Abstract
DNA binding with one finger (Dof) proteins are encoded by a ubiquitous plant-specific transcription factor gene family that plays a critical role in various biological processes including fruit ripening and organogenesis. The wild olive (Olea europaea var. sylvestris v1.0) genome was used to identify Dof gene family members using a set of bioinformatics tools. Gene structure, chromosome locations, phylogeny, protein motifs, miRNA targets and tissue-specific expression patterns were analyzed. Here, we identified 51 potential Dof genes unevenly distributed on all chromosomes and a few scaffolds. Dof proteins in olive clustered into eight subgroups (D1, B2, C3, C2.2, C1, C2.1, B1, and A) based on the established Arabidopsis classification. The prevalence of segmental duplication was observed as compared to tandem duplication, and this was the main factor underlying the expansion of the Dof gene family in olive. Tissue-specific expression profiling of OeuDof genes revealed that the majority of OeuDof genes were highly expressed in flowers, stem and meristem tissues. In seed and meristem tissues, cis-regulatory element (CRE) analysis revealed the presence of elements that are specifically responsive to light, circadian, auxin, and ABA. In addition, a comparative analysis between Dof genes in olive and Arabidopsis revealed eight groups or sub-families, although the C3 group of Arabidopsis was not represented in olive. This extensive genome evaluation of the Dof gene family in olive presents a reference for cloning and functional analysis of the members of this gene family.
Similar content being viewed by others
References
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49
Baldoni L, Tosti N, Ricciolini C, Belaj A, Arcioni S, Pannelli G, Germana MA, Mulas M, Porceddu A (2006) Genetic structure of wild and cultivated olives in the central Mediterranean basin. Ann Bot 98:935–942
Beghe D, Piotti A, Satovic Z, de la Rosa R, Belaj A (2017) Pollen-mediated gene flow and fine-scale spatial genetic structure in Olea europaea subsp. europaea var. sylvestris. Ann Bot 119:671–679
Bettaieb I, Bouktila D (2020) Genome-wide analysis of NBS-encoding resistance genes in the Mediterranean olive tree (Olea europaea subsp. europaea var. europaea): insights into their molecular diversity, evolution and function. Tree Genet Genomes 16:1–21
Bondarenko VS, Gelfand MS (2016) Evolution of the exon–intron structure in ciliate genomes. PLoS ONE 11:e0161476
Bouarroudj K, Tamendjari A, Larbat R (2016) Quality, composition and antioxidant activity of Algerian wild olive (Olea europaea L. subsp. Oleaster) oil. Ind Crops Prod 83:484–491
Breton C, Terral JF, Pinatel C, Medail F, Bonhomme F, Berville A (2009) The origins of the domestication of the olive tree. C R Biol 332:1059–1064
Bulow L, Hehl R (2016) Bioinformatic identification of conserved cis-sequences in coregulated genes. Methods Mol Biol 1482:233–245
Cai X, Zhang Y, Zhang C, Zhang T, Hu T, Ye J, Zhang J, Wang T, Li H, Ye Z (2013) Genome-wide analysis of plant-specific Dof transcription factor family in tomato. J Integr Plant Biol 55:552–566
Carbone F, Bruno L, Perrotta G, Bitonti MB, Muzzalupo I, Chiappetta A (2019) Identification of miRNAs involved in fruit ripening by deep sequencing of Olea europaea L. transcriptome. PLoS ONE 14:e0221460
Chen H, Ahmad M, Rim Y, Lucas WJ, Kim JY (2013) Evolutionary and molecular analysis of D of transcription factors identified a conserved motif for intercellular protein trafficking. New Phytol 198:1250–1260
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202
Cokol M, Nair R, Rost B (2000) Finding nuclear localization signals. EMBO Rep 1:411–415
Colombo M (2016) Botanicals authentication in food, food supplements and herbal medicinal products. Plant Biosyst Int J Deal All Aspects Plant Biol 150:22–26
Corrales AR, Nebauer SG, Carrillo L, Fernandez-Nohales P, Marques J, Renau-Morata B, Granell A, Pollmann S, Vicente-Carbajosa J, Molina RV, Medina J (2014) Characterization of tomato cycling Dof factors reveals conserved and new functions in the control of flowering time and abiotic stress responses. J Exp Bot 65:995–1012
Cruz F, Julca I, Gómez-Garrido J, Loska D, Marcet-Houben M, Cano E, Galán B, Frias L, Ribeca P, Derdak S (2016) Genome sequence of the olive tree, Olea europaea. Gigascience 5:29
Diaz I, Martinez M, Isabel-LaMoneda I, Rubio-Somoza I, Carbonero P (2005) The DOF protein, SAD, interacts with GAMYB in plant nuclei and activates transcription of endosperm-specific genes during barley seed development. Plant J 42:652–662
Diez CM, Trujillo I, Martinez-Urdiroz N, Barranco D, Rallo L, Marfil P, Gaut BS (2015) Olive domestication and diversification in the Mediterranean Basin. New Phytol 206:436–447
Dong G, Ni Z, Yao Y, Nie X, Sun Q (2007) Wheat Dof transcription factor WPBF interacts with TaQM and activates transcription of an alpha-gliadin gene during wheat seed development. Plant Mol Biol 63:73–84
Dong C, Hu H, Xie J (2016) Genome-wide analysis of the DNA-binding with one zinc finger (Dof) transcription factor family in bananas. Genome 59:1085–1100
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230
Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86
Gardiner J, Sherr I, Scarpella E (2010) Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 54(8–9):1389–1396
Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook. Springer, Berlin, pp 571–607
Goodstein D, Batra S, Carlson J, Hayes R, Phillips J, Shu S, Schmutz J, Rokhsar D (2014) Phytozome comparative plant genomics portal
Gu X, Zou Y, Su Z, Huang W, Zhou Z, Arendsee Z, Zeng Y (2013) An update of DIVERGE software for functional divergence analysis of protein family. Mol Biol Evol 30:1713–1719
Guo Y (2009) Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21:3518–3534
Gupta S, Malviya N, Kushwaha H, Nasim J, Bisht NC, Singh V, Yadav D (2015) Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241:549–562
Hernando-Amado S, Gonzalez-Calle V, Carbonero P, Barrero-Sicilia C (2012) The family of DOF transcription factors in Brachypodium distachyon: phylogenetic comparison with rice and barley DOFs and expression profiling. BMC Plant Biol 12:202
Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res 26:358–359
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
Horton P, Park K-J, Obayashi T, Nakai K (2006) Protein subcellular localization prediction with WoLF PSORT. In: Proceedings of the 4th Asia-Pacific bioinformatics conference. World Scientific, Singapore, pp 39–48
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
Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 9:486–487
Imaizumi T (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297
Iwamoto M, Tagiri A (2016) Micro RNA-targeted transcription factor gene RDD 1 promotes nutrient ion uptake and accumulation in rice. Plant J 85(4):466–477
Jones DM, Vandepoele K (2020) Identification and evolution of gene regulatory networks: insights from comparative studies in plants. Curr Opin Plant Biol 54:42–48
Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338
Jung JH, Lee S, Yun J, Lee M, Park CM (2014) The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci 215–216:29–38
Kang W-H, Kim S, Lee H-A, Choi D, Yeom S-I (2016) Genome-wide analysis of Dof transcription factors reveals functional characteristics during development and response to biotic stresses in pepper. Sci Rep 6:33332
Kassa A, Konrad H, Geburek T (2019) Molecular diversity and gene flow within and among different subspecies of the wild olive (Olea europaea L.): a review. Flora 250:18–26
Kim BH, Kwon Y, Lee BH, Nam KH (2014) Overexpression of miR172 suppresses the brassinosteroid signaling defects of bak1 in Arabidopsis. Biochem Biophys Res Commun 447:479–484
Konishi M, Yanagisawa S (2007) Sequential activation of two Dof transcription factor gene promoters during vascular development in Arabidopsis thaliana. Plant Physiol Biochem 45(8):623–629
Koralewski TE, Krutovsky KV (2011) Evolution of exon–intron structure and alternative splicing. PLoS ONE 6:e18055
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Kyriakopoulou CI, Kalogianni DP (2020) Genetic identification of the wild form of olive (Olea europaea var. sylvestris) using allele-specific real-time PCR. Foods 9:467
Lafka T-I, Lazou AE, Sinanoglou VJ, Lazos ES (2013) Phenolic extracts from wild olive leaves and their potential as edible oils antioxidants. Foods 2:18–31
Li W, Wang T, Zhang Y, Li Y (2016) Overexpression of soybean miR172c confers tolerance to water deficit and salt stress, but increases ABA sensitivity in transgenic Arabidopsis thaliana. J Exp Bot 67:175–194
Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003a) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol 3:17
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS, Thanki N, Yamashita RA, Yang M, Zhang D, Zheng C, Lanczycki CJ, Marchler-Bauer A (2020) CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48:D265–D268
Lumaret R, Ouazzani N (2001) Plant genetics. Ancient wild olives in Mediterranean forests. Nature 413:700
Ma J, Li M-Y, Wang F, Tang J, Xiong A-S (2015) Genome-wide analysis of Dof family transcription factors and their responses to abiotic stresses in Chinese cabbage. BMC Genomics 16:33
Malviya N, Gupta S, Singh V, Yadav M, Bisht N, Sarangi B, Yadav D (2015) Genome wide in silico characterization of Dof gene families of pigeonpea (Cajanus cajan (L.) Millsp.). Mol Biol Rep 42:535–552
Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130:111–119
Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo JO, Mellor N, Help-Rinta-Rahko H, Otero S, Smet W, Boekschoten M (2019) Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature 565(7740):490–494
Mohamed R, Pineda M, Aguilar M (2007) Antioxidant capacity of extracts from wild and crop plants of the Mediterranean region. J Food Sci 72:S059–S063
Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128
Moreno-Risueno MA, Martinez M, Vicente-Carbajosa J, Carbonero P (2007) The family of DOF transcription factors: from green unicellular algae to vascular plants. Mol Genet Genomics 277:379–390
Morgan CC, Loughran NB, Walsh TA, Harrison AJ, O’Connell MJ (2010) Positive selection neighboring functionally essential sites and disease-implicated regions of mammalian reproductive proteins. BMC Evol Biol 10:39
Nasim J, Malviya N, Kumar R, Yadav D (2016) Genome-wide bioinformatics analysis of Dof transcription factor gene family of chickpea and its comparative phylogenetic assessment with Arabidopsis and rice. Plant Syst Evol 302:1009–1026
Negi J, Moriwaki K, Konishi M, Yokoyama R, Nakano T, Kusumi K, Hashimoto-Sugimoto M, Schroeder JI, Nishitani K, Yanagisawa S (2013) A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr Biol 23:479–484
Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. Plant Sci 209:32–45
Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316
Paudel S, Magrati T, Lamichhane JR (2011) Antimicrobial activity of wild olive crude extracts in vitro. Int J Pharma Sci Res 2:110–113
Peng FY, Weselake RJ (2011) Gene coexpression clusters and putative regulatory elements underlying seed storage reserve accumulation in Arabidopsis. BMC Genomics 12:286
Ramirez-Parra E, Perianez-Rodriguez J, Navarro-Neila S, Gude I, Moreno-Risueno MA, Del Pozo JC (2017) The transcription factor OBP4 controls root growth and promotes callus formation. New Phytol 213:1787–1801
Ramírez-Tejero JA, Jiménez-Ruiz J, Leyva-Pérez MD, Barroso JB, Luque F (2020) Gene expression pattern in olive tree organs (Olea europaea L.). Genes 11(5):544
Rombauts S, Déhais P, Van Montagu M, Rouzé P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27:295–296
Rymen B, Kawamura A, Schafer S, Breuer C, Iwase A, Shibata M, Ikeda M, Mitsuda N, Koncz C, Ohme-Takagi M, Matsui M, Sugimoto K (2017) ABA suppresses root hair growth via the OBP4 transcriptional regulator. Plant Physiol 173:1750–1762
Samad AF, Sajad M, Nazaruddin N, Fauzi IA, Murad A, Zainal Z, Ismail I (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565
Song A, Gao T, Li P, Chen S, Guan Z, Wu D, Xin J, Fan Q, Zhao K, Chen F (2016) Transcriptome-wide identification and expression profiling of the DOF transcription factor gene family in Chrysanthemum morifolium. Front Plant Sci 7:199
Spanudakis E, Jackson S (2014) The role of microRNAs in the control of flowering time. J Exp Bot 65(2):365–380
Sun Z, Guo T, Liu Y, Liu Q, Fang Y (2015) The roles of Arabidopsis CDF2 in transcriptional and posttranscriptional regulation of primary microRNAs. PLoS Genet 11:e1005598
Takano M, Haque MA, Odaira S, Nakata K, Sasaki N, Nyunoya H (2013) Overexpression of a tobacco Dof transcription factor BBF1 stimulates the transcription of the tobacco mosaic virus resistance gene N and defense-related responses including ROS production. Plant Biotechnol. https://doi.org/10.5511/plantbiotechnology.12.1207a
Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643
Terzi LC (2008) Regulation of flowering time by RNA processing. Springer, Berlin
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thompson JD, Gibson TJ, Higgins DG (2003) Multiple sequence alignment using ClustalW and ClustalX. Curr Protocols Bioinform 1:2–3
Unver T, Wu Z, Sterck L, Turktas M, Lohaus R, Li Z, Yang M, He L, Deng T, Escalante FJ (2017) Genome of wild olive and the evolution of oil biosynthesis. Proc Natl Acad Sci 114:E9413–E9422
Venkatesh J, Park SW (2015) Genome-wide analysis and expression profiling of DNA-binding with one zinc finger (Dof) transcription factor family in potato. Plant Physiol Biochem 94:73–85
Wang Y, Fu B, Pan L, Chen L, Fu X, Li K (2013a) Overexpression of Arabidopsis Dof1, GS1 and GS2 enhanced nitrogen assimilation in transgenic tobacco grown under low-nitrogen conditions. Plant Mol Biol Report 31:886–900
Wang Y, Li J, Paterson AH (2013b) MCScanX-transposed: detecting transposed gene duplications based on multiple colinearity scans. Bioinformatics 29:1458–1460
Wei Q, Wang W, Hu T, Hu H, Mao W, Zhu Q, Bao C (2018) Genome-wide identification and characterization of Dof transcription factors in eggplant (Solanum melongena L.). PeerJ 6:e4481
Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117
Wen CL, Cheng Q, Zhao L, Mao A, Yang J, Yu S, Weng Y, Xu Y (2016) Identification and characterisation of Dof transcription factors in the cucumber genome. Sci Rep 6:23072
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759
Wu J, Fu L, Yi H (2016a) Genome-wide identification of the transcription factors involved in citrus fruit ripening from the transcriptomes of a late-ripening sweet orange mutant and its wild Type. PLoS ONE 11:e0154330
Wu Z, Cheng J, Cui J, Xu X, Liang G, Luo X, Chen X, Tang X, Hu K, Qin C (2016b) Genome-wide identification and expression profile of Dof transcription factor gene family in pepper (Capsicum annuum L.). Front Plant Sci 7:574
Xu P, Cai W (2019) Nitrate-responsive OBP4-XTH9 regulatory module controls lateral root development in Arabidopsis thaliana. PLoS Genet 15:e1008465
Xu P, Chen H, Ying L, Cai W (2016) AtDOF5.4/OBP4, a DOF transcription factor gene that negatively regulates cell cycle progression and cell expansion in Arabidopsis thaliana. Sci Rep 6:27705
Yamashino T, Yamawaki S, Hagui E, Ishida K, Ueoka-Nakanishi H, Nakamichi N, Mizuno T (2013) Clock-controlled and FLOWERING LOCUS T (FT)-dependent photoperiodic pathway in Lotus japonicus II: characterization of a microRNA implicated in the control of flowering time. Biosci Biotechnol Biochem 77:1179–1185
Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7:555–560
Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17:209–214
Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci 101:7833–7838
Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503
Yang X, Tuskan GA (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830
Yang J, Yang M-F, Zhang W-P, Chen F, Shen S-H (2011) A putative flowering-time-related Dof transcription factor gene, JcDof3, is controlled by the circadian clock in Jatropha curcas. Plant Sci 181:667–674
Yang FX, Zhu GF, Wang Z, Liu HL, Huang D (2015) A putative miR172-targeted CeAPETALA2-like gene is involved in floral patterning regulation of the orchid Cymbidium ensifolium. Genet Mol Res 14:12049–12061
Zou HF, Zhang YQ, Wei W, Chen HW, Song QX, Liu YF, Zhao MY, Wang F, Zhang BC, Lin Q (2013) The transcription factor AtDOF4.2 regulates shoot branching and seed coat formation in Arabidopsis. Biochem J 449:373–388
Acknowledgements
This work was supported by the University of the Punjab, Lahore, Pakistan.
Author information
Authors and Affiliations
Contributions
MS, M, MH, SAAAA, RMA, NA, MAJ and FG were involved in data analysis. MS and RMA provided overall direction and experimental design. SAAAA, MH, NA and M wrote the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Seon-In Yeom, Ph.D.
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.
Rights and permissions
About this article
Cite this article
Mariyam, Shafiq, M., Haseeb, M. et al. Genome-wide identification and characterization of a plant-specific Dof transcription factor gene family in olive (Olea europaea) and its comparison with Arabidopsis. Hortic. Environ. Biotechnol. 62, 949–968 (2021). https://doi.org/10.1007/s13580-021-00366-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13580-021-00366-7