Abstract
We cloned the GbABR1 gene from highly resistant Gossypium barbadense Xinhai15 based on the candidate genes screened by transcriptome sequencing that were related to resistance to Verticillium wilt. A sequence characteristic analysis showed that GbABR1 was an ERF subfamily B4 member and was a new member of the AP2 family of sea-island cotton. The GbABR1 gene was expressed highly in roots compared with the levels in leaves and stems in cotton. Expression was enhanced significantly in cotton after infection by Verticillium dahliae, indicating that GbABR1 probably plays an important role in the response to biotic stress. The results of subcellular localisation showed that GFP:GbABR1 was localised to the nucleus. GbABR1 silencing via the virus-induced gene silencing (VIGS) method indicated that the incidence of disease and the disease index in VIGS-silenced plants were much higher than in the control after infection by Verticillium dahliae. The GbABR1-overexpressing Arabidopsis plants showed similar resistance to Verticillium dahliae compared to the wild type. These results indicate that the GbABR1 gene plays a positive role in resistance to Verticillium wilt. The GbABR1-overexpressing Arabidopsis plants presented dwarfism, early maturation and early bolting compared with wild-type plants, suggesting that GbABR1 also participates in growth and development.
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Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, vol 63, 2nd edn. Academic Press, New York, pp 3899–3911
Berrocal-Lobo, M., Molina, A., and Solano, R. (2002). Constitutive expression of ETHYLENE RESPON SEFACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32. Doi: https://doi.org/10.1046/j.1365-313x.2002.01191.x
Broekaert WF, Delaure SL, De Bolle MF, Cammue BP (2006) The role of ethylene in host–pathogen interactions. Annu Rev Phytopathol 44:393–416. https://doi.org/10.1146/annurev.phyto.44.070505.143440
Chia, KF (2013) The Arabidopsis transcription factor ERF13 negatively regulates defense against Pseudomonas syringae. Dissertations & Theses, University of California, San Diego.
Deneris ES, Boulter J, Swanson LW (1989) Beta 3: a new member of nicotinic acetylcholine receptor gene family is expressed in brain. J Biol Chem 264:6268–6272
Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signaling. Protoplasma 245:3–14. https://doi.org/10.1007/s00709-010-0142-8
Feng JX, Liu D, Pan Y, Gong W, Ma LG, Luo JC, Deng XW, Zhu YX (2005) An annotation update via cDNA sequence analysis and comprehensive profiling of developmental, hormonal or environmental responsiveness of the Arabidopsis AP2/EREBP transcription factor gene family. Plant Mol Biol 59:853–868. https://doi.org/10.1007/s11103-005-1511-0
Gao S, Zhang H, Tian Y et al (2008) Expression of TERFl in rice regulates expression of stress-responsive genes and enhances tolerance to drought and high-salinity. Plant Ceil Reports 27:1787–1795. https://doi.org/10.1007/s00299-008-0602-1
Gao XQ, Robert C Jr, Britt LBS, He P (2011) Agrobacterium-mediated virus-induced gene silencing assay in cotton. J Vis Exp 54:e2938. https://doi.org/10.3791/2938.
Gayoso C, Pomar F, Novo-Uzal E, Merino F, deIlarduya OM (2010) The Ve-mediated resistance response of the tomato to V. dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol 10:232. https://doi.org/10.1186/1471-2229-10-232
Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin GB (2012) Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14:817–831. https://doi.org/10.1105/tpc.000794.
Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49. https://doi.org/10.1016/j.pbi.2003.11.011
Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22:1716–1732. https://doi.org/10.1105/tpc.109.073783
Lee DK, Yoon S, Kim YS, Kim JK (2016) Rice OsERF71-mediated root modification affects shoot drought tolerance. Plant Signal Behav 12(1):e1268311. https://doi.org/10.1080/15592324.2016.1268311
Liu WY, Chiou SJ, Ko CY et al (2010) Functional characterization of three ethylene response factor genes from Bupleurum kaoi indicates that BkERFs mediate resistance to Botrytis cinerea. J Plant Physiol 168(4):375–381. https://doi.org/10.1016/j.jplph.2010.07.006
Liu D, Chen X, Liu J et al (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63(10):3899–3911. https://doi.org/10.1093/jxb/ers079
Meng Xianpeng (2009). Isolation and characterization of transcription factor ERF related to disease-resistance in Gossypium barbadense L. Chinese Academy of Agricultural Sciences, Dissertations & Theses.
Meng X, Fuguang L, Chuanliang L, Chaojun Z, Zhixia W, Yajuan C (2010) Isolation and Characterization of an ERF Transcription Factor Gene from Cotton (Gossypium barbadenseL.). Plant Mol Biol Report 28:176–183. https://doi.org/10.1111/j.1744-7909.2010.00914.x.
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182. https://doi.org/10.1105/tpc.7.2.173
Okamuro JK, Caster B, Villarroel R (1997) The AP2 domain of APETALA2 define a large new family of DNA binding protein in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081. https://doi.org/10.1073/pnas.94.13.7076
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. Biochem Biophys Res Commun 12:998–1009. https://doi.org/10.1006/bbrc.2001.6299.
Scarpeci TE, Frea VS, Zanor MI, Valle EM (2016) Overexpression of AtERF019delays plant growth and senescence and improves drought tolerance in Arabidopsis. J Exp Bot. https://doi.org/10.1093/jxb/erw429
Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17(8):2384–2396. https://doi.org/10.1105/tpc.105.033043.
Sun Quan HJ, Zhu X, Wang W, He X, Shi Y, Yuan Y, Du X, Cai Y (2013) Analysis of sea-island cotton and upland cotton in response to V. dahliae infection by RNA sequencing. BMC Genomics 14:852. https://doi.org/10.1186/1471-2164-14-852
Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. Plant J 35:574–587. https://doi.org/10.1046/j.1365-313X.2003.01830.x
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183. https://doi.org/10.1105/tpc.000596
Xu Z S, Xia L Q, Chen M, et al. (2007). Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. https://doi.org/10.1007/s11103-007-9237-9.
Xu ZS, Chen M, Ma YZ, Li LC (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Inte. Plant Biol 53:570–585. https://doi.org/10.1111/j.1744-7909.2011.01062.x.
Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276. https://doi.org/10.1016/j.tplants.2012.09.001
Zarei A, Korbes AP, Younessi P (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol Biol 75:321–331. https://doi.org/10.1007/s11103-010-9728-y.
Zhang Z, Li F, Li D et al (2010) Expression of ethylene response factor JERF1 in rice improves tolerance to drought [J]. Planta 232:765–774. https://doi.org/10.1007/s00425-010-1208-8
Zhang WW, Jiang TF, Cui X, Qi FJ, Jian GL (2012) Colonization in cotton plants by a green fluorescent protein labelled strain of V. dahliae. Eur J Plant Pathol 34:1–10. https://doi.org/10.1007/s10658-012-0131-1.
Zhang H, Huang L, Dai Y, Liu S, Hong Y, Tian L, Huang L, Cao Z, Li D, Song F (2015) Arabidopsis AtERF15 positively regulates immunity against Pseudomonas syringae pv. Tomato DC3000 and Botrytis cinerea. Front. Plant Sci 6:686. https://doi.org/10.3389/fpls.2015.00686.
Zhang Q., Gao M., Wu L., Wang Y., Chen Y. (2016a). Divergent expression patterns in two Vernicia species revealed the potential role of the hub gene VmAP2/ERF036 in resistance to fusarium oxysporum in Vernicia montana. Genes, Dec 1;7(12). https://doi.org/10.3390/genes7120109
Zhang WW, Zhang HC, Qi FJ, Jian GL (2016b) Generation of transcriptome profiling and gene functional analysis in Gossypium hirsutum upon V. dahliae infection. Biochem Biophys Res Commun 473:879–885. https://doi.org/10.1016/j.bbrc.2016.03.143
Zuo KJ, Qin J, Zhao JY, Ling H, Zhang LD, Cao YF, Tang KX (2007) Over-expression GbERF2 tanscription factor in tobacco enhances brown spots disease resistance by activating expression of downstream genes. Gene 391:80–90. https://doi.org/10.1016/j.gene.2006.12.019
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This work was supported by the National Key Research and Development Program of China (NO:2016YFD0101900), the Natural Science Foundation of China (NSFC grant No. 31571724, U1704104), Innovation and Talent Introduction Program on Crop Stress Biology (111 Project), Henan outstanding talent project (154200510006).
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Liu, Y., Liu, X., Long, L. et al. GbABR1 is associated with Verticillium wilt resistance in cotton. Biologia 73, 449–457 (2018). https://doi.org/10.2478/s11756-018-0058-x
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DOI: https://doi.org/10.2478/s11756-018-0058-x