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Isolation and characterization of ZmERF1 encoding ethylene responsive factor-like protein 1 in popcorn (Zea mays L.)

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Abstract

The ethylene response factor (ERF) plays a key role in the transcriptional regulation of plant growth, development, and response to various environmental perturbations. Study of ERF transcription factors, especially those in cultivated crops, could facilitate their molecular genetic modification. In this study, an ERF1 gene, designated as ZmERF1, which was found to be localized in the nucleus, was isolated from popcorn (Zea mays L.). Further analysis showed that the ZmERF1 proteins could bind to the GCC box motif and act as a transcriptional activator. A clear picture of ZmERF1 expression pattern showed that ZmERF1 expression varies during different development stages of endosperm. Furthermore, its expression could be highly induced by salinity, osmotic and heat stress, suggesting that the gene is involved in stress signaling pathways in maize. Therefore, ZmERF1 could play important role in abiotic stress tolerance and endosperm development in maize.

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Abbreviations

TFs:

Transcription factors

ERF:

Ethylene response factor

qPCR:

Quantitative real-time PCR

IPTG:

Isopropyl beta-D-thiogalactopyranoside

DAP:

Days after pollination

ORF:

Open reading frame

MS:

Murashige and Skoog

NJ:

Neighbor-joining

AbA:

Aureobasidin A

References

  • Abdel Hamid AK, Mamdouh SS, Mamdouh MN et al (2011) A DREB gene from the xero-halophyte Atriplex halimus is induced by osmotic but not ionic stress and shows distinct differences from glycophytic homologues. Plant Cell Tissue Organ Cult 106:191–206

    Article  Google Scholar 

  • Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37:1125–1135

    Article  CAS  PubMed  Google Scholar 

  • Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a β-sheets revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO 17:5484–5496

    Article  CAS  Google Scholar 

  • Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bfenner ML, Cheikh N (1995) The role of hormones in photosynthate partitioning and seed filling. In: Davies PJ (ed) The plant hormones. Kluwer Academic Publishers, Netherlands, pp 649–670

    Chapter  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ- rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chakravarthy S, Tuori RP, D’Ascenzo MD (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chuck G, Muszynski M, Kellogg E, Hake S, Schmidt RJ (2002) The control of spikelet meristem identity by the branched silkless1 gene in maize. Science 298:1238–1241

    Article  CAS  PubMed  Google Scholar 

  • Dong YB, Zhang ZW, Shi QL, Wang QL, Zhou Q, Li YL (2012) Quantitative trait loci mapping and meta-analysis across three generations for popping characteristics in popcorn. J Cereal Sci 56:581–586

    Article  CAS  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) DREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-, salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • El-Sharkawy I, Sherif S, Mila I (2009) Molecular characterization of seven genes encoding ethylene-responsive transcriptional factors during plum fruit development and ripening. J Exp Bot 60:907–922

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gu LJ, Cheng HM (2014) Isolation, molecular cloning and characterization of a coldresponsive gene, AmDUF1517, from Ammopiptanthus mongolicus. Plant Cell Tissue Organ Cult 117:201–211

    Article  CAS  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  CAS  PubMed  Google Scholar 

  • Jin TC, Chang Q, Li WF, Yin DX, Li ZJ, Wang DL, Liu B, Liu LX (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell Tissue Organ Cult 100:219–227

    Article  CAS  Google Scholar 

  • Kirch T, Simon R, Grünewald M, Werr W (2003) The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 15:694–705

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kudo K, Oi T, Uno Y (2014) Functional characterization and expression profiling of a DREB2-type gene from lettuce (Lactuca sativa L. Plant Cell Tissue Organ Cult 116:97–109

    Article  CAS  Google Scholar 

  • Liu YY (2008) Identification and cloning of differentially expressed genes in endosperm at two key development stages of different maize inbreds. Henan Agricultural University, Doctoral Dissertation

  • Marsch-Martinez N, Greco R, Becker JD, Dixit S, Bergervoet JH, Karaba A, de Folter S, Pereira A (2006) BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62:825–843

    Article  CAS  PubMed  Google Scholar 

  • Menke FLH, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate-and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455–4463

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakano T, Fujisawa M, Shima Y, Ito Y (2014) The AP2/ERF transcription factor SlERF52 functions in flower pedicel abscission in tomato. J Exp Bot. doi:10.1093/jxb/eru154

    PubMed Central  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohta M, Matsui K, Hiratsu K (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Okamuro JK, Caster B, Villarroel R (1997) The AP2 domain of APETACA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci 94:7076–7081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad Q, Regad F, Latché A, Pech JC, Bouzayen M (2006) Sl-ERF, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol 47:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Quan RD, Hu SJ, Zhang ZL, Zhang HW, Zhang ZJ, Huang RF (2010) Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnol J 8:476–488

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H (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 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signalling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE FACTOR1. Genes Dev 12:3703–3714

    Article  CAS  PubMed Central  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. PNAS 94:1035–1040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang M, Sun J, Liu Y, Chen F, Shen S (2006) Isolation and functional characterization of the JcERF gene, a putative AP2/EREBP domain-containing transcription factor, in the woody oil plant Jatropha curcas. Plant Mol Biol 63:419–428

    Article  PubMed  Google Scholar 

  • van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

  • Van der Graaff E, Dulk-Ras AD, Hooykaas PJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980

    PubMed  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 YJ, Zhang C, Jia PY, Wang XQ, Wang WR, Dong L (2013) Isolation and expression analysis of three EIN3-like genes in tree peony (Paeonia suffruticosa). Plant Cell Tissue Organ Cult 112:181–190

    Article  CAS  Google Scholar 

  • 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 8:659–671

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  PubMed  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. Integr Plant Biol 53:570–585

    Article  CAS  Google Scholar 

  • Xu KD, Huang XH, Wu MM, Wang Y, Chang YX, Liu K, Zhang J, Zhang Y, Zhang FL, Yi LM, Li TT, Wang RY, Tan GX, Li CW (2014) A rapid, highly efficient and economical method of Agrobacterium-mediated in planta transient transformation in living onion epidermis. PLoS One 9:e83556

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yan HW, Hong L, Zhou YQ, Jiang HY, Zhu SW, Fan J, Cheng BJ (2013) A genome-wide analysis of the ERF gene family in sorghum. Genet Mol Res 12:2038–2055

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Huang R (2010) Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol 73:241–249

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Broeckling CD, Blancaflor EB (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Li W, Chen J, Yang Y, Zhang Z, Zhang H, Wang XC, Huang R (2007) Transcriptional activator TSRF1 reversely regulates pathogen resistance and osmotic stress tolerance in tobacco. Plant Mol Biol 63:63–71

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Yang Y, Zhang Z, Chen J, Wang XC, Huang R (2008) Expression of the ethylene response factor gene TSRF1 enhances abscisic acid responses during seedling development in tobacco. Planta 228:777–787

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZJ, Wang J, Zhang RX, Huang RF (2012) The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J 71:273–287

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Guo JS, Feng ZH, Cui XH, Zhu J (2012) Molecular characterization of a novel AP2 transcription factor ThWIND1-L from Thellungiella halophila. Plant Cell Tissue Organ Cult 10:423–433

    Article  Google Scholar 

  • Zhu Q, Zhang J, Gao X (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12

    Article  CAS  PubMed  Google Scholar 

  • Zhuang J, Deng DX, Yao QH, Zhang J, Xiong F, Chen JM, Xiong AS (2010) Discovery, phylogeny and expression patterns of AP2-like genes in maize. Plant Growth Regul 62:51–58

    Article  CAS  Google Scholar 

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Acknowledgments

This work is funded by the National Hi-Tech Research and Development Program of China (2012AA10A307).

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Authors and Affiliations

  1. College of Agronomy, Henan Agricultural University, Collaborative Innovation Center of Henan Grain Crops, National Key Laboratory of Wheat and Maize Crop Science, 95 Wenhua Rd, Zhengzhou, 450002, China

    Qingling Shi, Yongbin Dong, Dahe Qiao, Qilei Wang, Zhiyan Ma, Feifei Zhang, Qiang Zhou, He Xu, Fei Deng & Yuling Li

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  1. Qingling Shi
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  2. Yongbin Dong
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  3. Dahe Qiao
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  4. Qilei Wang
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  6. Feifei Zhang
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  7. Qiang Zhou
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  8. He Xu
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  10. Yuling Li
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Correspondence to Yuling Li.

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Qingling Shi and Yongbin Dong have contributed equally to this work.

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Shi, Q., Dong, Y., Qiao, D. et al. Isolation and characterization of ZmERF1 encoding ethylene responsive factor-like protein 1 in popcorn (Zea mays L.). Plant Cell Tiss Organ Cult 120, 747–756 (2015). https://doi.org/10.1007/s11240-014-0644-8

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  • DOI: https://doi.org/10.1007/s11240-014-0644-8

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