Genome-Wide Identification Transcriptional Expression Analysis of E2F-DP Transcription Factor Family in Wheat

Recent studies have shown that a variety of cytokines are involved in cell cycle regulation and that the E2F-DP transcription factor (TF) family is one of the important regulatory links. However, little is known about E2F-DP gene family members and their evolutionary and functional characteristics in plants, especially under stress conditions. Their characterization has not been performed in bread wheat (Triticum aestivum). In this study, 27 E2F-DP genes were identified from the wheat genome (TaE2F-DP). The phylogenetic analysis split these 27 genes into three groups. Five typical conserved motifs of TaE2F-DP protein ranging in length from 28 to 50 amino acid residues had been found. Using chromosome location, we found that the E2F-DP gene family members were distributed on all 21 chromosomes of wheat. Conjoint analysis indicated the association between E2F-DP genes in wheat and its three ancestors (T. urartu, T. dicoccoides, and Aegilops tauschii). Transcriptome analysis showed that in several genes, expression was stress related. To uncover the reason for induction expression patterns of TaE2F-DPs during abiotic and biotic stresses in wheat, the cis-regulatory elements functionally associated with stress responding and hormones in the promoter region of TaE2F-DPs were analyzed. In addition, qRT-PCR results further confirmed that these TaE2F-DP genes are involved in wheat stress response. In summary, this study provided evolutionary and functional information of TaE2F-DP gene family members and revealed the gene expression of different members under different stress treatments. These findings provide comprehensive insights into the E2F-DP family members in wheat and offer candidate E2F-DP genes for further researches on their roles in stress resistance and potential for improving wheat breeding programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

• Get 10 units per month
• Download Article/Chapter or eBook
• 1 Unit = 1 Article or 1 Chapter
• Cancel anytime

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Rent this article via DeepDyve

Similar content being viewed by others

Genome-Wide Identification and Characterization of the E2F/DP Transcription Factor Family in Triticum aestivum L.

Genome-wide identification and expression analysis of the GRAS gene family under abiotic stresses in wheat (Triticum aestivum L.)

Genome-wide exploration of C2H2 zinc finger family in durum wheat (Triticum turgidum ssp. Durum): insights into the roles in biological processes especially stress response

References

• Andorf CM, Cannon EK, Portwood JL et al (2015) MaizeGDB update: new tools, data and interface for the maize model organism database. Nucleic Acids Res 44(D1):D1195–D1201. https://doi.org/10.1093/nar/gkv1007ArticleCASPubMedPubMed CentralGoogle Scholar
• Alaux M, Rogers J, Letellier T et al (2018) Linking the International Wheat Genome Sequencing Consortium bread wheat reference genome sequence to wheat genetic and phenomic data. Genome Biol 19:111. https://doi.org/10.1186/s13059-018-1491-4ArticleCASPubMedPubMed CentralGoogle Scholar
• Liu B, Kun Wu (2000) Advances in the role of E2F transcription factors in cell cycle regulation. Weisheng Dulixue Zazhi 14(1):53–55. https://doi.org/10.3969/j.issn.1002-3127.2000.01.020ArticleCASGoogle Scholar
• Berardini TZ, Reiser L, Li D et al (2015) The Arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis 53(8):474–485. https://doi.org/10.1002/dvg.22877ArticleCASPubMedPubMed CentralGoogle Scholar
• Bisova K, Krylov DM, Umen JG (2005) Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol 137(2):475–491. https://doi.org/10.1104/pp.104.054155ArticleCASPubMedPubMed CentralGoogle Scholar
• Brenchley R, Spannagl M, Pfeifer M et al (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705–710. https://doi.org/10.1038/nature11650
• Coffman JA (2004) Cell cycle development. Developmental Cell 6(3):321–7. https://doi.org/10.1016/S1534-5807(04)00067-X
• Cooper S, Shayman JA (2001) Revisiting retinoblastoma protein phosphorylation during the mammalian cell cycle. Cellular and Molecular Life Sciences CMLS 58(4):580–95. https://doi.org/10.1007/PL00000883
• Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264. https://doi.org/10.1146/annurev.arplant.54.031902.134836ArticleCASPubMedGoogle Scholar
• Dyson N (1998) The regulation of E2F by pRB-family proteins. Gene Dev 12: 2245–2262. https://doi.org/10.1101/gad.12.15.2245
• Fang ZW, He YQ, Liu YK, Jiang WQ, Song JH, Wang SP, Ma DF, Yin JL (2020) Bioinformatic identification and analyses of the non-specific lipid transfer proteins in wheat. J Integr Agr 19(05):1170–1185. https://doi.org/10.1016/S2095-3119(19)62776-0ArticleCASGoogle Scholar
• Guo J, Song J, Wang F et al (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol Biol 64(4):349–360. https://doi.org/10.1007/s11103-007-9154-yArticleCASPubMedGoogle Scholar
• Gutierrez C, Ramirez-Parra E, Castellano MM et al (2002) G1 to S transition: more than a cell cycle engine switch. Curr Opin Plant Biol 5(6):480–486. https://doi.org/10.1016/S1369-5266(02)00301-1ArticleCASPubMedGoogle Scholar
• Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168(4):2197–206. https://doi.org/10.1534/genetics.104.032193
• Hu L, Liu S (2011) Genome-Wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genet Mol Biol 34(4):624–633. https://doi.org/10.1590/S1415-47572011005000054ArticleCASPubMedPubMed CentralGoogle Scholar
• Huttly AK (1988) Sequence heterogeneity and differential expression of the alpha-Amy2 gene family in wheat. Mol Gen Genet 214(2):232–240. https://doi.org/10.1007/BF00337716ArticleCASPubMedGoogle Scholar
• Iaquinta PJ, Lees JA (2007) Life and death decisions by the E2F transcription factors. Curr Opin Cell Biol 19(6):649–657. https://doi.org/10.1016/j.ceb.2007.10.006ArticleCASPubMedPubMed CentralGoogle Scholar
• International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788. https://doi.org/10.1126/science.1251788ArticleCASGoogle Scholar
• Jiang WJ, Yang LY, He YH, Zhang HZ, Li WL, Chen HC, Ma DM, Yin JY (2019) Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum). PeerJ Preprints 6:e27402v1. https://doi.org/10.7717/peerj.8062
• Kovesdi I, Reichel R, Nevins JR (1986) Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45(2):219–228. https://doi.org/10.1016/0092-8674(86)90386-7ArticleCASPubMedGoogle Scholar
• Lammens T, Li J, Leone G, Veylder LD (2009) Atypical E2Fs: new players in the E2F transcription factor family. Trends Cell Biol 19(3):111–118. https://doi.org/10.1016/j.tcb.2009.01.002ArticleCASPubMedPubMed CentralGoogle Scholar
• Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
• Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320. https://doi.org/10.1093/molbev/msn067ArticleCASPubMedGoogle Scholar
• Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer Y, Rouzé 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(1):325–327. https://doi.org/10.1093/nar/30.1.325ArticleCASPubMedPubMed CentralGoogle Scholar
• Li Z (2015) Identification and expression analysis of the E2F/DP genes under salt stress in Medicago truncatula. Dissertation, Northeast Forestry University. (in Chinese with English abstract) https://doi.org/10.1007/s13258-014-0218-5
• Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2 -ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262ArticleCASPubMedGoogle Scholar
• Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804 ArticleCASGoogle Scholar
• Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux CR, Albani D (2002) The E2F family of transcription factors from Arabidopsis thaliana novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 277(12):9911–9919. https://doi.org/10.1074/jbc.M110616200ArticleCASPubMedGoogle Scholar
• Ma DF, Fang ZW, Yin JL, Chao KX, Jing JX, Li Q (2016) Molecular mapping of stripe rust resistance gene YrHu derived from Psathyrostachys huashanica. Mol Breeding 36:64–93. https://doi.org/10.1007/s11032-016-0487-6ArticleCASGoogle Scholar
• Mohseni S, Che H, Djillali Z et al (2012) Wheat CBF gene family: identification of polymorphisms in the CBF coding sequence. Genome 55(12):865–881. https://doi.org/10.1139/gen-2012-0112ArticleCASPubMedGoogle Scholar
• Moolhuijzen P, Dunn DS, Bellgard M et al (2007) Wheat genome structure and function: genome sequence data and the International Wheat Genome Sequencing Consortium. Aust J Agr Res 58:470–475. https://doi.org/10.1071/AR06155ArticleCASGoogle Scholar
• Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116(2):221–234. https://doi.org/10.1016/S0092-8674(03)01080-8ArticleCASPubMedGoogle Scholar
• Müller H, Moroni MC, Vigo E et al (1997) Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol Cell Biol 17(9):5508–5520. https://doi.org/10.1128/mcb.17.9.5508
• Muthamilarasan M, Prasad M (2014) An overview of wheat genome sequencing and its implications for crop improvement. J Genet 93:619–622. https://doi.org/10.1007/s12041-014-0455-zArticlePubMedGoogle Scholar
• Naouar N , Vandepoele K , Lammens T et al (2010) Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J 57(1):184–194. https://doi.org/10.1111/j.1365-313X.2008.03662.x
• Ouyang S, Zhu W, Hamilton J et al (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35(Database): D883-D887. https://doi.org/10.1093/nar/gkl976
• Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Mol Biol 10(1):11. https://doi.org/10.1186/1471-2199-10-11ArticleCASPubMedPubMed CentralGoogle Scholar
• Pingault L, Choulet F, Alberti A et al (2015) Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome. Genome Biol 16:29. https://doi.org/10.1186/s13059-015-0601-9ArticleCASPubMedPubMed CentralGoogle Scholar
• Ramirez-Parra E, Fründt C, Gutierrez C (2010) A genome-wide identification of E2F-regulated genes in Arabidopsis. Plant J Cell Mol Biol 33(4):801–811. https://doi.org/10.1046/j.1365-313X.2003.01662.xArticleGoogle Scholar
• Rudi A, IWGSC, Kellye E, Nils S et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403). https://doi.org/10.1126/science.aar7191
• Sakuma Y, Maruyama K, Osakabe Y et al (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18(5):1292–1309 ArticleCASGoogle Scholar
• Sander VDH, Dyson NJ (2008) Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 9:713–724. https://doi.org/10.1038/nrm2469ArticleCASGoogle Scholar
• Shen WH (2002) The plant E2F-Rb pathway and epigenetic control. Trends Plant Sci 7(11):505–511. https://doi.org/10.1016/s1360-1385(02)02351-8ArticleCASPubMedGoogle Scholar
• Sherr CJ (1996) Cancer cell cycles. Science 274:1672–1677. https://doi.org/10.1126/science.274.5293.1672
• Slansky JE, Farnham PJ (1996) Introduction to the E2F family: protein structure and gene regulation. Transcriptional Control of Cell Growth 1-30. https://doi.org/10.1007/978-3-642-79910-5_1
• Song J, Ma D, Yin J, Yang L, He Y, Zhu Z, Tong H, Chen L, Zhu G, Liu Y, Gao C (2019) Genome-wide characterization and expression profiling of squamosa promoter binding protein-like (SBP) transcription factors in wheat (Triticum aestivum L.). Agronomy 9, 527. https://doi.org/10.3390/agronomy9090527
• Stevaux O, Dyson NJ (2002) A revised picture of the E2F transcriptional network and RB function. Curr Opin Cell Biol 14(6):684–691. https://doi.org/10.1016/S0955-0674(02)00388-5ArticleCASPubMedGoogle Scholar
• Sun C, Zhang P, Fang Z, Zhang X, Yin JL, Ma D (2018) Genetic analysis and molecular mapping of stripe rust resistance in an excellent wheat line Sanshumai1. J Plant Pathol 101:473–480. https://doi.org/10.1007/s42161-018-0166-zArticleGoogle Scholar
• Takahasi Y (2000) Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Gene Dev 14(7):804–816 ArticleGoogle Scholar
• Trimarchi JM, Lees JA (2002) Transcription sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3(1):11–20. https://doi.org/10.1038/nrm714ArticleCASPubMedGoogle Scholar
• Tsuda K, Tsvetanov S, Takumi S et al (2000) New members of a cold-responsive group-3 Lea/Rab-related Cor gene family from common wheat (Triticum aestivum L.). Genes Genet Syst 75(4):179–188. https://doi.org/10.1266/ggs.75.179
• Vandepoele K, Raes J, de Veylder L, Rouze P, Rombauts S, Inze D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14(4):903–916 ArticleCASGoogle Scholar
• Veylder LD, Jér me Joubès, Dirk Inzé, (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6(6):536–543. https://doi.org/10.1016/j.pbi.2003.09.001ArticleCASPubMedGoogle Scholar
• Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (2005) Protein identification and analysis tools in the ExPASy Server. Humana Press. https://doi.org/10.1385/1-59259-890-0:571ArticleGoogle Scholar
• Yan X, Jiang T, Wang X et al (2018) Identification and related expression analysis of E2F/DP transcription factor gene family in Moso bamboo. Mol Plant Breed 16(21):127–133. (in Chinese with English abstract) https://doi.org/10.13271/j.mpb.016.006997
• Chen X, Zhu Q (2014) Progress in E2F transcription factor family. Mod Med 9:1109–1113. https://doi.org/10.3969/j.issn.1671-7562.2014.09.041ArticleGoogle Scholar
• Xu G, Guo C, Shan H et al (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA 109(4):1187–1192. https://doi.org/10.1073/pnas.1109047109ArticlePubMedPubMed CentralGoogle Scholar
• Yin JL, Fang ZW, Sun C et al (2018) Rapid identification of a stripe rust resistant gene in a space-induced wheat mutant using specific locus amplified fragment (SLAF) sequencing. Sci Rep 8(1):3086. https://doi.org/10.1038/s41598-018-21489-5ArticleCASPubMedPubMed CentralGoogle Scholar
• Zhou X, Zhu X, Shao W et al (2020) Genome-wide mining of wheat DUF966 gene family provides new insights into salt stress responses. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.569838
• Zhu YX, Xu XB, Hu YH et al (2015) Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus L. Plant Cell Rep 34:1629–1646. https://doi.org/10.1007/s00299-015-1814-9ArticleCASPubMedGoogle Scholar

Funding

This work was partially supported by the Key Project of Hubei Provincial Department of Education (D20191305) and Open Project Program of Key Laboratory of Integrated Pest Management on Crops in Central China/Hubei Key Laboratory of Crop Diseases, Insect Pests, and Weeds Control (2020ZTSJJ8).

Author information

Authors and Affiliations

1. Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education/Hubei Collaborative Innovation Center for Grain Industry/College of Agriculture, Yangtze University, Hubei, Jingzhou, 434000, China Haotian Zhang, Wenqiang Jiang, Junliang Yin & Dongfang Ma
2. Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu, Nanjing, 210014, China Haotian Zhang, Wenqiang Jiang, Huaigu Chen & Wei Li
3. Enshi Tobacco Company of Hubei Province, Enshi, Hubei, 445000, China Pengliang Xia
4. Institute of Plant Protection and Soil Science, Hubei Academy of Agricultural Sciences, Wuhan, Hubei, 430064, China Dongfang Ma

1. Haotian Zhang