Skip to main content
Log in

Transcriptome-based identification and expression profiling of AP2/ERF members in Caragana intermedia and functional analysis of CiDREB3

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

The AP2/ERF transcription factor family plays important roles in regulation of plant growth and development as well as the response of plants to stress. However, there are currently few studies focusing on the function of the AP2/ERF-type transcription factors in Caragana intermedia Kuang et H. C. Fu. Here, the expression pattern of AP2/ERF transcription factors family in different tissues and under four stress treatments were evaluated, and the function of CiDREB3 was examined.

Methods and results

In this study, the genes encoding the AP2/ERF family of transcription factors were screened from the C. intermedia drought transcriptome database and subjected to bioinformatic analysis using the online tool and software. The expression pattern of the members of AP2/ERF transcription factors in C. intermedia were detected via quantitative real-time PCR (qRT-PCR). The function of CiDREB3 on growth, development and drought tolerance was evaluated by transgenic Arabidopsis. As a result, 22 sequences with complete ORFs were obtained and all sequences were divided into 13 sub-groups. Most of the AP2/ERF transcription factors exhibited tissue-specific expression and were induced by cold, heat, NaCl and mannitol treatments. Furthermore, heterologous expression of CiDREB3 altered the morphology of the transgenic Arabidopsis thaliana L. Heynh and improved its drought tolerance during seedlings development.

Conclusions

Taken together, the results of the present study helped to better understand the function of the AP2/ERF family transcription factors in response to multiple abiotic stresses and uncovered the role of CiDREB3 in affecting the morphology and abiotic stress tolerance of Arabidopsis.

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

References

  1. Licausi F, Ohme-Takagi M, Perata P (2019) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199(3):639–649. https://doi.org/10.1111/nph.12291

    Article  CAS  Google Scholar 

  2. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17(18):5484–5496. https://doi.org/10.1093/emboj/17.18.5484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94(13):7076–7081. https://doi.org/10.1073/pnas.94.13.7076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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(3):998–1009. https://doi.org/10.1006/bbrc.2001. 6299

    Article  CAS  PubMed  Google Scholar 

  5. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432. https://doi.org/10.1104/pp.105.073783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Xue GP (2002) Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucleic acids res 30(15):e77. https://doi.org/10.1093/nar/gnf076

    Article  PubMed  PubMed Central  Google Scholar 

  7. Li MY, Xu ZS, Huang Y, Tian C, Wang F, Xiong AS (2015) Genome-wide analysis of AP2/ERF transcription factors in carrot (Daucus carota L.) reveals evolution and expression profiles under abiotic stress. Mol Genet Genomics 290(6):2049–2061. https://doi.org/10.1007/s00438-015-1061-3

    Article  CAS  PubMed  Google Scholar 

  8. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6(9):1211–1225. https://doi.org/10.1105/tpc.6.9.1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7(2):173–182. https://doi.org/10.1105/tpc.7.2.173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Scarpeci TE, Frea VS, Zanor MI, Valle EM (2017) Overexpression of AtERF019 delays plant growth and senescence, and improves drought tolerance in Arabidopsis. J Exp Bot 68(3):673–685. https://doi.org/10.1093/jxb/erw429

    Article  CAS  PubMed  Google Scholar 

  11. Wen W, Xie Z, Yu G, Zhao C, Zhang J, Huang L, Xu B, Huang B (2018) Switchgrass PvDREB1C plays opposite roles in plant cold and salt tolerance in transgenic tobacco. Hereditas 155:15. https://doi.org/10.1186/s41065-017-0050-4

    Article  PubMed  Google Scholar 

  12. Yu Y, Duan X, Ding X, Chen C, Zhu D, Yin K, Cao L, Song X, Zhu P, Li Q, NIsa ZU, Yu J, Du J, Song Y, Li H, Liu B, Zhu Y (2017) A novel AP2/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis. Plant Mol Biol 94(4–5):509–530. https://doi.org/10.1007/s11103-017-0623-7

    Article  CAS  PubMed  Google Scholar 

  13. Kulkarni M, Soolanayakanahally R, Ogawa S, Uga Y, Selvaraj MG, Kagale S (2017) Drought Response in Wheat: Key Genes and Regulatory Mechanisms Controlling Root System Architecture and Transpiration Efficiency. Front Chem 5:106. https://doi.org/10.3389/fchem.2017.00106

    Article  PubMed  PubMed Central  Google Scholar 

  14. Wu J, Folta KM, Xie Y, Jiang W, Lu J, Zhang Y (2017) Overexpression of Muscadinia rotundifolia CBF2 gene enhances biotic and abiotic stress tolerance in Arabidopsis. Protoplasma 254(1):239–251. https://doi.org/10.1007/s00709-015-0939-6

    Article  CAS  PubMed  Google Scholar 

  15. Liao X, Guo X, Wang Q, Wang Y, Zhao D, Yao L, Wang S, Liu G, Li T (2017) Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J 89(3):510–526. https://doi.org/10.1111/tpj.13401

    Article  CAS  PubMed  Google Scholar 

  16. Imin N, Nizamidin M, Wu T, Rolfe BG (2007) Factors involved in root formation in Medicago truncatula. J Exp Bot 58(3):439–451. https://doi.org/10.1093/jxb/erl224

    Article  CAS  PubMed  Google Scholar 

  17. Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, Inukai Y (2011) The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J 67(3):472–484. https://doi.org/10.1111/j.1365-313X.2011.04610.x

    Article  CAS  PubMed  Google Scholar 

  18. Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64(6):936–947. https://doi.org/10.1111/j.1365-313X.2010.04384.x

    Article  CAS  PubMed  Google Scholar 

  19. Maes T, Van de Steene N, Zethof J, Karimi M, D’Hauw M, Mares G, Van Montagu M, Gerats T (2001) Petunia Ap2-like genes and their role in flower and seed development. Plant Cell 13(2):229–244. https://doi.org/10.1105/tpc.13.2.229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8(2):155–168. https://doi.org/ 10.1105/ tpc.8.2.155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Feng K, Hou XL, Xing GM, Liu JX, Duan AQ, Xu ZS, Li MY, Zhuang J, Xiong AS (2020) Advances in AP2/ERF super-family transcription factors in plant. Crit Rev Biotechnol 40(6):750–776. https://doi.org/10.1080/07388551.2020.1768509

    Article  CAS  PubMed  Google Scholar 

  22. Liu W, Li Q, Wang Y, Wu T, Yang Y, Zhang X, Han Z, Xu X (2017) Ethylene response factor AtERF72 negatively regulates Arabidopsis thaliana response to iron deficiency. Biochem Biophys Res Commun 491(3):862–868. https://doi.org/10.1016/j.bbrc.2017.04.014

    Article  CAS  PubMed  Google Scholar 

  23. Jin R, Kim BH, Ji CY, Kim HS, Li HM, Ma DF, Kwak SS (2017) Overexpressing IbCBF3 increases low temperature and drought stress tolerance in transgenic sweetpotato. Plant Physiol Biochem 118:45–54. https://doi.org/10.1016/j.plaphy.2017.06.002

    Article  CAS  PubMed  Google Scholar 

  24. Caarls L, Van der Does D, Hickman R, Jansen W, Verk MC, Proietti S, Lorenzo O, Solano R, Pieterse CM, Van Wees SC (2017) Assessing the Role of ETHYLENE RESPONSE FACTOR Transcriptional Repressors in Salicylic Acid-Mediated Suppression of Jasmonic Acid-Responsive Genes. Plant Cell Physiol 58(2):266–278. https://doi.org/10.1093/pcp/pcw187

    Article  CAS  PubMed  Google Scholar 

  25. Han X, Feng Z, Xing D, Yang Q, Wang R, Qi L, Li G (2015) Two NAC transcription factors from Caragana intermedia altered salt tolerance of the transgenic Arabidopsis. BMC Plant Biol 15:208. https://doi.org/10.1186/s12870-015-0591-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24(1):34–36. https://doi.org/10.1016/s0968-0004(98)01336-x

    Article  CAS  PubMed  Google Scholar 

  27. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43(W1):W39–W49. https://doi.org/10.1093/nar/gkv416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwizt D, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203. https://doi.org/10.1093/nar/gkw1129

    Article  CAS  PubMed  Google Scholar 

  29. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19(2):271–273. https://doi.org/10.1038/cr.2009.6

    Article  CAS  PubMed  Google Scholar 

  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Shu Y, Liu Y, Zhang J, Song L, Guo C (2015) Genome-wide analysis of the AP2/ERF superfamily genes and their responses to abiotic stress in Medicago truncatula. Front Plant Sci 6:1247. https://doi.org/10.3389/fpls.2015.01247

    Article  PubMed  Google Scholar 

  32. Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PloS one 9(11):e111988. https://doi.org/10.1371/journal.pone.0111988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52(2):344–360. https://doi.org/10.1093/pcp/pcq196

    Article  CAS  PubMed  Google Scholar 

  34. Chen L, Han J, Deng X, Tan S, Li L, Li L, Zhou J, Peng H, Yang G, He G, Zhang W (2016) Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon. Sci Rep 6:21623. https://doi.org/10.1038/srep21623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cui L, Feng K, Wang M, Wang M, Deng P, Song W, Nie X (2016) Genome-wide identification, phylogeny and expression analysis of AP2/ERF transcription factors family in Brachypodium distachyon. BMC Genomics 17(1):636. https://doi.org/10.1186/s12864-016-2968-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wu H, Lv H, Li L, Liu J, Mu S, Li X, Gao J (2015) Genome-Wide Analysis of the AP2/ERF Transcription Factors Family and the Expression Patterns of DREB Genes in Moso Bamboo (Phyllostachys edulis). PloS one 10(5):e0126657. https://doi.org/10.1371/journal.pone.0126657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Huang Z, Zhong XJ, He J, Jiang MY, Yu XF, Li X (2016) [Identification and characterization of AP2/ERF transcription factors in moso bamboo (Phyllostachys edulis)]. Mol Biol 50(5):785–796. https://doi.org/10.7868/S0026898416050062

    Article  CAS  Google Scholar 

  38. Song X, Li Y, Hou X (2013) Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genomics 14:573. https://doi.org/10.1186/1471-2164-14-573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu Z, Kong L, Zhang M, Lv Y, Liu Y, Zou M, Lu G, Cao J, Yu X (2013) Genome-wide identification, phylogeny, evolution and expression patterns of AP2/ERF genes and cytokinin response factors in Brassica rapa ssp. pekinensis. PloS one 8(12): e83444. https://doi.org/10.1371/journal.pone.0083444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) In silico analysis of transcription factor repertoires and prediction of stress-responsive transcription factors from six major gramineae plants. DNA Res 18(5):321–332. https://doi.org/10.1093/dnares/dsr019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59(15):4095–4107. https://doi.org/10.1093/ jxb/ern248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Agarwal G, Garg V, Kudapa H, Doddamani D, Pazhamala LT, Khan AW, Thudi M, Lee SH, Varshney RK (2016) Genome-wide dissection of AP2/ERF and HSP90 gene families in five legumes and expression profiles in chickpea and pigeonpea. Plant Biotechnol J 14(7):1563–1577. https://doi.org/10.1111/pbi.12520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wei G, Pan Y, Lei J, Zhu YX (2005) Molecular cloning, phylogenetic analysis, expressional profiling and in vitro studies of TINY2 from Arabidopsis thaliana. J Biochem Mol Biol 38(4):440–446. https://doi.org/10.5483/bmbrep.2005.38.4.440

    Article  CAS  PubMed  Google Scholar 

  44. Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF (2008) TINY, a dehydration-responsive element (DRE)-binding protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 283(10):6261–6271. https://doi.org/10.1074/jbc.M706800200

    Article  CAS  PubMed  Google Scholar 

  45. Wilson K, Long D, Swinburne J, Coupland G (1996) A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8(4):659–671. https://doi.org/10.1105/tpc.8.4.659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grant from National Natural Science Foundation of China (Grant Numbers: 31560199).

Author information

Authors and Affiliations

Authors

Contributions

GL and QY conceived and designed the research. KL and TY participated in the experiment and data collection together. QY and KL contributed new reagents or analytical tools. KL, QY and FY analyzed the data. KL wrote first draft of the manuscript. JC and RW guided the writing and modification of the paper. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jingyu Cong or Guojing Li.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

This manuscript does not contain any studies conducted on human or animal subjects.

Consent to participate

All authors listed in the article have approved the manuscript that is enclosed.

Consent to publish

All authors agree and give consent for the publication.

Additional information

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.

Supplementary material 1 (DOCX 3121.5 kb)

Supplementary material 2 (DOCX 34.8 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, K., Yang, Q., Yang, T. et al. Transcriptome-based identification and expression profiling of AP2/ERF members in Caragana intermedia and functional analysis of CiDREB3. Mol Biol Rep 48, 7953–7965 (2021). https://doi.org/10.1007/s11033-021-06826-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06826-8

Keywords

Navigation