Skip to main content
Log in

Genome-wide identification and expression profiles of AP2/ERF transcription factor family in mung bean (Vigna radiata L.)

  • Plant Genetics • Original Paper
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

Mung bean (Vigna radiata L. Wilczek) is an economically important grain legume crop in Asia, with high nutritional quality and potential in other parts of the world particularly arid and semiarid regions. Considering the potential adverse effects of drought, high salt, and other abiotic stresses on crop yield, significant efforts have been made to understand the underlying molecular mechanisms of tolerance to these abiotic stresses in legumes. In this study, a total of 186 putative AP2/ERF genes were identified, which were named VrERF1-186. These VrERF genes were classified into four main subfamilies according to the number of AP2 domains and sequence similarity, including 24 AP2 gene members, 81 ERF gene members, 79 DREB gene members, and 2 RAV members. VrERF genes are scattered across all 11 chromosomes and form small gene clusters on chromosomes due to segmental or tandem duplication. Promoter analysis revealed various cis-acting elements related to light, hormones, and stress responsiveness processes. The expression profiles of the VrERF genes in tissues during development and in response to abiotic stresses were assessed by transcriptome sequencing, and the selected reference genes were validated by qRT-PCR. A total of 174 VrERF genes were expressed in at least one of five tissues, while others showed distinct expression patterns in different tissues or under specific abiotic stress treatments, which indicates that VrERF genes are involved in developmental and environmental stress responses in V. radiata. In conclusion, the genome localization, genome-wide characterization, gene duplication, phylogenetic relationships, and expression pattern of VrERF genes in V. radiata were analyzed, and these results will lay the foundation for further functional analysis of these genes and improve stress tolerance to adverse conditions in plants.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All the data generated in the experiments are presented in manuscript and its supplementary files.

References

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  CAS  Google Scholar 

  • Agarwal G, Garg V, Kudapa H, Doddaman 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 14:1563–1577

    Article  CAS  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:202–208

    Article  Google Scholar 

  • Cao D, Lin Z, Huang L, Damaris RN, Yang P (2021) Genome-wide analysis of AP2/ERF superfamily in lotus (Nelumbo nucifera) and the association between NnADAP and rhizome morphology. BMC Genomics 22:171

  • Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29

    Article  CAS  Google Scholar 

  • Chankaew S, Somta P, Sorajjapinun W, Srinives P (2011) Quantitative trait loci mapping of Cercospora leaf spot resistance in mungbean, Vigna radiata (L.) Wilczek. Mol Breed 28:255–264

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  Google Scholar 

  • Chen H, Je J, Song C, Hwang JE, Lim CO (2012) A proximal promoter region of Arabidopsis DREB2C confers tissue-specific expression under heat stress. J Integr Plant Biol 54:640–651

    Article  CAS  Google Scholar 

  • Chen H, Wang L, Wang S, Liu C, Blair MW, Cheng X (2015) Transcriptome sequencing of mung bean (Vigna radiate L) genes and the identification of EST-SSR markers. PLoS One 10:e0120273

    Article  Google Scholar 

  • Chen H, Liu L, Wang L, Wang S, Cheng X (2016a) VrDREB2A, a DREB-binding transcription factor from Vigna radiata, increased drought and high-salt tolerance in transgenic Arabidopsis thaliana. J Plant Res 129:263–273

    Article  CAS  Google Scholar 

  • Chen HY, Hsieh EJ, Cheng MC, Chen CY, Hwang SY, Lin TP (2016b) ORA47 (octadecanoid-responsive AP2/ERF-domain transcription factor 47) regulates jasmonic acid and abscisic acid biosynthesis and signaling through binding to a novel cis-element. New Phytol 211:599–613

    Article  CAS  Google Scholar 

  • Cheng Z, Zhang X, Zhao K, Yao W, Li R, Zhou B, Jiang T (2019) Over-expression of ERF38 gene enhances salt and osmotic tolerance in transgenic Poplar. Front Plant Sci 10:1375

    Article  Google Scholar 

  • Cui LC, Feng KW, Wang MX, Wang M, Deng PC, Song WN, Nie XJ (2016) Genome-wide identification, phylogeny and expression analysis of AP2/ERF transcription factors family in Brachypodium distachyon. BMC Genomics 17

  • Dossa K, Wei X, Li DH, Fonceka D, Zhang YX, Wang LH, Yu JY, Liao SB, Diouf D, Cisse N, Zhang XR (2016) Insight into the AP2/ERF transcription factor superfamily in sesame and expression profiling of DREB subfamily under drought stress. BMC Plant Biol 16

  • Duran-Medina Y, Serwatowska J, Reyes-Olalde JI, De Folter S, Marsch-Martinez N (2017) The AP2/ERF transcription factor DRNL modulates gynoecium development and affects its response to cytokinin. Front Plant Sci 8:1841

    Article  Google Scholar 

  • Eddy SR (2011) Accelerated profile HMM searches. PLoS Computer Biology 7

  • Eckardt NA (2019) DREB duo defines distinct drought and cold response pathways. Plant Cell 31:1196–1197

    Article  CAS  Google Scholar 

  • Fan W, Hai MR, Guo YL, Ding ZH, Tie WW, Ding XP, Yan Y, Wei Y, Liu Y. Wu C, Shi H, Li K, Hu W (2016) The ERF transcription factor family in cassava: genome-wide characterization and expression analyses against drought stress. Sci Rep 6

  • Fang ZW, Zhang XH, Gao JF, Wang PK, Xu XY, Liu ZX, Shen SH, Feng BL (2015) A buckwheat (Fagopyrum esculentum) DRE-binding transcription factor gene, FeDREB1, enhances freezing and drought tolerance of transgenic Arabidopsis. Plant Mol Biol Rep 33:1510–1525

    Article  CAS  Google Scholar 

  • 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 40:750-776

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:281–288

  • Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo BJ, Wei YF, Xu RB, Lin S, Luan HY, Lv C, Zhang X, Song X, Xu R (2016) Genome-wide analysis of APETALA2/ethylene-responsive factor (AP2/ERF) gene family in barley (Hordeum vulgare L.). PLoS One 11

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  Google Scholar 

  • Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987

    Article  Google Scholar 

  • Hong B, Ma C, Yang Y, Wang T, Yamaguchi-Shinozaki K, Gao J (2009) Over-expression of AtDREB1A in chrysanthemum enhances tolerance to heat stress. Plant Mol Biol 70:231–240

    Article  CAS  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  CAS  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  Google Scholar 

  • Jin X, Yin X, Ndayambaza B, Zhang Z, Min X, Lin X, Wang Y, Liu W (2019) Genome-Wide identification and expression profiling of the ERF gene family in Medicago sativa L. under various abiotic stresses. DNA Cell Biol 38:1056–1068

    Article  CAS  Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci U S A 102:3117–3122

    Article  CAS  Google Scholar 

  • Kang YJ, Kim SK, Kim MY, Lestari P, Kim KH, Ha BK, Jun TH, Hwang WJ, Lee T, Lee J, Shim S, Yoon MY, Jang YE, Han KS, Taeprayoon P, Yoon N, Somta P, Tanya P, Kim KS, Gwag JG, Moon JK, Lee YH, Park BS, Bombarely A, Doyle JJ, Jackson SA, Schafleitner R, Srinives P, Varshney RK, Lee SH (2014) Genome sequence of mungbean and insights into evolution within Vigna species. Nat Commun 5:5443

    Article  CAS  Google Scholar 

  • Kim NY, Jang YJ, Park OK (2018) AP2/ERF Family Transcription Factors ORA59 and RAP2.3 Interact in the Nucleus and Function Together in Ethylene Responses. Front Plant Sci 9:1675

  • Lee JG, Yi G, Seo J, Kang BC, Choi JH, Lee EJ (2020) Jasmonic acid and ERF family genes are involved in chilling sensitivity and seed browning of pepper fruit after harvest. Sci Rep 10:17949

  • V LescotDe´hais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze´ P, Rombauts S, 2002 PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences Nucleic Acids Res 30 325 327

  • Li A, Zhou YA, Jin C, Song WQ, Chen CB, Wang CG (2013) LaAP2L1, a heterosis-associated AP2/EREBP transcription factor of larix, increases organ size and final biomass by affecting cell proliferation in Arabidopsis. Plant Cell Physiol 54:1822–1836

  • Li H, Wang Y, Wu M, Li LH, Li C, Han ZP, Yuan JY, Chen CB, Song WQ, Wang CG (2017) Genome-wide identification of AP2/ERF transcription factors in Cauliflower and expression profiling of the ERF family under salt and drought stresses. Front Plant Sci 8:946

    Article  Google Scholar 

  • Ma R, Xiao Y, Lv Z, Tan H, Chen R, Li Q, Chen J, Wang Y, Yin J, Zhang L, Chen W (2017) AP2/ERF Transcription Factor, Ii049, Positively Regulates Lignan Biosynthesis in Isatis indigotica through Activating Salicylic Acid Signaling and Lignan/Lignin Pathway Genes. Front Plant Sci 8:1361

  • (MAPKKK) gene family in bread wheat (Triticum aestivum L.). BMC Genomics 17: 668

  • Mittal A, Jiang YW, Ritchie GL, Burke JJ, Rock CD (2015) AtRAV1 and AtRAV2 overexpression in cotton increases fiber length differentially under drought stress and delays flowering. Plant Sci 241:78–95

  • 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  Google Scholar 

  • Onate-Sanchez L, Singh KB (2002) Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol 128:1313–1322

    Article  CAS  Google Scholar 

  • Peng XJ, Ma XY, Fan WH, Su M, Cheng LQ, Iftekhar A, Byung HL, Qi DM, Liu SSH, GS, (2011) Improved drought and salt tolerance of Arabidopsis thaliana by transgenic expression of a novel DREB gene from Leymus chinensis. Plant Cell Rep 30:1493–1502

    Article  CAS  Google Scholar 

  • Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69

    Article  CAS  Google Scholar 

  • Rozas J, Ferrer MA, Sánchez-DelBarrio JC, GuiraoRico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    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 Bioph Res Co 290:998–1009

    Article  CAS  Google Scholar 

  • Seo YJ, Park JB, Cho YJ, Jung C, Seo HS, Park SK, Nahm BH, Song JT (2010) Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol Cells 30:271–277

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Wessler SR (2005) Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci 10:54–56

    Article  CAS  Google Scholar 

  • Wang M, Yue H, Feng KW, Deng PC, Song WN, Nie XJ (2016) Genome-wide identification, phylogeny and expressional profiles of mitogen activated protein kinase kinase kinase

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  Google Scholar 

  • Zhang GY, Chen M, Chen XP, Xu ZS, 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 59:4095–4107

    Article  CAS  Google Scholar 

  • Zhang S, Zhu C, Lyu Y, Chen Y, Zhang Z, Lai Z, Lin Y (2020) Genome-wide identification, molecular evolution, and expression analysis provide new insights into the APETALA2/ethylene responsive factor (AP2/ERF) superfamily in Dimocarpus longan Lour. BMC Genomics 21:62

    Article  Google Scholar 

  • Zhao MJ, Yin LJ, Liu Y, Ma J, Zheng JC, Lan JH, Fu JD, Chen M, Xu ZS, Ma YZ (2019) The ABA-induced soybean ERF transcription factor gene GmERF75 plays a role in enhancing osmotic stress tolerance in Arabidopsis and soybean. BMC Plant Biol 19:506

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the National Key R&D Program of China (2018YFD1000700/2018YFD1000703), Agricultural Science and Technology Innovation Program (ASTIP) of CAAS, Central Public-interest Scientific Institution Basal Research Fund (No. S2021XC05) and China Agriculture Research System of MOF and MARA-Food Legumes (CARS-08).

Author information

Authors and Affiliations

Authors

Contributions

HLC and XZC conceived and designed all the experiments; HLC and LLH carried out the experiments and drafted the manuscript. HLC processed and analyzed the data. SHW and LXW cultured the plants and collected the samples for study. All authors read the manuscript and approved for publication and revised the manuscript.

Corresponding authors

Correspondence to Honglin Chen or Xuzhen Cheng.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by: Izabela Pawłowicz

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 file1 (RAR 330 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, H., Hu, L., Wang, L. et al. Genome-wide identification and expression profiles of AP2/ERF transcription factor family in mung bean (Vigna radiata L.). J Appl Genetics 63, 223–236 (2022). https://doi.org/10.1007/s13353-021-00675-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-021-00675-8

Keywords

Navigation