Skip to main content
SpringerLink
Log in

The ethylene response factor OsERF109 negatively affects ethylene biosynthesis and drought tolerance in rice

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Drought is an important factor limiting plant development and crop production. Dissecting the factors involved in this process is the key for enhancement of plant tolerance to drought stress by genetic approach. Here, we evaluated the regulatory function of a novel rice ethylene response factor (ERF) OsERF109 in drought stress. Expression of OsERF109 was rapidly induced by stress and phytohormones. Subcellular localization and transactivation assay demonstrated that OsERF109 was localized in nucleus and possessed transactivation activity. Transgenic plants overexpressing (OE) and knockdown with RNA interfering (RI) OsERF109 exhibited significantly reduced and improved drought resistance, respectively, indicating that OsERF109 negatively regulates drought resistance in rice. Furthermore, measurement by gas chromatography showed that ethylene contents were less in OE while more in RI lines than these in wild types, supporting the data of drought tolerance and water loss in transgenic lines. Quantitative real-time PCR analysis also proved the regulation of OsERF109 in the expression of OSACS6, OSACO2, and OsERF3, which have been identified to play important roles in ethylene biosynthesis. Based on these results, our data evidence that OsERF109 regulates drought resistance by affecting the ethylene biosynthesis in rice. Overall, our study reveals the negative role of OsERF109 in ethylene biosynthesis and drought tolerance in rice.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ABRE:

ABA-responsive elements

ACC:

1-Aminocyclopropane-1-carboxylic acid

AP2:

APETALA2

CaMV:

Cauliflower mosaic virus

cDNA:

DNA complementary to RNA

CRT:

C-repeat

DRE:

Dehydration responsive element

DREB:

Dehydration responsive element binding factor

ERF:

Ethylene response factor

GA:

Gibberellic acid

GFP:

Green fluorescent protein

GUS:

β-Glucuronidase

MS:

Murashige and Skoog

MYBRS:

MYC recognition site

MYCRS:

MYC recognition site

qPCR:

Quantitative real-time polymerase chain reaction

Trp:

Tryptophan

References

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    Article  CAS  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Tao L, Zeng L, VEGA-SANCHEZ ME, Umemura K, WANG GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein–protein interactions in rice. Mol Plant Pathol 7:417–427

    Article  CAS  PubMed  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Satoh R et al (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S et al (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joo J, Choi HJ, Lee YH, Kim YK, Song SI (2013) A transcriptional repressor of the ERF family confers drought tolerance to rice and regulates genes preferentially located on chromosome 11. Planta 238:155–170

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zhang L, Yu Y, Quan R, Zhang Z, Zhang H, Huang R (2011) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68:88–99

    Article  CAS  PubMed  Google Scholar 

  • Lin R, Park H, Wang H (2008) Role of Arabidopsis RAP2.4 in regulating light-and ethylene-mediated developmental processes and drought stress tolerance. Mol Plant 1:42–57

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manavella PA, Arce AL, Dezar CA, Bitton F, Renou JP, Crespi M, Chan RL (2006) Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant J 48:125–137

    Article  CAS  PubMed  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96

    Article  CAS  PubMed  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  CAS  PubMed  Google Scholar 

  • Nowak K, Wojcikowska B, Gaj MD (2015) ERF022 impacts the induction of somatic embryogenesis in Arabidopsis through the ethylene-related pathway. Planta 241:967–985

    Article  CAS  PubMed  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onate-Sanchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143:400–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rashid M, Guangyuan H, Guangxiao Y, Hussain J, Xu Y (2012) AP2/ERF transcription factor in rice: genome-wide canvas and syntenic relationships between monocots and eudicots. Evol Bioinform 8:321

    Article  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  • Rong W, Qi L, Wang A et al (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Biol 52:627–658

    Article  CAS  Google Scholar 

  • Sharoni AM, Nuruzzaman M, Satoh K et al (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    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 U S A 94:1035–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todaka D, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2012) Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5:1–9

    Article  Google Scholar 

  • Trujillo LE, Sotolongo M, Menendez C et al (2008) SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant Cell Physiol 49:512–525

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS One 6, e25216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang A, Tan D, Takahashi A, Li TZ, Harada T (2007) MdERFs, two ethylene-response factors involved in apple fruit ripening. J Exp Bot 58:3743–3748

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wan L, Zhang L et al (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78:275–288

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu K, Xu X, Fukao T et al (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhang Z, Chen J et al (2005) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222:494–501

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237:1443–1451

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by the Major Special Foundation of Transgenic Plants in China (2014ZX08009-15B and 2013ZX08001003) and by National Natural Science Foundation of China (31171465).

Author Contribution

RH, JD, and DY conceived and designed the research. YY and DY conducted the experiments. RH, JD, JG, SZ and FW analyzed and discussed the data. YY wrote the manuscript. All authors read and approved the manuscript.

Author information

Author notes

    Authors and Affiliations

    1. College of Life Sciences, Agricultural University of Hebei, Baoding, 071001, China

      Yanwen Yu, Juntao Gu, Fengru Wang & Jingao Dong

    2. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

      Yanwen Yu, Dexin Yang, Shirong Zhou & Rongfeng Huang

    3. National Key Facility of Crop Gene Resources and Genetic Improvement, Beijing, 100081, China

      Rongfeng Huang

    Authors
    1. Yanwen Yu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Dexin Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Shirong Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Juntao Gu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Fengru Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Jingao Dong
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Rongfeng Huang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Jingao Dong or Rongfeng Huang.

    Ethics declarations

    Conflict of Interest

    The authors declare that they have no conflict of interest.

    Additional information

    Handling Editor: Bhumi Nath Tripathi

    Yanwen Yu and Dexin Yang contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Fig. S1

    The knockdown of OsERF109 in RI lines did not interfere the expression of its homologous genes. (a) The comparison of the C terminus with its homologous genes by DNAMAN software, which was used to the interference of OsERF109 transcription. (b) The expression of OsERF109 and homologous genes in RI transgenic lines. Transcripts are indicated relative to the expression level of the wild type Nip and error bars (± SD) are according to three independent biological experiments. (PDF 414 kb)

    Fig. S2

    Transgenic lines overexpression or knockdown of OsERF109 did not affect the growth at mature stage. Transgenic lines of 4-month-old rice grew in paddy field did not show obvious different phenotypes with the corresponding wild types. The OE-95 and RI-20 were selected from the paddy field to take photos with the corresponding wild type Zh17 and Nip, respectively. (PDF 165 kb)

    Table S1

    The primers used in this study. (PDF 173 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Yu, Y., Yang, D., Zhou, S. et al. The ethylene response factor OsERF109 negatively affects ethylene biosynthesis and drought tolerance in rice. Protoplasma 254, 401–408 (2017). https://doi.org/10.1007/s00709-016-0960-4

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00709-016-0960-4

    Keywords

    Search

    Navigation