Skip to main content
SpringerLink
Log in

A novel CBF that regulates abiotic stress response and the ripening process in oil palm (Elaeis guineensis) fruits

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

A new member of the C-repeat binding factor (CBF) encoding an AP2-domain protein was isolated from ripening oil palm (Elaeis guineensis var. Dura × Pisifera) fruit. Bioinformatics analysis revealed that EgCBF3 has an AP2 DNA binding domain containing 57 amino acids. According to the signature sequences found upstream and downstream of the AP2 domain, it was predicted that the deduced amino acid sequence belongs to the A-1 group of the CBF/DREB1 subfamily. EgCBF3 is differentially expressed in the fruit mesocarp tissue with the highest transcript accumulation in ripening fruit at 17 weeks after anthesis (w.a.a.). In the vegetative tissues, it showed higher expression levels in the roots compared to the leaves. In the mesocarp tissue, expression of EgCBF3 was upregulated after 2 h and peaked after 24 h of cold, ethylene and ABA treatments, while for drought and salt stresses, it exhibited the highest expression after 4 and 8 h, respectively. GFP fusion protein of EgCBF3 was localized to the nucleus of the onion’s epidermal cells. The in vitro and in vivo DNA-protein transactivation assay using electrophoretic mobility shift assay (EMSA) and yeast one-hybrid analysis revealed that EgCBF3 was able to bind to the DRE/CRT cis-element. Tomato was chosen as a model system for the climacteric oil palm fruits. Expression profile of the ethylene and abscisic acid biosynthesis-related genes and ripening-related genes were affected by transient overexpression of EgCBF3 in the tomato fruits at different developmental stages. These results suggest that EgCBF3 can mediate abiotic stress response in ripening fruits and may function as a regulator of ripening process-related genes.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

w.a.a.:

Weeks after anthesis

ACS:

1-aminocyclopropane-1-carboxylic acid synthase

ACO:

1-aminocyclopropane-1-carboxylic acid oxidase

NCED1:

9-cis-epoxycarotenoid dioxygenase 1

PG:

Polygalacturonase

PDS:

Phytoene desaturase

PSY:

Phytoene synthetase

LeEF1α:

Elongation factor 1α

Act:

Actin

NLS:

Nuclear localization signal

EMSA:

Electrophoretic mobility shift assay

References

  • Akhtar M, Jaiswal A, Taj G, Jaiswal JP, Qureshi MI, Singh NK (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91(3):385–395

    Article  CAS  PubMed  Google Scholar 

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Regul 26(2):143–159

    Article  CAS  Google Scholar 

  • Baud S, Mendoza MS, To A, Harscoët E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON 2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838

    Article  CAS  PubMed  Google Scholar 

  • Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB, Arondel V (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci U S A 108(30):12527–12532

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cara B, Giovannoni JJ (2008) Molecular biology of ethylene during tomato fruit development and maturation. Plant Sci 175:106–113

    Article  CAS  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissues. Phytochemical Bull 19:11–15

    Google Scholar 

  • Dutta A, Sen J, Deswal R (2007) Down regulation of terpenoid indole alkaloid biosynthetic pathway by low temperature and cloning of an AP2 type C-repeat binding factor (CBF) from Catharanthus roseus (L). G. Don. Plant Cell Rep 26:1869–1878

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Chu C (2008) Abscisic acid and the pre-harvest sprouting in cereals. Plant Signal Behav 3:1046–1048

    Article  PubMed Central  PubMed  Google Scholar 

  • Gapper NE, McQuinn RP, Giovannoni JJ (2013) Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82:575–591

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–749

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni J (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68(6):533–555

    Article  CAS  PubMed  Google Scholar 

  • He LG, Wang HL, Liu DC, Zhao YJ, Xu M, Zhu M, Wei GQ, Sun ZH (2012) Isolation and expression of a cold-responsive gene PtCBF in Poncirus trifoliata and isolation of citrus CBF promoters. BIOLOGIA PLANTARUM 56(3):484–492

    Article  CAS  Google Scholar 

  • Ithnin M, Singh R, Kushairi Din A (2011) Elaeis. In: Kole C (ed) Wild crop relatives: genomic and breeding resources. Plantation and Ornamental Crops, Springer-Verlag Berlin Heidelberg. doi:10.1007/978-3-642-21201-7_6

    Google Scholar 

  • Jiang F, Wang F, Wu Z, Li Y, Shi G, Hu J, Hou X (2011) Components of the Arabidopsis CBF cold-response pathway are conserved in non-heading Chinese cabbage. Plant Mol Biol Rep 29:525–532

    Article  CAS  Google Scholar 

  • Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371

    Article  CAS  PubMed  Google Scholar 

  • Li CW, Su RC, Cheng CP, Sanjaya YSJ, Hsieh TH, Chao TC, Chan MT (2011) Tomato RAV transcription factor is a pivotal modulator involved in the AP2/EREBP-mediated defence pathway. Plant Physiol 156(1):213–227

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336

    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 Central  PubMed  Google Scholar 

  • Liu Y, Zhao TJ, Liu JM, Liu WQ, Liu Q, Yan YB, Zhou HM (2006) The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett 580:1303–1308

    Article  CAS  PubMed  Google Scholar 

  • Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11

    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(2):86–96

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:472–493

    Article  Google Scholar 

  • Murphy DJ (2009) Oil palm: future prospects for yield and quality improvements. Lipid Technol 21:257–260

    Article  Google Scholar 

  • Nakano W, Suzuki T, Fujimura KT, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71

    Article  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci U S A 96:13839–13844

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Omidvar V, Abdullah SNA, Ebrahimi M, Ho CL, Mahmood M (2013) Gene expression of the oil palm transcription factor EgAP2-1 during fruit ripening and in response to ethylene and ABA treatments. BIOLOGIA PLANTARUM 57(4):646–654

    Article  CAS  Google Scholar 

  • Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, Causse M, Renard CMCG, Faurobert M (2010) Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232:483–500

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan G, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36

    Article  PubMed Central  PubMed  Google Scholar 

  • Ping L, Lian ZG, Xin LX, He WL, Ming ZZ (2009) Cloning of 9-cis-epoxycarotenoid dioxygenase (NCED) gene encoding a key enzyme during abscisic acid (ABA) biosynthesis and ABA-regulated ethylene production in detached young persimmon calyx. Chinese Sci Bull 54:2830–2838

    Article  Google Scholar 

  • Prescott A, Martin C (1987) A rapid method for the quantitative assessment of levels of specific mRNAs in plants. Plant Mol Biol Rep 4:219–224

    Article  CAS  Google Scholar 

  • Riov J, Dagan E, Goren R, Yang SF (1990) Characterization of abscisic acid-induced ethylene production in citrus leaf and tomato fruit tissues. Plant Physiol 92:48–53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rock CD (2010) Stress Signaling I: The Role of Abscisic Acid (ABA). In A. Pareek, S.K. Sopory, H.J. Bohnert and Govindjee (eds.), Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation. Springer Science + Business Media B.V. pp.33–73

  • Rodrigo MJ, Marcos JF, Alferez F, Mallent M, Zacarias L (2003) Characterization of Pinalate, a novel Citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content. J Exp Bot 54:727–738

    Article  CAS  PubMed  Google Scholar 

  • Rugkong A, McQuinn R, Giovannoni JJ, Rose JKC, Watkins CB (2011) Expression of ripening-related genes in cold-stored tomato fruit. Postharvest Biol Technol 61:1–14

    Article  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Seymour GB, Poole M, Giovannoni JJ, Tucker GA (2013) The molecular biology and biochemistry of fruit ripening. Wiley, New York

    Book  Google Scholar 

  • Sharma MK, Kumar R, Solanke AU, Tyagi AK, Sharma R, Sharma AK (2010) Identification phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284:455–475

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozakiy 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 

  • Singh R, Ong-Abdullah M, Leslie Low ET, Abdul Manaf MA, Rosli Rajanaidu Nookiah R, Ooi LCL, Ooi SE et al (2013) Oil palm genome sequence reveals divergence of interfertile species in old and new worlds. Nature 500:335–341

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ethylene-insensitive3 and ethylene-response-factor1. Genes Dev 2:3703–3714

    Article  Google Scholar 

  • Solomons NW, Orozco M (2003) Alleviation of vitamin a deficiency with palm fruit and its products. Asia Pac J Clin Nutr 12:373–384

    CAS  PubMed  Google Scholar 

  • Srivastava A, Handa AK (2005) Hormonal regulation of tomato fruit development: a molecular perspective. J Plant Growth Regul 24:67–82

    Article  CAS  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 Central  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Tranbarger TJ, Dussert S, Joe T, Argout X, Summo M, Champion A, Cros D, Omore A, Nouy B, Morcillo F (2011) Regulatory mechanisms underlying oil palm fruit mesocarp maturation, ripening, and functional specialization in lipid and carotenoid metabolism. Plant Physiol 156:564–584

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vega-Garcia MO, Lopez-Espinoza G, Ontiveros JC, Caro-Corrales JJ, Vargas FD, Lopez-Valenzuela JA (2010) Changes in protein expression associated with chilling injury in tomato fruit. J Am Soc Hortic Sci 135:83–89

    Google Scholar 

  • Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  Google Scholar 

  • Wang HL, Tao JJ, He LG, Zhao YJ, Xu M, Liu DC, Sun ZH (2009) cDNA cloning and expression analysis of a Poncirus trifoliata CBF gene. Physiol Plant 53:625–630

    CAS  Google Scholar 

  • Wang QJ, Xu KY, Tong ZG, Wang SH, Gao ZH, Zhang JY, Zong CW, Qiao YS, Zhang Z (2010) Characterization of a new dehydration responsive element binding factor in central arctic cowberry. Plant Cell Tiss Organ Cult 101:211–219

    Article  CAS  Google Scholar 

  • Weigel D (1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7:388–389

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Yuan Y, Zhang L, Wan L, Zheng Y, Zhou P, Li D (2011) Identification and characterization of differential gene expression in the mesocarp and kernel of oil palm nuts using suppression subtractive hybridization. Tree Genet Genom. doi:10.1007/s11295-011-0390-6

    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(2):251–264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang Y, Li R, Qi M (2000) In vivo analysis of promoters and transcription factors by agro-infiltration of tobacco leaves. Plant J 22(6):543–551. doi:10.1046/j.1365-313x.2000.00760.x

  • Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220:262–270

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zhang H, Quan R, Wang XC, Huang R (2009a) Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol 150:365–377

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang M, Yuan B, Ping L (2009b) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60(6):1579–1588

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Li N, Gao F, Yang A, Zhang J (2010) Overexpression of TsCBF1 gene confers improved drought tolerance in transgenic maize. Mol Breed 26:455–465

    Article  CAS  Google Scholar 

  • Zhao DY, Shen L, Fan B, Yu M, Zheng Y, Lv S, Sheng J (2009) Ethylene and cold participate in the regulation of LeCBF1 gene expression in postharvest tomato fruits. FEBS Let 583:3329–3334

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The project was supported by the Research University Grant awarded to Universiti Putra Malaysia.

Authors’ contribution

Mortaza Ebrahimi carried out the research as part of his PhD project. Siti Nor Akmar Abdullah is the project leader and main supervisor. Maheran Abdul Aziz and Parameswari Namasivayam are both co-supervisors.

Data archiving statement

Elaeis guineensis ethylene-responsive factor (CBF3) gene, complete cds

ACCESSION KC312892

VERSION KC312892.1 GI.460332880

Author information

Authors and Affiliations

  1. Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Mortaza Ebrahimi, Siti Nor Akmar Abdullah & Maheran Abdul Aziz

  2. Department of Tissue Culture and Gene Transformation, ABRII, Karaj, Alborz, Iran

    Mortaza Ebrahimi

  3. Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Siti Nor Akmar Abdullah

  4. Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Parameswari Namasivayam

Authors
  1. Mortaza Ebrahimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siti Nor Akmar Abdullah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maheran Abdul Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Parameswari Namasivayam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siti Nor Akmar Abdullah.

Additional information

Communicated by W. Ratnam

This article is part of the Topical Collection on Gene Expression

Key message

EgCBF3 belongs to the A-1 group of DREB1 from the AP2/ERF superfamily of plant-specific transcription factors. EgCBF3 can mediate abiotic stress response and regulate fruit ripening through modulation of ethylene and abscisic acid biosynthesis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ebrahimi, M., Abdullah, S.N.A., Aziz, M.A. et al. A novel CBF that regulates abiotic stress response and the ripening process in oil palm (Elaeis guineensis) fruits. Tree Genetics & Genomes 11, 56 (2015). https://doi.org/10.1007/s11295-015-0874-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0874-x

Keywords

Search

Navigation