Abstract
DNA-binding with one finger (Dof) proteins are a large family of transcription factors involved in a variety of biological processes in plants. In rice, 30 different Dof genes have been identified through genome analysis. Here we report the functional characteristics of a rice Dof gene, OsDof12, which encodes a predicted Dof protein. The nuclear localization of OsDof12 was investigated by the transient expression assays of the OsDof12–GFP fusion protein in onion epidermal cells. Trans-activation assays in a yeast one-hybrid system indicated that OsDof12 had transcriptional activity. RNA expression analyses showed that the expression of OsDof12 was not tissue-specific in general and fluctuated at different development stages in rice. In addition, OsDof12 was strongly inhibited by dark treatments. The transgenic lines overexpressing OsDof12 showed early flowering under long-day (LD) conditions, whereas OsDof12 overexpression had no effect on flowering time under short-day (SD) conditions. In transgenic lines overexpressing OsDof12, the transcription levels of Hd3a and OsMADS14 were up-regulated under LD conditions but not SD conditions, whereas the expression of Hd1, OsMADS51, Ehd1 and OsGI did not change under LD and SD conditions. These results suggested that OsDof12 might regulate flowering by controlling the expression of Hd3a and OsMADS14.
Similar content being viewed by others
Abbreviations
- Dof:
-
DNA-binding with one finger
- PCR:
-
Polymerase chain reaction
- SDP:
-
Short-day plant
- LDP:
-
Long-day plant
- Hd1:
-
Heading date 1
- CO:
-
CONSTANS
- Hd3a:
-
Heading date 3a
- FT:
-
Flowering locus T
- GI:
-
GIGANTEA
- RT-PCR:
-
Reverse transcription polymerase chain reaction
- GFP:
-
Green fluorescent protein
- MADS:
-
MCM1, AGAMOUS, DEFICIENS and SRF
- Se5:
-
Photoperiodic sensitivity 5
- SD:
-
Short-day
- LD:
-
Long-day
- Ehd1:
-
Early heading date 1
- ABA:
-
Abscisic acid
- GUS:
-
Glucuronidase
- QTL:
-
Quantitative Trait Loci
References
Baumann K, De Paolis A, Costantino P, Gualberti G (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11:323–334
Chen W, Chao G, Singh KB (1996) The promoter of an H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J 10:955–966
Corbesier L, Coupland G (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Environ 28(1):54–66
Díaz I, Vicente-Carbajosa J, Abraham Z, Martinez M, Isabel-LaMoneda I, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J 29:453–464
Díaz 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
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936
Dong GJ, Ni ZF, Yao YY, Nie XL, Sun QX (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
Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, Camilleri C, Costantino 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
Hayama R, Izawa T, Shimamoto K (2002) Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. Plant Cell Physiol 43:494–504
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282
Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) KFK1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297
Isabel-LaMoneda I, Díaz I, Martínez M, Mena M, Carbonero P (2003) SAD: a new DOF protein from barley that activates transcription of a cathepsin B-like thiol protease gene in the aleurone of germinating seeds. Plant J 33:329–340
Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 16:2006–2020
Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120
Kang HG, Singh K (2000) Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. Plant J 21:329–339
Kang HG, Foley RC, Oñate-Sánchez L, Lin C, Singh KB (2003) Target genes for OBP3, a Dof transcription factor, include novel basic helix-loop-helix domain proteins inducible by salicylic acid. Plant J 35:362–372
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965
Kim SL, Lee SY, Kim HJ, Nam HG, An GH (2007) OsMADS51, a short-day flowering promoter in rice. Plant Physiol 145:1484–1494
Kisu Y, Harada Y, Goto M, Esaka M (1997) Cloning of the pumpkin ascorbate oxidase gene and analysis of a cis-acting region involved in induction by auxin. Plant Cell Physiol 38:631–637
Kisu Y, Ono T, Shimofurutani N, Suzuki M, Esaka M (1998) Characterization and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene. Plant Cell Physiol 39:1054–1064
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105
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
Mackay JP, Crossley M (1998) Zinc fingers are sticking together. Trends Biochem Sci 23:1–4
Martinez M, Rubio-Somoza I, Fuentes R, Lara P, Carbonero P, Díaz I (2005) The barley cystatin gene (Icy) is regulated by DOF transcription factors in aleurone cells upon germination. J Exp Bot 412:547–556
Marzabal P, Gas E, Fontanet P, Vicente-Carbajosa Torrent M, Ludevid MD (2008) The maize Dof protein PBF activates transcription of gamma-zein during maize seed development. Plant Mol Biol 67:441–454
Mena M, Vicente-Carbajosa J, Schmidt RJ, Carbonero P (1998) An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native b-hordein promoter in barley endosperm. Plant J 16:53–62
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
Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(Suppl):S111–S130
Papi M, Sabatini S, Bouchez D, Camilleri C, Costantino P, Vittorioso P (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev 14:28–33
Papi M, Sabatini S, Altamura MM, Hennig L, Schafer E, Costantino P, Vittorioso P (2002) Inactivation of the phloem-specific Dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol 128:411–417
Park DH, Lim PO, Kim JK, 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
Plesch G, Ehrhardt T, Mueller-Roeber B (2001) Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J 28:455–464
Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857
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 290:2105–2110
Robson F, Costa MMR, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619–631
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616
Shigyo M, Tabei N, Yoneyama T, Yanagisawa S (2007) Evolutionary processes during the formation of the plant-specific Dof transcription factor family. Plant Cell Physiol 48:179–185
Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289
Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, Zanor MI, Gershenzon J, Strnad M, Szopa J, Mueller-Roeber B, Witt I (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47:10–24
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036
Thomas B, Vince-Prue D (1997) Photoperiodism in plants. Academic Press, London
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 USA 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 (2001) Identification of Dof proteins with implication in the gibberellin-regulated expression of a peptidase gene following the germination of rice grains. Biochim Biophys Acta 1520:54–62
Washio K (2003) Functional dissections between GAMYB and Dof transcription factors suggest a role for protein–protein associations in the gibberellin-mediated expression of the RAmy1A gene in the rice aleurone. Plant Physiol 133:850–863
Yamamoto MP, Onodera Y, Touno SM, Takaiwa F (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol 141:1694–1707
Yanagisawa S (1995) A novel DNA binding domain that may form a single zinc finger motif. Nucleic Acids Res 23:3403–3410
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 factor. Trends Plant Sci 12:555–560
Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 4:386–391
Yanagisawa S, Izui K (1993) Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. J Biol Chem 268:16028–16036
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
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484
Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312
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
Zhu Y, Cai XL, Wang ZY, Hong MM (2003) An interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem 278:47803–47811
Acknowledgments
This research was supported by grants from National Science Foundation of China (90208001 and 30550005), Chinese Academy of Sciences (KSCX2-SW-306), and the Plant Gene Research Center (Beijing).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, D., Yang, C., Li, X. et al. Functional characterization of rice OsDof12 . Planta 229, 1159–1169 (2009). https://doi.org/10.1007/s00425-009-0893-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-009-0893-7