Abstract
The Dof proteins are members of a major family of plant transcription factors that contain a single C2/C2 class of zinc-finger DNA-binding domain. The size of gene families and the role of transcription factors in trees have only been partially addressed. We studied the size and structure of the Dof gene family in loblolly and maritime pines. The presence of the conserved Dof domain was a typical feature in the ten Dof genes identified in both pine species. Three of the genes lack intron structures and the other seven have a single intron. An analysis of putative cis elements in the promoter region of the genes suggests that the members of the family play different roles throughout the life cycle of the trees in a way that is unrelated to the subfamily to which they belong. Using the information available in the maritime pine database, we have cloned the corresponding open reading frames and initiated structural and functional studies. The gene expression of maritime pine Dof factors was examined at different developmental stages: from embryo to adult tree. This study has revealed a differential pattern of gene expression based on developmental stage and tissue specificity. The interaction both in vitro and in vivo between Dof factors has been addressed and our data showed a negative effect of Dof 2 in the Dof 5-regulated expression of a target gene in maritime pine. These findings suggest that both genes interact in the regulation of gene expression.
Similar content being viewed by others
References
Boggy GJ, Woolf PJ (2010) A mechanistic model of PCR for accurate quantification of quantitative PCR data. PLoS ONE 5:e12355
Canales J, Flores-Monterrosso A, Rueda-López M, Ávila C, Cánovas FM (2010) Identification of genes regulated by ammonium availability in the roots of maritime pine trees. Amino Acids 39:991–1001
Canales J, Ávila C, Cánovas FM (2011) A maritime pine antimicrobial peptide involved in ammonium nutrition. Plant Cell Environ 34:1443–1453
Cánovas FM, Cantón FR, Gallardo F, García-Gutiérrez A, de Vicente A (1991) Accumulation of glutamine synthetase during early development of maritime pine (Pinus pinaster) seedlings. Planta 185:372–378
Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene group. BMC Genomics 9:561
Craven-Bartle B, Pascual-Moreno MB, Cánovas FM, Avila C (2013) A Myb transcription factor regulates genes of the phenylalanine pathway in maritime pine. Plant J 74:755–766
Diaz I, Martinez M, LaMoneda II, 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
Fernández-Pozo N, Canales J, Guerrero-Fernández D, Villalobos DP, Díaz-Moreno SM, Bautista R, Flores-Monterroso A, Guevara MA, Perdiguero P, Collada C, Cervera MT, Soto A, Ordás R, Cantón FR, Ávila C, Cánovas FM, Claros MG (2011) EuroPineDB: a high-coverage web database for maritime pine transcriptome. BMC Genomics 12:366
Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Ruhl 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
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker John M (ed) The proteomics protocols handbook. Humana Press, Clifton, pp 571–607
Gómez-Maldonado J, Crespillo R, Ávila C, Cánovas FM (2001) Efficient preparation of maritime pine (Pinus pinaster) protoplasts suitable for transgene expression analysis. Plant Mol Biol Rep 19:361–366
Gómez-Maldonado J, Avila C, de la Torre F, Cañas R, Cánovas FM, Campbell MM (2004) Functional interactions between a glutamine synthetase promoter and MYB proteins. Plant J 39:513–526
Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, Camilleri C, Constantino P, Vittorioso P (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14:1253–1263
Hernando-Amado S, González-Calle V, Carbonero P, Barreo-Sicilia C (2012) The family of Dof transcription facotrs in Brachypodium distachyon: phylogenetic comparison with rice and barley DOFs and expression profiling. BMC Plant Biol 12:202
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, de Pamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
Kushwaha H, Gupta S, Singh VK, Rastogi S, Yadav D (2011) Genome wide identification of Dof transcription factor gene family in sorghum and its comparative phylogenetic analysis with rice and Arabidopsis. Mol Biol Rep 38:5037–5053
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van De Peer Y, Rouze 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 30:325–327
Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol 3:17
Martinez M (2011) Plant protein-coding gene families: emerging bioinformatics approaches. Trends Plant Sci 16:558–567
Moreno-Risueño MA, Martínez M, Vicente-Carbajosa J, Carbonero P (2007) The family of Dof transcription factors: from green unicellular algae to vascular plants. Mol Gent Genomics 277:379–790
Park DH, Lim PO, Kim JS, Cho DS, Hong SH, Nam HG (2003) The Arabidopsis COG1 gene encodes a Dof domain transcription factor and negatively regulates phytochrome signaling. Plant J 34:161–171
Rigault P, Boyle B, Lepage P, Cooke JEK, Bousquet J, MacKay JJ (2011) A white spruce gene catalog for conifer genome analysis. Plant Physiol 157:14–28
Ritz C, Spiess AN (2008) qpcR: an R package for sigmoidal model selection in quantitative real-time polymerase chain reaction analysis. Bioinformatics 24:1549–1551
Rogozin IB, Sverdlov AV, Babenko VN, Koonin EV (2005) Analysis of evolution of exon–intron structure of eukaryotic genes. Brief Bioinform 6:118–134
Roy SW, Penny D (2006) Patterns of intron loss and gain in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24:171–181
Rueda-López M, Crespillo R, Cánovas FM, Ávila C (2008) Differential regulation of two glutamine synthetase genes by a single Dof transcription factor. Plant J 56:73–85
Shiu S-H, Shih M-C, Li W-H (2005) Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol 139:18–26
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment thorough sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Umemura Y, Ishiduka T, Yamamoto R, Esaka M (2004) The Dof domain, a zinc finger DNA-binding domain conserved only in higher plants, truly functions as a Cys2/Cys2 Zn finger domain. Plant J 37:741–749
Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci 94:7685–7690
Ward JM, Cufr CA, Denzel MA, Neff MM (2005) The Dof transcription factor OBP3 modulates phytochrome and cryptochrome signaling in Arabidopsis. Plant Cell 17:475–485
Washio K (2003) Functional dissections between GAMYB and Dof transcription factors suggest a role for protein–protein association in the gibberellin-mediated expression of the RAmy1A gene in the rice aleurone. Plant Physiol 133:850–863
Wegrzyn JL, Lee JM, Tearse BR, Neale DB (2008) TreeGenes: a forest tree genome database. Int J Plant Genom Volume 2008, Article ID 412875, 7 pages doi:10.1155/2008/412875
Yanagisawa S (1997) Dof DNA-binding domains of plant transcription factors contribute to multiple protein–protein interactions. Eur J Biochem 230:403–410
Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21:281–288
Yanagisawa S (2002) The Dof family of plant transcription factors. Trend Plant Sci 7:555–560
Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391
Yanagisawa S, Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10:75–89
Zhang B, Chen W, Foley RC, Büttner M, Singh KB (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7:2241–2252
Acknowledgments
We are most grateful to Aranzazu Flores-Monterroso for providing the sequence of Dof 2 used in the production of the recombinant protein. The authors are also grateful for access to the UMA Bioinformatic Platform facilities of the Europine database. This work was supported by grants (CVI-3739) from Junta de Andalucia to C Ávila and (BIO2012-33797) from the Spanish Ministry of Science and Innovation to FM Cánovas. M Rueda-López was supported by a predoctoral fellowship from Junta de Andalucia.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Alia.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rueda-López, M., García-Gutiérrez, A., Cánovas, F.M. et al. The family of Dof transcription factors in pine. Trees 27, 1547–1557 (2013). https://doi.org/10.1007/s00468-013-0903-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-013-0903-z