Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Intragenic Control of Expression of a Rice MADS Box Gene OsMADS1

  • Jeon, Jong-Seong (Plant Metabolism Research Center and Graduate School of Biotechnology, Kyung Hee University) ;
  • Lee, Sichul (Department of Life Science and National Research Laboratory of Plant Functional Genomics, Pohang University of Science and Technology) ;
  • An, Gynheung (Department of Life Science and National Research Laboratory of Plant Functional Genomics, Pohang University of Science and Technology)
  • Received : 2008.06.02
  • Accepted : 2008.07.29
  • Published : 2008.11.30
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Abstract

OsMADS1 is a rice MADS box gene necessary for floral development. To identify the key cis-regulatory regions for its expression, we utilized transgenic rice plants expressing GUS fusion constructs. Histochemical analysis revealed that the 5.7-kb OsMADS1 intragenic sequences, encompassing exon 1, intron 1, and a part of exon 2, together with the 1.9-kb 5' upstream promoter region, are required for the GUS expression pattern that coincides with flower-preferential expression of OsMADS1. In contrast, the 5' upstream promoter sequence lacking this intragenic region caused ectopic expression of the reporter gene in both vegetative and reproductive tissues. Notably, incorporation of the intragenic region into the CaMV35S promoter directed the GUS expression pattern similar to that of the endogenous spatial expression of OsMADS1 in flowers. In addition, our transient gene expression assay revealed that the large first intron following the CaMV35S minimal promoter enhances flower-preferential expression of GUS. These results suggest that the OsMADS1 intragenic sequence, largely intron 1, contains a key regulatory region(s) essential for expression.

Keywords

Acknowledgement

Supported by : Crop Functional Genomic Center, Rural Development Administration, Korea Science and Engineering Foundation

References

  1. Agrawal, G.K., Abe, K., Yamazaki, M., Miyao, A., and Hirochika, H. (2005). Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-offunction mutants of the OsMADS1 gene. Plant Mol. Biol. 59, 125-135 https://doi.org/10.1007/s11103-005-2161-y
  2. Barrero, J.M., Gonzalez-Bayon, R., del Pozo, J.C., Ponce, M.R., and Micol, J.L. (2007). INCURVATA2 encodes the catalytic subunit of DNA Polymerase alpha and interacts with genes involved in chromatin-mediated cellular memory in Arabidopsis thaliana. Plant Cell 19, 2822-2838 https://doi.org/10.1105/tpc.107.054130
  3. Bastow, R., Mylne, J.S., Lister, C., Lippman, Z., Martienssen, R.A., and Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164-167 https://doi.org/10.1038/nature02269
  4. Bhattacharyya, N., and Banerjee, D. (1999). Transcriptional regulatory sequences within the first intron of the chicken apolipoproteinAI(apoAI) gene. Gene 234, 371-380 https://doi.org/10.1016/S0378-1119(99)00183-3
  5. Busch, M.A., Bomblies, K., and Weigel, D. (1999). Activation of a floral homeotic gene in Arabidopsis. Science 285, 585-587 https://doi.org/10.1126/science.285.5427.585
  6. Callis, J., Fromm, M., and Walbot, V. (1987) Introns increase gene expression in cultured maize cells. Genes Dev. 1, 1183-1200 https://doi.org/10.1101/gad.1.10.1183
  7. Chen, Z.X., Wu, J.G., Ding, W.N., Chen, H.M., Wu, P., and Shi, C.H. (2006). Morphogenesis and molecular basis on naked seed rice, a novel homeotic mutation of OsMADS1 regulating transcript level of AP3 homologue in rice. Planta 223, 882-890 https://doi.org/10.1007/s00425-005-0141-8
  8. Chung, Y.-Y., Kim, S.-R., Finkel, D., Yanofsky, M., and An, G. (1994). Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Mol. Biol. 26, 657-665 https://doi.org/10.1007/BF00013751
  9. Deyholos, M.K., and Sieburth, L.E. (2000). Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12, 1799-1810 https://doi.org/10.1105/tpc.12.10.1799
  10. Fu, H., Kim, S.Y., and Park, W.D. (1995). High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5' and 3' flanking sequences and leader intron. Plant Cell 7, 1387-1394 https://doi.org/10.1105/tpc.7.9.1387
  11. Guo, H., Duong, H., Ma, N., and Lin, C. (1999). The Arabidopsis blue light receptor cryptochrome 2 is a nuclear protein regulated by a blue light-dependent post-transcriptional mechanism. Plant J. 19, 279-287 https://doi.org/10.1046/j.1365-313X.1999.00525.x
  12. Helliwell, C.A., Webster, C.I., and Gray, J.C. (1997). Light-regulated expression of the pea plastocyanin gene is mediated by elements within the transcribed region of the gene. Plant J. 12, 499-506 https://doi.org/10.1046/j.1365-313X.1997.00499.x
  13. Huang, F., and Gallo, V. (1997). Gene structure of the rat kainate receptor subunit KA2 and characterization of an intronic negative regulatory region. J. Biol. Chem. 272, 8618-8627 https://doi.org/10.1074/jbc.272.13.8618
  14. Jeon, J.-S., Chung, Y.-Y., Lee, S., Yi, G.-H., Oh, B.-G., and An, G. (1999). Isolation and characterization of an anther-specific gene, RA8, from rice (Oryza sativa L.). Plant Mol. Biol. 39, 35-44 https://doi.org/10.1023/A:1006157603096
  15. Jeon, J.-S., Jang, S., Lee, S., Nam, J., Kim, C., Lee, S.-H., Chung, Y.-Y., Kim, S.-R., Lee, Y.-H., Cho, Y.-G., et al. (2000a). leafy hull sterile 1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12, 871-884 https://doi.org/10.1105/tpc.12.6.871
  16. Jeon, J.-S., Lee, S., Jung, K.-H., Jun, S.-H., Kim, C., and An, G. (2000b). Tissue-preferential expression of a rice alpha-tubulin gene, OsTubA1, mediated by the first intron. Plant Physiol. 123, 1005-1014 https://doi.org/10.1104/pp.123.3.1005
  17. Jeong, D.H., An, S., Kang, H.G., Moon, S., Han, J.J., Park, S., Lee, H.S., An, K., and An, G. (2002). T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol. 130, 1636-1644 https://doi.org/10.1104/pp.014357
  18. Jeong, Y.M., Mun, J.-H., Lee, I., Woo, J.C., Hong, C.B., and Kim, S.-G. (2006). Distinct roles of the first introns on the expression of Arabidopsis profilin gene family members. Plant Physiol. 140, 196-209
  19. Kamiya, N., Nagasaki, H., Morikami, A., Sato, Y., and Matsuoka, M. (2003). Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J. 35, 429-441 https://doi.org/10.1046/j.1365-313X.2003.01816.x
  20. Khush, G.S., and Librojo, A.L. (1985). Naked seed rice (NSR) is allelic to op and Ihs. Rice Genet. News. 2, 71
  21. Kinoshita, T., Hidano, Y., and Takahashi, M. (1976). A mutant 'long hull sterile' found out in the rice variety, 'Sorachi' - Genetical studies on rice plant, LXVII - , Mem. Fac. Agr. Hokkaido Univ. 10, 247-268
  22. Lee, S., Jeon, J.-S., Jung, K.-H., and An, G. (1999). Binary vectors for efficient transformation of rice. J. Plant Biol. 42, 310-316 https://doi.org/10.1007/BF03030346
  23. Lee, S., Jeon, J.S., An, K., Moon, Y.H., Lee, S., Chung, Y.Y., and An, G. (2003). Alteration of floral organ identity in rice through ectopic expression of OsMADS1S. Planta 217, 904-911 https://doi.org/10.1007/s00425-003-1066-8
  24. Lim, H.M., Cho, J.I., Lee, S., Cho, M.H., Bhoo, S.H., An, G., Hahn, T.R., and Jeon, J.S. (2007). Identification of a 20-bp regulatory element of the Arabidopsis Arabidopsis propho sphate:fructose-6-phosphate 1-phosphotransferase ${\alpha}2$ gene that is essential for expression. Plant Cell Rep. 26, 683-692 https://doi.org/10.1007/s00299-006-0272-9
  25. Lohmann, J.U., Hong, R., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793-803 https://doi.org/10.1016/S0092-8674(01)00384-1
  26. Luehrsen, K.R., and Walbot, V. (1991). Intron enhancement of gene expression and splicing efficiency of introns in maize cells. Mol. Gen. Genet. 225, 81-93
  27. Luehrsen, K.R., and Walbot, V. (1994). Addition of A- and U-rich sequence increases the splicing efficiency of a deleted form of a maize intron. Plant Mol. Biol. 24, 449-463 https://doi.org/10.1007/BF00024113
  28. Marshall, J.S., Stubbs, J.D., Chitty, J.A., Surin, B., and Taylor, W.C. (1997). Expression of the $C_4$ Me 1 gene from Flaveria bidentis requires an interaction between 5' and 3' sequences. Plant Cell 9, 1515-1525 https://doi.org/10.1105/tpc.9.9.1515
  29. Maas, C., Laufs, J., Grant, S., Korfhage, C., and Werr, W. (1991). The combination of a novel stimulatory element in the first exon of the maize Shrunken-1 gene with the following intron 1 enhances reporter gene expression up to 1000-fold. Plant Mol. Biol. 16, 199-207 https://doi.org/10.1007/BF00020552
  30. Mascarenhas, D., Mettler, I.J., Pierce, D.A., and Lowe, H.W. (1990). Intron-mediated enhancement of heterologous gene expression in maize. Plant Mol. Biol. 15, 913-920 https://doi.org/10.1007/BF00039430
  31. McElroy, D., Zhang, W., Cao, J., and Wu, R. (1990). Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2, 163-171 https://doi.org/10.1105/tpc.2.2.163
  32. Molkentin, J.D., Li, L., and Olson, E.N. (1996). Phosphorylation of the MADS-box transcription factor MEF2C enhances its DNA binding activity. J. Biol. Chem. 271, 17199-17204 https://doi.org/10.1074/jbc.271.29.17199
  33. Moon, Y.H., Jung, J.Y., Kang, H.G., and An, G. (1999). Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol. Biol. 40, 167-177 https://doi.org/10.1023/A:1026429922616
  34. Ng, M., and Yanofsky, M. (2000). Three ways to learn the ABCs. Curr. Opin. Plant Biol. 3, 47-52 https://doi.org/10.1016/S1369-5266(99)00036-9
  35. Nobuyoshi, M., Lin, X.-H., Takimoto, Y., Deuel, T.F., and Wang, Z.-Y. (1997). Transcription regulation of the PDGF A-chain gene by first intron elements. Biochem. Biophy. Res. Commun. 230, 569-572 https://doi.org/10.1006/bbrc.1996.6011
  36. Prasad, K., Sriram, P., Kumar, C.S., Kushalappa, K., and Vijayraghavan, U. (2001). Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev. Genes Evol. 211, 281-290 https://doi.org/10.1007/s004270100153
  37. Prasad, K., Parameswaran, S., and Vijayraghavan, U. (2005). OsMADS 1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J. 43, 915-928 https://doi.org/10.1111/j.1365-313X.2005.02504.x
  38. Rijpkema, A.S., Gerats, T., and Vandenbussche, M. (2007). Evolutionary complexity of MADS complexes. Curr. Opin. Plant Biol. 10, 32-38 https://doi.org/10.1016/j.pbi.2006.11.010
  39. Rose, A.B., and Last, R.L. (1997). Introns act post-transcriptionally to increase expression of the Arabidopsis thaliana tryptophan pathway gene PAT1. Plant J. 11, 455-464 https://doi.org/10.1046/j.1365-313X.1997.11030455.x
  40. Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T., and Goodrich, J. (2006). Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638-4649 https://doi.org/10.1038/sj.emboj.7601311
  41. Sheldon, C.C., Conn, A.B., Dennis, E.S., and Peacock, W.J. (2002). Different regulatory regions are required for the vernalization-induced repression of FLOWERING LCOUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527-2537 https://doi.org/10.1105/tpc.004564
  42. Sheldon, C.C., Finnegan, E.J., Dennis, E.S., and Peacock, W.J. (2006). Quantitative effects of vernalization on FLC and SOC1 expression. Plant J. 45, 871-883 https://doi.org/10.1111/j.1365-313X.2006.02652.x
  43. Sieburth, L.E., and Meyerowitz, E.M. (1997). Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9, 355-365 https://doi.org/10.1105/tpc.9.3.355
  44. Sivitz, A.B., Reinders, A., Johnson, M.E., Krentz, A.D., Grof, C.P., Perroux, J.M., and Ward, J.M. (2007). Arabidopsis sucrose transporter. High-affinity transport activity, intragenic control of expression, and early flowering mutant phenotype. Plant Physiol. 143, 188-198 https://doi.org/10.1104/pp.106.089003
  45. Sung, S., He, Y., Eshoo, T.W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S.E., and Amasino, R.M. (2006). Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706-710 https://doi.org/10.1038/ng1795
  46. Vasil, V., Clancy, M., Ferl, R.J., Vasil, I., and Hannah, L.C. (1989). Increased gene expression by the first intron of maize Shrunken-1 locus in grass species. Plant Physiol. 91, 1575-1579 https://doi.org/10.1104/pp.91.4.1575
  47. Weigel, D., and Meyerowitz, E.M. (1994). The ABCs of floral homeotic genes. Cell 78, 203-209 https://doi.org/10.1016/0092-8674(94)90291-7
  48. Wight, P.A., and Dobretsova, A. (1997). The first intron of the myelin proteolipid protein gene confers cell type-specific expression by a transcriptional repression mechanism in non-expressing cell types. Gene 201, 111-117 https://doi.org/10.1016/S0378-1119(97)00435-6
  49. Xiao, H., Wang, Y., Liu, D., Wang, W., Li, X., Zhao, X., Xu, J., Zhai, W., and Zhu, L. (2003). Functional analysis of the rice AP3 homologue OsMADS1S by RNA interference. Plant Mol. Biol. 52, 957-966 https://doi.org/10.1023/A:1025401611354