Abstract
Zeins are seed storage proteins that form accretions called protein bodies in the rough endoplasmic reticulum of maize endosperm cells. Four types of zeins, alpha, beta, gamma, and delta, aggregate in a distinctive spatial pattern within the protein body. We created transgenic tobacco plants expressing alpha-zein, gamma-zein, or both to examine the interactions between these proteins leading to the formation of protein bodies in the endosperm. Whereas gamma-zein accumulated in seeds of these plants, stable accumulation of alpha-zein required simultaneous synthesis of gamma-zein. The zein proteins formed accretions in the endoplasmic reticulum similar to those in maize endosperm. Protein bodies were also found in protein storage vacuoles. The accumulation of both types of zeins peaked early in development and declined during maturation. Even in the presence of gamma-zein, there was a turnover of alpha-zein, suggesting that the interaction between the two proteins might be transitory. We suggest that gamma-zein plays an important role in protein body formation and demonstrate the utility of tobacco for studying interactions between different zeins.
Full Text
The Full Text of this article is available as a PDF (3.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Argos P., Pedersen K., Marks M. D., Larkins B. A. A structural model for maize zein proteins. J Biol Chem. 1982 Sep 10;257(17):9984–9990. [PubMed] [Google Scholar]
- Bagga S., Adams H., Kemp J. D., Sengupta-Gopalan C. Accumulation of 15-Kilodalton Zein in Novel Protein Bodies in Transgenic Tobacco. Plant Physiol. 1995 Jan;107(1):13–23. doi: 10.1104/pp.107.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Boston R. S., Fontes E. B., Shank B. B., Wrobel R. L. Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants. Plant Cell. 1991 May;3(5):497–505. doi: 10.1105/tpc.3.5.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coleman C. E., Lopes M. A., Gillikin J. W., Boston R. S., Larkins B. A. A defective signal peptide in the maize high-lysine mutant floury 2. Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6828–6831. doi: 10.1073/pnas.92.15.6828. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dannenhoffer J. M., Bostwick D. E., Or E., Larkins B. A. opaque-15, a maize mutation with properties of a defective opaque-2 modifier. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1931–1935. doi: 10.1073/pnas.92.6.1931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontes E. B., Shank B. B., Wrobel R. L., Moose S. P., OBrian G. R., Wurtzel E. T., Boston R. S. Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell. 1991 May;3(5):483–496. doi: 10.1105/tpc.3.5.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geli M. I., Torrent M., Ludevid D. Two Structural Domains Mediate Two Sequential Events in [gamma]-Zein Targeting: Protein Endoplasmic Reticulum Retention and Protein Body Formation. Plant Cell. 1994 Dec;6(12):1911–1922. doi: 10.1105/tpc.6.12.1911. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman E. M., Baumgartner B., Chrispeels M. J. Uptake and apparent digestion of cytoplasmic organelles by protein bodies (protein storage vacuoles) in mung bean cotyledons. Eur J Cell Biol. 1981 Jun;24(2):226–235. [PubMed] [Google Scholar]
- Kodrzycki R., Boston R. S., Larkins B. A. The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell. 1989 Jan;1(1):105–114. doi: 10.1105/tpc.1.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lending C. R., Larkins B. A. Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell. 1989 Oct;1(10):1011–1023. doi: 10.1105/tpc.1.10.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levanony H., Rubin R., Altschuler Y., Galili G. Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol. 1992 Dec;119(5):1117–1128. doi: 10.1083/jcb.119.5.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li C. P., Larkins B. A. Expression of protein disulfide isomerase is elevated in the endosperm of the maize floury-2 mutant. Plant Mol Biol. 1996 Mar;30(5):873–882. doi: 10.1007/BF00020800. [DOI] [PubMed] [Google Scholar]
- Li X., Wu Y., Zhang D. Z., Gillikin J. W., Boston R. S., Franceschi V. R., Okita T. W. Rice prolamine protein body biogenesis: a BiP-mediated process. Science. 1993 Nov 12;262(5136):1054–1056. doi: 10.1126/science.8235623. [DOI] [PubMed] [Google Scholar]
- Lopes M. A., Takasaki K., Bostwick D. E., Helentjaris T., Larkins B. A. Identification of two opaque2 modifier loci in quality protein maize. Mol Gen Genet. 1995 Jun 10;247(5):603–613. doi: 10.1007/BF00290352. [DOI] [PubMed] [Google Scholar]
- Marocco A., Santucci A., Cerioli S., Motto M., Di Fonzo N., Thompson R., Salamini F. Three high-lysine mutations control the level of ATP-binding HSP70-like proteins in the maize endosperm. Plant Cell. 1991 May;3(5):507–515. doi: 10.1105/tpc.3.5.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCreery T., Helentjaris T. Hybridization of digoxigenin-labeled probes to Southern blots and detection by chemiluminescence. Methods Mol Biol. 1994;28:107–112. doi: 10.1385/0-89603-254-x:107. [DOI] [PubMed] [Google Scholar]
- McCreery T., Helentjaris T. Production of hybridization probes by the PCR utilizing digoxigenin-modified nucleotides. Methods Mol Biol. 1994;28:67–71. doi: 10.1385/0-89603-254-x:67. [DOI] [PubMed] [Google Scholar]
- Ohtani T., Galili G., Wallace J. C., Thompson G. A., Larkins B. A. Normal and lysine-containing zeins are unstable in transgenic tobacco seeds. Plant Mol Biol. 1991 Jan;16(1):117–128. doi: 10.1007/BF00017922. [DOI] [PubMed] [Google Scholar]
- Prat S., Cortadas J., Puigdomènech P., Palau J. Nucleic acid (cDNA) and amino acid sequences of the maize endosperm protein glutelin-2. Nucleic Acids Res. 1985 Mar 11;13(5):1493–1504. doi: 10.1093/nar/13.5.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rabanal F., Ludevid M. D., Pons M., Giralt E. CD of proline-rich polypeptides: application to the study of the repetitive domain of maize glutelin-2. Biopolymers. 1993 Jul;33(7):1019–1028. doi: 10.1002/bip.360330704. [DOI] [PubMed] [Google Scholar]
- Rechinger K. B., Simpson D. J., Svendsen I., Cameron-Mills V. A role for gamma 3 hordein in the transport and targeting of prolamin polypeptides to the vacuole of developing barley endosperm. Plant J. 1993 Nov;4(5):841–853. doi: 10.1046/j.1365-313x.1993.04050841.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Shewry P. R., Napier J. A., Tatham A. S. Seed storage proteins: structures and biosynthesis. Plant Cell. 1995 Jul;7(7):945–956. doi: 10.1105/tpc.7.7.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takaiwa F., Oono K., Kato A. Analysis of the 5' flanking region responsible for the endosperm-specific expression of a rice glutelin chimeric gene in transgenic tobacco. Plant Mol Biol. 1991 Jan;16(1):49–58. doi: 10.1007/BF00017916. [DOI] [PubMed] [Google Scholar]
- Thompson G. A., Siemieniak D. R., Sieu L. C., Slightom J. L., Larkins B. A. Sequence analysis of linked maize 22 kDa alpha-zein genes. Plant Mol Biol. 1992 Feb;18(4):827–833. doi: 10.1007/BF00020030. [DOI] [PubMed] [Google Scholar]
- Wallace J. C., Galili G., Kawata E. E., Cuellar R. E., Shotwell M. A., Larkins B. A. Aggregation of lysine-containing zeins into protein bodies in Xenopus oocytes. Science. 1988 Apr 29;240(4852):662–664. doi: 10.1126/science.2834822. [DOI] [PubMed] [Google Scholar]
- Wallace J. C., Lopes M. A., Paiva E., Larkins B. A. New Methods for Extraction and Quantitation of Zeins Reveal a High Content of gamma-Zein in Modified opaque-2 Maize. Plant Physiol. 1990 Jan;92(1):191–196. doi: 10.1104/pp.92.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williamson J. D., Galili G., Larkins B. A., Gelvin S. B. The synthesis of a 19 kilodalton zein protein in transgenic petunia plants. Plant Physiol. 1988 Dec;88(4):1002–1007. doi: 10.1104/pp.88.4.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]