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Transcriptional regulation of seed storage protein genes in Arabidopsis and cereals

Published online by Cambridge University Press:  31 August 2011

Dong-Mei Xi  and
Cheng-Chao Zheng
Dong-Mei Xi
Affiliation:
Experimental Center, Linyi University, Linyi, Shandong276005, PR China State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, Shandong271018, PR China
Cheng-Chao Zheng*
Affiliation:
State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, Shandong271018, PR China
*
*Correspondence Fax: 86-538-8226399 Email: cczheng@sdau.edu.cn
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Abstract

Seed storage proteins (SSPs) are synthesized during development and the expression of their genes is under tight tissue-specific and temporal transcriptional regulation. In this review we summarize the current knowledge concerning the regulatory steps controlling SSP synthesis in Arabidopsis and cereals, which involves the interaction of cis regulatory elements with corresponding trans-acting factors. In some cases, the regulation of SSP genes requires the concerted action of multiple transcription factors (TFs). There is an evolutionary conservation between the prolamins (the main group of SSPs in many cereal grains) and a major group of dicot seed albumins; this relates to both the regulatory elements and the TFs that are functionally exchangeable between the monocot and dicot species.

Keywords

Arabidopsiscerealpromoter regionseed storage proteintranscription factors
Type
Review Article
Information
Seed Science Research , Volume 21 , Issue 4 , December 2011 , pp. 247 - 254
Copyright
Copyright © Cambridge University Press 2011

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References

Albani, D., Hammond-Kosack, M.C., Smith, C., Conlan, S., Colot, V., Holdsworth, M. and Bevan, M.W. (1997) The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9, 171–184.Google ScholarPubMed
Alonso, R., Onate-Sanchez, L., Weltmeier, F., Ehlert, A., Diaz, I., Dietrich, K., Vicente-Carbajosa, J. and Droge-Laser, W. (2009) A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21, 1747–1761.Google Scholar
Angeles-Nunez, J.G. and Tiessen, A. (2011) Mutation of the transcription factor LEAFY COTYLEDON 2 alters the chemical composition of Arabidopsis seeds, decreasing oil and protein content, while maintaining high levels of starch and sucrose in mature seeds. Journal of Plant Physiology, doi:10.1016/j.jplph.2011.05.003.CrossRefGoogle ScholarPubMed
Baumann, K., De Paolis, A., Costantino, P. and 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.CrossRefGoogle ScholarPubMed
Baumlein, H., Nagy, I., Villarroel, R., Inze, D. and Wobus, U. (1992) Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant Journal 2, 233–239.CrossRefGoogle ScholarPubMed
Chamberland, S., Daigle, N. and Bernier, F. (1992) The legumin boxes and the 3′ part of a soybean β-conglycinin promoter are involved in seed gene expression in transgenic tobacco plants. Plant Molecular Biology 19, 937–949.CrossRefGoogle ScholarPubMed
Diaz, I., Vicente-Carbajosa, J., Abraham, Z., Martinez, M., Isabel-La Moneda, I. and Carbonero, P. (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant Journal 29, 453–464.Google Scholar
Diaz, I., Martinez, M., Isabel-LaMoneda, I., Rubio-Somoza, I. and 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 Journal 42, 652–662.CrossRefGoogle ScholarPubMed
Dong, G., Ni, Z., Yao, Y., Nie, X. and Sun, Q. (2007) Wheat Dof transcription factor WPBF interacts with TaQM and activates transcription of an α-gliadin gene during wheat seed development. Plant Molecular Biology 63, 73–84.Google Scholar
Gazzarrini, S., Tsuchiya, Y., Lumba, S., Okamoto, M. and McCourt, P. (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Developmental Cell 7, 373–385.Google Scholar
Gehring, M., Bubb, K.L. and Henikoff, S. (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451.CrossRefGoogle ScholarPubMed
Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F. and Goodman, H.M. (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4, 1251–1261.Google ScholarPubMed
Gubler, F., Kalla, R., Roberts, J.K. and Jacobsen, J.V. (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI α-amylase gene promoter. Plant Cell 7, 1879–1891.Google Scholar
Hammond-Kosack, M.C., Holdsworth, M.J. and Bevan, M.W. (1993) In vivo footprinting of a low molecular weight glutenin gene (LMWG-1D1) in wheat endosperm. EMBO Journal 12, 545–554.Google Scholar
Holdsworth, M.J., Munoz-Blanco, J., Hammond-Kosack, M., Colot, V., Schuch, W. and Bevan, M.W. (1995) The maize transcription factor Opaque-2 activates a wheat glutenin promoter in plant and yeast cells. Plant Molecular Biology 29, 711–720.CrossRefGoogle ScholarPubMed
Hsieh, T.F., Ibarra, C.A., Silva, P., Zemach, A., Eshed-Williams, L., Fischer, R.L. and Zilberman, D. (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451–1454.Google Scholar
Isabel-LaMoneda, I., Diaz, I., Martinez, M., Mena, M. and 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 Journal 33, 329–340.Google Scholar
Izawa, T., Foster, R., Nakajima, M., Shimamoto, K. and Chua, N.H. (1994) The rice bZIP transcriptional activator RITA-1 is highly expressed during seed development. Plant Cell 6, 1277–1287.Google Scholar
Kagaya, Y., Toyoshima, R., Okuda, R., Usui, H., Yamamoto, A. and Hattori, T. (2005) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant and Cell Physiology 46, 399–406.Google Scholar
Kawakatsu, T. and Takaiwa, F. (2010) Cereal seed storage protein synthesis: fundamental processes for recombinant protein production in cereal grains. Plant Biotechnology Journal 8, 939–953.CrossRefGoogle ScholarPubMed
Kawakatsu, T., Yamamoto, M.P., Touno, S.M., Yasuda, H. and Takaiwa, F. (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant Journal 59, 908–920.Google Scholar
Keith, K., Kraml, M., Dengler, N.G. and McCourt, P. (1994) Fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6, 589–600.Google Scholar
Kreis, M. and Shewry, P.R. (1989) Unusual features of cereal seed protein structure and evolution. Bioessays 10, 201–207.Google Scholar
Kroj, T., Savino, G., Valon, C., Giraudat, J. and Parcy, F. (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130, 6065–6073.Google Scholar
Lara, P., Onate-Sanchez, L., Abraham, Z., Ferrandiz, C., Diaz, I., Carbonero, P. and Vicente-Carbajosa, J. (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. Journal of Biological Chemistry 278, 21003–21011.Google Scholar
Lelievre, J.M., Oliveira, L.O. and Nielsen, N.C. (1992) 5′-CATGCAT-3′ elements modulate the expression of glycinin genes. Plant Physiology 98, 387–391.Google Scholar
Lijavetzky, D., Carbonero, P. and Vicente-Carbajosa, J. (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evolutionary Biology 3, 17–27.Google Scholar
Lohmer, S., Maddaloni, M., Motto, M., Di Fonzo, N., Hartings, H., Salamini, F. and Thompson, R.D. (1991) The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO Journal 10, 617–624.Google Scholar
Lotan, T., Ohto, M., Yee, K.M., West, M.A., Lo, R., Kwong, R.W., Yamagishi, K., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93, 1195–1205.CrossRefGoogle ScholarPubMed
Luerssen, H., Kirik, V., Herrmann, P. and Misera, S. (1998) FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant Journal 15, 755–764.Google Scholar
Marzabal, P., Busk, P.K., Ludevid, M.D. and Torrent, M. (1998) The bifactorial endosperm box of γ-zein gene: characterisation and function of the Pb3 and GZM cis-acting elements. Plant Journal 16, 41–52.Google Scholar
Marzabal, P., Gas, E., Fontanet, P., Vicente-Carbajosa, J., Torrent, M. and Ludevid, M.D. (2008) The maize Dof protein PBF activates transcription of γ-zein during maize seed development. Plant Molecular Biology 67, 441–454.Google Scholar
McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I.K. (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66, 895–905.Google Scholar
Mena, M., Vicente-Carbajosa, J., Schmidt, R.J. and 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 Journal 16, 53–62.CrossRefGoogle ScholarPubMed
Mena, M., Cejudo, F.J., Isabel-Lamoneda, I. and Carbonero, P. (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiology 130, 111–119.CrossRefGoogle ScholarPubMed
Moreno-Risueno, M.A., Gonzalez, N., Diaz, I., Parcy, F., Carbonero, P. and Vicente-Carbajosa, J. (2008) FUSCA3 from barley unveils a common transcriptional regulation of seed-specific genes between cereals and Arabidopsis. Plant Journal 53, 882–894.Google Scholar
Onate, L., Vicente-Carbajosa, J., Lara, P., Diaz, I. and Carbonero, P. (1999) Barley BLZ2, a seed-specific bZIP protein that interacts with BLZ1 in vivo and activates transcription from the GCN4-like motif of B-hordein promoters in barley endosperm. Journal of Biological Chemistry 274, 9175–9182.Google Scholar
Onodera, Y., Suzuki, A., Wu, C.Y., Washida, H. and Takaiwa, F. (2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. Journal of Biological Chemistry 276, 14139–14152.Google Scholar
Parcy, F. and Giraudat, J. (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant Journal 11, 693–702.Google Scholar
Parcy, F., Valon, C., Raynal, M., Gaubier-Comella, P., Delseny, M. and Giraudat, J. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6, 1567–1582.Google ScholarPubMed
Parcy, F., Valon, C., Kohara, A., Misera, S. and Giraudat, J. (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9, 1265–1277.Google Scholar
Pirovano, L., Lanzini, S., Hartings, H., Lazzaroni, N., Rossi, V., Joshi, R., Thompson, R.D., Salamini, F. and Motto, M. (1994) Structural and functional analysis of an Opaque-2-related gene from sorghum. Plant Molecular Biology 24, 515–523.CrossRefGoogle ScholarPubMed
Qu le, Q., Xing, Y.P., Liu, W.X., Xu, X.P. and Song, Y.R. (2008) Expression pattern and activity of six glutelin gene promoters in transgenic rice. Journal of Experimental Botany 59, 2417–2424.Google Scholar
Raz, V., Bergervoet, J.H. and Koornneef, M. (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128, 243–252.Google Scholar
Schmidt, R.J., Ketudat, M., Aukerman, M.J. and Hoschek, G. (1992) Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4, 689–700.Google Scholar
Skirycz, A., Reichelt, M., Burow, M., Birkemeyer, C., Rolcik, J., Kopka, J., Zanor, M.I., Gershenzon, J., Strnad, M., Szopa, J., Mueller-Roeber, B. and Witt, I. (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant Journal 47, 10–24.CrossRefGoogle ScholarPubMed
Stone, S.L., Kwong, L.W., Yee, K.M., Pelletier, J., Lepiniec, L., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proceedings of the National Academy of Sciences, USA 98, 11806–11811.Google Scholar
Suzuki, A., Wu, C.Y., Washida, H. and Takaiwa, F. (1998) Rice MYB protein OSMYB5 specifically binds to the AACA motif conserved among promoters of genes for storage protein glutelin. Plant and Cell Physiology 39, 555–559.Google Scholar
Suzuki, M., Kao, C.Y., Cocciolone, S. and McCarty, D.R. (2001) Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant Journal 28, 409–418.CrossRefGoogle ScholarPubMed
Suzuki, M., Ketterling, M.G., Li, Q.B. and McCarty, D.R. (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiology 132, 1664–1677.Google Scholar
Takaiwa, F., Yamanouchi, U., Yoshihara, T., Washida, H., Tanabe, F., Kato, A. and Yamada, K. (1996) Characterization of common cis-regulatory elements responsible for the endosperm-specific expression of members of the rice glutelin multigene family. Plant Molecular Biology 30, 1207–1221.Google Scholar
To, A., Valon, C., Savino, G., Guilleminot, J., Devic, M., Giraudat, J. and Parcy, F. (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18, 1642–1651.Google Scholar
Tsuchiya, Y., Nambara, E., Naito, S. and McCourt, P. (2004) The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis. Plant Journal 37, 73–81.CrossRefGoogle ScholarPubMed
Vettore, A.L., Yunes, J.A., Cord Neto, G., da Silva, M.J., Arruda, P. and Leite, A. (1998) The molecular and functional characterization of an Opaque2 homologue gene from Coix and a new classification of plant bZIP proteins. Plant Molecular Biology 36, 249–263.Google Scholar
Vicente-Carbajosa, J. and Carbonero, P. (2005) Seed maturation: developing an intrusive phase to accomplish a quiescent state. International Journal of Developmental Biology 49, 645–651.CrossRefGoogle ScholarPubMed
Vicente-Carbajosa, J., Moose, S.P., Parsons, R.L. and Schmidt, R.J. (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proceedings of the National Academy of Sciences, USA 94, 7685–7690.Google Scholar
Vicente-Carbajosa, J., Onate, L., Lara, P., Diaz, I. and Carbonero, P. (1998) Barley BLZ1: a bZIP transcriptional activator that interacts with endosperm-specific gene promoters. Plant Journal 13, 629–640.Google Scholar
Vicient, C.M., Bies-Etheve, N. and Delseny, M. (2000) Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L. Journal of Experimental Botany 51, 995–1003.Google Scholar
Washida, H., Wu, C.Y., Suzuki, A., Yamanouchi, U., Akihama, T., Harada, K. and Takaiwa, F. (1999) Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. Plant Molecular Biology 40, 1–12.CrossRefGoogle ScholarPubMed
Wobus, U. and Weber, H. (1999) Seed maturation: genetic programmes and control signals. Current Opinion in Plant Biology 2, 33–38.CrossRefGoogle ScholarPubMed
Wu, C.Y., Suzuki, A., Washida, H. and Takaiwa, F. (1998) The GCN4 motif in a rice glutelin gene is essential for endosperm-specific gene expression and is activated by Opaque-2 in transgenic rice plants. Plant Journal 14, 673–683.Google Scholar
Wu, C., Washida, H., Onodera, Y., Harada, K. and Takaiwa, F. (2000) Quantitative nature of the Prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant Journal 23, 415–421.Google Scholar
Yamamoto, M.P., Onodera, Y., Touno, S.M. and Takaiwa, F. (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiology 141, 1694–1707.CrossRefGoogle ScholarPubMed
Yanagisawa, S. (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant Journal 21, 281–288.CrossRefGoogle ScholarPubMed
Yanagisawa, S. (2002) The Dof family of plant transcription factors. Trends in Plant Science 7, 555–560.Google Scholar
Yanagisawa, S. (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant and Cell Physiology 45, 386–391.Google Scholar
Yoshihara, T., Washida, H. and Takaiwa, F. (1996) A 45-bp proximal region containing AACA and GCN4 motif is sufficient to confer endosperm-specific expression of the rice storage protein glutelin gene, GluA-3. FEBS Letters 383, 213–218.CrossRefGoogle ScholarPubMed