the data. SKP supervised the project and complemented the writing.

Corresponding author

Correspondence to Soon Ki Park.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 461 KB)

Supplementary file2 (PDF 95 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yun, S.D., Kim, MH., Oh, S.A. et al. Overexpression of C-Repeat Binding Factor1 (CBF1) Gene Enhances Heat Stress Tolerance in Arabidopsis. J. Plant Biol. 65, 253–260 (2022). https://doi.org/10.1007/s12374-022-09350-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-022-09350-9

Keywords

Navigation