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. 1991 Jun;10(6):1469–1479. doi: 10.1002/j.1460-2075.1991.tb07667.x

Positive and negative cis-acting DNA domains are required for spatial and temporal regulation of gene expression by a seed storage protein promoter.

M M Bustos 1, D Begum 1, F A Kalkan 1, M J Battraw 1, T C Hall 1
PMCID: PMC452810  PMID: 2026144

Abstract

Mutations affecting spatial and temporal regulation of a beta-phaseolin gene encoding the major storage protein of bean (Phaseolus vulgaris) were analyzed by stable and transient transformation approaches. The results substantiate the value of transient assays for rapid determination of the functionality of cis-acting sequences and the importance of stable transformation to identify tissue-specific determinants. Spatial information is specified primarily by two upstream activating sequences (UAS). UAS1 (-295 to -109) was sufficient for seed-specific expression from both homologous and heterologous (CaMV 35S) promoters. In situ localization of GUS expression in tobacco embryos demonstrated that UAS1 activity was restricted to the cotyledons and shoot meristem. A second positive domain, UAS2 (-468 to -391), extended gene activity to the hypocotyl. Temporal control of GUS expression was found to involve two negative regulatory sequences, NRS1 (-391 to -295) and NRS2 (-518 to -418), as well as the positive domain UAS1. The deletion of either negative element caused premature onset of GUS expression. These findings indicate combinatorial interactions between multiple sequence motifs specifying spatial information, and provide the first example of the involvement of negative elements in the temporal control of gene expression in higher plants.

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Selected References

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  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Allen R. D., Bernier F., Lessard P. A., Beachy R. N. Nuclear factors interact with a soybean beta-conglycinin enhancer. Plant Cell. 1989 Jun;1(6):623–631. doi: 10.1105/tpc.1.6.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barker S. J., Harada J. J., Goldberg R. B. Cellular localization of soybean storage protein mRNA in transformed tobacco seeds. Proc Natl Acad Sci U S A. 1988 Jan;85(2):458–462. doi: 10.1073/pnas.85.2.458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benfey P. N., Ren L., Chua N. H. The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J. 1989 Aug;8(8):2195–2202. doi: 10.1002/j.1460-2075.1989.tb08342.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benfey P. N., Ren L., Chua N. H. Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J. 1990 Jun;9(6):1677–1684. doi: 10.1002/j.1460-2075.1990.tb08291.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bevan M. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 1984 Nov 26;12(22):8711–8721. doi: 10.1093/nar/12.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  8. Bustos M. M., Guiltinan M. J., Jordano J., Begum D., Kalkan F. A., Hall T. C. Regulation of beta-glucuronidase expression in transgenic tobacco plants by an A/T-rich, cis-acting sequence found upstream of a French bean beta-phaseolin gene. Plant Cell. 1989 Sep;1(9):839–853. doi: 10.1105/tpc.1.9.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chappell J., Chrispeels M. J. Transcriptional and Posttranscriptional Control of Phaseolin and Phytohemagglutinin Gene Expression in Developing Cotyledons of Phaseolus vulgaris. Plant Physiol. 1986 May;81(1):50–54. doi: 10.1104/pp.81.1.50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chen Z. L., Pan N. S., Beachy R. N. A DNA sequence element that confers seed-specific enhancement to a constitutive promoter. EMBO J. 1988 Feb;7(2):297–302. doi: 10.1002/j.1460-2075.1988.tb02812.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dangl J. L., Hauffe K. D., Lipphardt S., Hahlbrock K., Scheel D. Parsley protoplasts retain differential responsiveness to u.v. light and fungal elicitor. EMBO J. 1987 Sep;6(9):2551–2556. doi: 10.1002/j.1460-2075.1987.tb02543.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davidson E. H. Lineage-specific gene expression and the regulative capacities of the sea urchin embryo: a proposed mechanism. Development. 1989 Mar;105(3):421–445. doi: 10.1242/dev.105.3.421. [DOI] [PubMed] [Google Scholar]
  13. Ellis J. G., Llewellyn D. J., Dennis E. S., Peacock W. J. Maize Adh-1 promoter sequences control anaerobic regulation: addition of upstream promoter elements from constitutive genes is necessary for expression in tobacco. EMBO J. 1987 Jan;6(1):11–16. doi: 10.1002/j.1460-2075.1987.tb04711.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fang R. X., Nagy F., Sivasubramaniam S., Chua N. H. Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell. 1989 Jan;1(1):141–150. doi: 10.1105/tpc.1.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Frearson E. M., Power J. B., Cocking E. C. The isolation, culture and regeneration of Petunia leaf protoplasts. Dev Biol. 1973 Jul;33(1):130–137. doi: 10.1016/0012-1606(73)90169-3. [DOI] [PubMed] [Google Scholar]
  16. Galau G. A., Dure L., 3rd Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by reciprocal heterologous complementary deoxyribonucleic acid--messenger ribonucleic acid hybridization. Biochemistry. 1981 Jul 7;20(14):4169–4178. doi: 10.1021/bi00517a034. [DOI] [PubMed] [Google Scholar]
  17. Goldberg R. B., Barker S. J., Perez-Grau L. Regulation of gene expression during plant embryogenesis. Cell. 1989 Jan 27;56(2):149–160. doi: 10.1016/0092-8674(89)90888-x. [DOI] [PubMed] [Google Scholar]
  18. Goldberg R. B., Hoschek G., Ditta G. S., Breidenbach R. W. Developmental regulation of cloned superabundant embryo mRNAs in soybean. Dev Biol. 1981 Apr 30;83(2):218–231. doi: 10.1016/0012-1606(81)90468-1. [DOI] [PubMed] [Google Scholar]
  19. Goldberg R. B., Hoschek G., Tam S. H., Ditta G. S., Breidenbach R. W. Abundance, diversity, and regulation of mRNA sequence sets in soybean embryogenesis. Dev Biol. 1981 Apr 30;83(2):201–217. doi: 10.1016/0012-1606(81)90467-x. [DOI] [PubMed] [Google Scholar]
  20. Greenwood J. S., Chrispeels M. J. Correct targeting of the bean storage protein phaseolin in the seeds of transformed tobacco. Plant Physiol. 1985 Sep;79(1):65–71. doi: 10.1104/pp.79.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guerche P., Tire C., De Sa F. G., De Clercq A., Van Montagu M., Krebbers E. Differential Expression of the Arabidopsis 2S Albumin Genes and the Effect of Increasing Gene Family Size. Plant Cell. 1990 May;2(5):469–478. doi: 10.1105/tpc.2.5.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hagerman P. J. Sequence-directed curvature of DNA. Annu Rev Biochem. 1990;59:755–781. doi: 10.1146/annurev.bi.59.070190.003543. [DOI] [PubMed] [Google Scholar]
  23. Hoffman L. M., Donaldson D. D. Characterization of two Phaseolus vulgaris phytohemagglutinin genes closely linked on the chromosome. EMBO J. 1985 Apr;4(4):883–889. doi: 10.1002/j.1460-2075.1985.tb03714.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hughes D. W., Galau G. A. Temporally modular gene expression during cotyledon development. Genes Dev. 1989 Mar;3(3):358–369. doi: 10.1101/gad.3.3.358. [DOI] [PubMed] [Google Scholar]
  25. Jofuku K. D., Goldberg R. B. Kunitz trypsin inhibitor genes are differentially expressed during the soybean life cycle and in transformed tobacco plants. Plant Cell. 1989 Nov;1(11):1079–1093. doi: 10.1105/tpc.1.11.1079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jones H., Ooms G., Jones M. G. Transient gene expression in electroporated Solanum protoplasts. Plant Mol Biol. 1989 Nov;13(5):503–511. doi: 10.1007/BF00027310. [DOI] [PubMed] [Google Scholar]
  27. Lam E., Benfey P. N., Gilmartin P. M., Fang R. X., Chua N. H. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7890–7894. doi: 10.1073/pnas.86.20.7890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lipphardt S., Brettschneider R., Kreuzaler F., Schell J., Dangl J. L. UV-inducible transient expression in parsley protoplasts identifies regulatory cis-elements of a chimeric Antirrhinum majus chalcone synthase gene. EMBO J. 1988 Dec 20;7(13):4027–4033. doi: 10.1002/j.1460-2075.1988.tb03296.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Logemann J., Lipphardt S., Lörz H., Häuser I., Willmitzer L., Schell J. 5' upstream sequences from the wun1 gene are responsible for gene activation by wounding in transgenic plants. Plant Cell. 1989 Jan;1(1):151–158. doi: 10.1105/tpc.1.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mutschler M. A., Bliss F. A., Hall T. C. Variation in the Accumulation of Seed Storage Protein Among Genotypes of Phaseolus vulgaris (L.). Plant Physiol. 1980 Apr;65(4):627–630. doi: 10.1104/pp.65.4.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Odell J. T., Nagy F., Chua N. H. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. 1985 Feb 28-Mar 6Nature. 313(6005):810–812. doi: 10.1038/313810a0. [DOI] [PubMed] [Google Scholar]
  32. Ow D. W., Jacobs J. D., Howell S. H. Functional regions of the cauliflower mosaic virus 35S RNA promoter determined by use of the firefly luciferase gene as a reporter of promoter activity. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4870–4874. doi: 10.1073/pnas.84.14.4870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Perez-Grau L., Goldberg R. B. Soybean Seed Protein Genes Are Regulated Spatially during Embryogenesis. Plant Cell. 1989 Nov;1(11):1095–1109. doi: 10.1105/tpc.1.11.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schernthaner J. P., Matzke M. A., Matzke A. J. Endosperm-specific activity of a zein gene promoter in transgenic tobacco plants. EMBO J. 1988 May;7(5):1249–1255. doi: 10.1002/j.1460-2075.1988.tb02938.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sengupta-Gopalan C., Reichert N. A., Barker R. F., Hall T. C., Kemp J. D. Developmentally regulated expression of the bean beta-phaseolin gene in tobacco seed. Proc Natl Acad Sci U S A. 1985 May;82(10):3320–3324. doi: 10.1073/pnas.82.10.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shuttuck-Eidens D. M., Beachy R. N. Degradation of beta-Conglycinin in Early Stages of Soybean Embryogenesis. Plant Physiol. 1985 Aug;78(4):895–898. doi: 10.1104/pp.78.4.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. St Schell J. Transgenic plants as tools to study the molecular organization of plant genes. Science. 1987 Sep 4;237(4819):1176–1183. doi: 10.1126/science.237.4819.1176. [DOI] [PubMed] [Google Scholar]
  38. Stief A., Winter D. M., Strätling W. H., Sippel A. E. A nuclear DNA attachment element mediates elevated and position-independent gene activity. Nature. 1989 Sep 28;341(6240):343–345. doi: 10.1038/341343a0. [DOI] [PubMed] [Google Scholar]
  39. Sun S. M., Mutschler M. A., Bliss F. A., Hall T. C. Protein Synthesis and Accumulation in Bean Cotyledons during Growth. Plant Physiol. 1978 Jun;61(6):918–923. doi: 10.1104/pp.61.6.918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Walker J. C., Howard E. A., Dennis E. S., Peacock W. J. DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6624–6628. doi: 10.1073/pnas.84.19.6624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamamoto K. R. Steroid receptor regulated transcription of specific genes and gene networks. Annu Rev Genet. 1985;19:209–252. doi: 10.1146/annurev.ge.19.120185.001233. [DOI] [PubMed] [Google Scholar]

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