Abstract
Main conclusion
This study analyzed the AP2/ERF transcription factors in celery and showed that two dehydration-responsive-element-binding (DREB) transcription factors, AgDREB1 and AgDREB2, contribute to the enhanced resistance to abiotic stress in transgenic Arabidopsis.
Abstract
The AP2/ERF family is a large family of transcription factors (TFs) in higher plants that plays a central role in plant growth, development, and response to environmental stress. Here, 209 AP2/ERF family members were identified in celery based on genomic and transcriptomic data. The TFs were classified into four subfamilies (i.e., DREB, ERF, RAV, and AP2) and Soloist. Evolution analysis indicated that the AP2/ERF TFs are ancient molecules and have expanded in the long-term evolution process of plants and whole-genome duplication events. AgAP2/ERF proteins may be associated with multiple biological processes as predicted by the interaction network. The expression profiles and sequence alignment analysis of the TFs in the DREB-A1 group showed that eight genes could be divided into four branches. Two genes, AgDREB1 and AgDREB2, from the DREB-A1 group were selected for further analysis. Subcellular localization assay suggested that the two proteins are nuclear proteins. Yeast one hybrid assay demonstrated that the two proteins could bind to the dehydration-responsive element (DRE). The overexpression of AgDREB1 and AgDREB2 in Arabidopsis induced the increased tolerance to cold treatment and the up-regulation of the COR genes expression. AgDREB1 and AgDREB2 might function as transcriptional activators in regulating the downstream genes by binding to corresponding DRE to enhance stress tolerance in celery.
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Abbreviations
- CBF:
-
C-repeat-binding factors
- CRT:
-
C-repeat
- DEGs:
-
Differentially expressed genes
- DRE:
-
Dehydration-responsive element
- DREB:
-
Dehydration-responsive element binding
- GUS:
-
β-Glucuronidase
- LTRE:
-
Low-temperature responsive element
- POD:
-
Peroxidase
- RPKM:
-
Reads per kilobase per million mapped reads
- RT-qPCR:
-
Real-time quantitative PCR
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- TFs:
-
Transcription factors
- Trp:
-
Tryptophan
- WT:
-
Wild type
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. https://doi.org/10.1007/s12041-012-0201-3
Beynon ER, Symons ZC, Jackson RG, Lorenz A, Rylott EL, Bruce NC (2009) The role of oxophytodienoate reductases in the detoxification of the explosive 2,4,6-trinitrotoluene by Arabidopsis. Plant Physiol 151(1):253–261. https://doi.org/10.1104/pp.109.141598
Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422(6930):433–438. https://doi.org/10.1038/nature01521
Chen M, Li LC, Ma YZ, Xu ZS (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53(7):570–585. https://doi.org/10.1111/j.1744-7909.2011.01062.x
Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Liu X, Li H, Zheng W, Sun J (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24(7):2898–2916. https://doi.org/10.1105/tpc.112.098277
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Agarwal M, Zhu JK (2003) ICE1, a regulator of cold induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17(8):1043–1054. https://doi.org/10.1101/gad.1077503
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55(395):225–236. https://doi.org/10.1093/jxb/erh005
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33(4):751–763. https://doi.org/10.1046/j.1365-313X.2003.01661.x
Feng K, Hou XL, Li MY, Jiang Q, Xu ZS, Liu JX, Xiong AS (2018) CeleryDB: a genomic database for celery. Database. https://doi.org/10.1093/database/bay070
Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49(5):459–471. https://doi.org/10.1023/a:1015570308704
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54(5):767–781. https://doi.org/10.1023/B:PLAN.0000040902.06881.d4
Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296(5565):92–100. https://doi.org/10.1126/science.1068275
Hobert O (2008) Gene regulation by transcription factors and microRNAs. Science 319(5871):1785–1786. https://doi.org/10.1126/science.1151651
Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya Tsai YC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231(6):1459–1473. https://doi.org/10.1007/s00425-010-1147-4
Ito TM, Polido PB, Rampim MC, Kaschuk G, Souza SG (2014) Genome-wide identification and phylogenetic analysis of the AP2/ERF gene superfamily in sweet orange (Citrus sinensis). Genet Mol Res 13(3):7839–7851. https://doi.org/10.4238/2014.September.26.22
Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127(3):910–917. https://doi.org/10.1104/pp.010548
Jagloottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280(5360):104–106. https://doi.org/10.1126/science.280.5360.104
Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259. https://doi.org/10.1038/srep08259
Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45(D1):D1040–D1045. https://doi.org/10.1093/nar/gkw982
Jin JH, Wang M, Zhang HX, Khan A, Wei AM, Luo DX, Gong ZH (2018) Genome-wide identification of the AP2/ERF transcription factor family in pepper (Capsicum annuum L.). Genome 61(9):663–674. https://doi.org/10.1139/gen-2018-0036
Jofuku KD, den Boer BG, Van MM, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6(9):1211–1225. https://doi.org/10.2307/3869820
Kudo K, Oi T, Uno Y (2014) Functional characterization and expression profiling of a DREB2-type gene from lettuce (Lactuca sativa L.). Plant Cell Tiss Organ Cult 116(1):97–109. https://doi.org/10.1007/s11240-013-0386-z
Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17(11):3155–3175. https://doi.org/10.1105/tpc.105.035568
Li MY, Feng W, Qian J, Jing M, Xiong AS (2014) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L) by deep transcriptome sequencing. Hortic Res 1:10. https://doi.org/10.1038/hortres.2014.10 (eCollection 2014)
Li MY, Feng W, Qian J, Wang GL, Chang T, Xiong AS (2016) Validation and comparison of reference genes for qPCR normalization of celery (Apium graveolens) at different development stages. Front Plant Sci 7:313. https://doi.org/10.3389/fpls.2016.00313
Li H, Wang Y, Wu M, Li L, Li C, Han Z, Yuan J, Chen C, Song W, Wang C (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. https://doi.org/10.3389/fpls.2017.00946
Li MY, Hou XL, Wang F, Tan GF, Xu ZS, Xiong AS (2018) Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol 38(2):172–183. https://doi.org/10.1080/07388551.2017.1312275
Liu L, White MJ, Macrae TH (1999) Transcription factors and their genes in higher plants functional domains, evolution and regulation. Eur J Biochem 262(2):247–257. https://doi.org/10.1046/j.1432-1327.1999.00349.x
Macadam JW, Nelson CJ, Sharp RE (1992) Peroxidase activity in the leaf elongation zone of tall fescue: I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiol 99(3):872–878. https://doi.org/10.2307/4274442
Magnani E, Sjölander K, Hake S (2004) From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 16(9):2265–2277. https://doi.org/10.1105/tpc.104.023135
Miura K, Jin JB, Lee J, Chan YY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19(4):1403–1414. https://doi.org/10.1105/tpc.106.048397
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
Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101(11):3985–3990. https://doi.org/10.1073/pnas.0303029101
Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104(52):21002–21007. https://doi.org/10.1073/pnas.0705639105
Novillo F, Medina J, Rodríguez-Franco M, Neuhaus G, Salinas J (2012) Genetic analysis reveals a complex regulatory network modulating CBF gene expression and Arabidopsis response to abiotic stress. J Exp Bot 63(1):293–304. https://doi.org/10.1093/jxb/err279
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
Pfaffla MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. https://doi.org/10.1093/nar/29.9.e45
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157(1):135–143. https://doi.org/10.1046/j.1469-8137.2003.00658.x
Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45(8):1042–1052. https://doi.org/10.1093/pcp/pch118
Que F, Hou XL, Wang GL, Xu ZS, Tan GF, Li T, Wang YH, Khadr Ahmed, Xiong AS (2019) Advances in research on the carrot, an important root vegetable in the Apiaceae family. Hortic Res 6:69. https://doi.org/10.1038/s41438-019-0150-6
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110. https://doi.org/10.1126/science.290.5499.2105
Rushton Paul J, Somssich Imre E, Ringler Patricia, Shen Qingxi J (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258. https://doi.org/10.1016/j.tplants.2010.02.006
Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374–378. https://doi.org/10.2144/03342mt01
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchishinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophy Res Commun 290(3):998–1009. https://doi.org/10.1006/bbrc.2001.6299
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2010) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292. https://doi.org/10.1046/j.1365-313X.2002.01359.x
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
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
Soltész A, Smedley M, Vashegyi I, Galiba G, Harwood W, Vágújfalvi A (2013) Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J Exp Bot 64(7):1849–1862. https://doi.org/10.1093/jxb/ert050
Song X, Wang J, Ma X, Li Y, Lei T, Wang L, Ge W, Guo D, Wang Z, Li C, Zhao J, Wang X (2016) Origination, expansion, evolutionary trajectory, and expression bias of AP2/ERF superfamily in Brassica napus. Front Plant Sci 7(307):1186. https://doi.org/10.3389/fpls.2016.01186
Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci U S A 95(24):14570–14575. https://doi.org/10.1073/pnas.95.24.14570
Takumi S, Koike A, Nakata M, Kume S, Ohno R, Nakamura C (2003) Cold-specific and light-stimulated expression of a wheat (Triticum aestivum L.) Cor gene Wcor15 encoding a chloroplast-targeted protein. J Exp B 54(391):2265–2274. https://doi.org/10.1093/jxb/erg247
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
Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154(2):571–577. https://doi.org/10.1104/pp.110.161794
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F (2014) The genome of the mesopolyploid crop species Brassica rapa. Nature Genet 43(10):1035–1039. https://doi.org/10.1038/ng.919
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552. https://doi.org/10.1385/1-59259-890-0:571
Wu ZJ, Li XH, Liu ZW, Li H, Wang YX, Zhuang J (2015) Transcriptome-based discovery of AP2/ERF transcription factors related to temperature stress in tea plant (Camellia sinensis). Funct Integr Genomics 15(6):741–752. https://doi.org/10.1007/s10142-015-0457-9
Wuitschick JD, Lindstrom PR, Meyer AE, Karrer KM (2004) Homing endonucleases encoded by germ line-limited genes in Tetrahymena thermophila have APETELA2 DNA binding domains. Eukaryot Cell 3(3):685–694. https://doi.org/10.1128/EC.3.3.685-694.2004
Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59(1):191–203. https://doi.org/10.1007/s11103-005-6503-6
Xu R, Li Y (2011) Control of final organ size by Mediator complex subunit 25 in Arabidopsis thaliana. Development 138(20):4545–4554. https://doi.org/10.1242/dev.071423
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(5):267–276. https://doi.org/10.1016/j.tplants.2012.09.001
Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1(2):641–646. https://doi.org/10.1038/nprot.2006.97
Zhang Y, Chen C, Jin XF, Xiong AS, Peng RH, Hong YH, Yao QH, Chen JM (2009) Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Reports 42(8):486–492. https://doi.org/10.5483/BMBRep.2009,42(8),pp.486
Zhao TJ, Sun S, Liu Y, Liu JM, Liu Q, Yan YB, Zhou HM (2006) Regulating the drought-responsive element (DRE)-mediated signaling pathway by synergic functions of trans-active and trans-inactive DRE binding factors in Brassica napus. J Biol Chem 281(16):10752–10759. https://doi.org/10.1074/jbc.M510535200
Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379(4):985–989. https://doi.org/10.1016/j.bbrc.2008.12.163
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgements
The research was supported by Jiangsu Agricultural Science and Technology Innovation Fund (CX(18)2007), New Century Excellent Talents in University (NCET-11-0670), National Natural Science Foundation of China (31272175), and Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD).
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Li, MY., Liu, JX., Hao, JN. et al. Genomic identification of AP2/ERF transcription factors and functional characterization of two cold resistance-related AP2/ERF genes in celery (Apium graveolens L.). Planta 250, 1265–1280 (2019). https://doi.org/10.1007/s00425-019-03222-2
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DOI: https://doi.org/10.1007/s00425-019-03222-2