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Post-transcriptional regulation of methionine content in maize kernels

Summary

Message levels for a methionine-rich 10 kDa zein were determined in three inbred lines of maize and their reciprocal crosses at various stages during endosperm development. Inbred line BSSS-53, which overexpresses the 10 kDa protein in mature kernels, was shown to have higher mRNA levels in developing endosperm, as compared to inbred lines W23 and W64A. Differences in mRNA levels could not be explained by differences in transcription rate of the 10 kDa zein gene, indicating differential post-transcriptional regulation of this storage protein in the different inbred lines analyzed. Among progeny segregating for the BSSS-53 allele of the 10 kDa zein structural gene Zps10l(22), mRNA levels are independent of Zps10/(22) segregation, indicating that post-transcriptional regulation of mRNA levels takes place via a trans-acting mechanism. In the same progeny, mRNA levels are also independent of allelic segregation of the regulatory locus Zpr10/(22). Thus, the trans-acting factor encoded by Zpr10/(22) determines accumulation of 10 kDa zein at a translational or post-translational step. Multiple trans-acting factors are therefore involved in post-transcriptional regulation of the methionine-rich 10 kDa zein.

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References

  • An G, Mitra A, Choi HK, Costa MA, An K, Thornburg RW, Ryan CA (1989) Functional analysis of the 3′ control region of the potato wound-inducible proteinase inhibitor II gene. The Plant Cell 1:115–122

    Google Scholar 

  • Beach LR, Spencer D, Randall PJ, Higgins TJV (1985) Transcriptional and post-transcriptional regulation of storage protein gene expression in sulfur-deficient pea seeds. Nucleic Acids Res 13:999–1013

    Google Scholar 

  • Benner MS, Phillips RL, Kirihara JA, Messing JW (1989) Genetic analysis of methionine-rich storage protein accumulation in maize. Theor Appl Genet 78:761–767

    Google Scholar 

  • Boronat A, Martinez MC, Reina M, Puigdomenech P, Palau J (1987) Isolation and sequencing of a 28 kD glutelin-2 gene from maize. Common elements in the 5′ flanking regions among zein and glutelin genes. Plant Sci 47:95–102

    Google Scholar 

  • Burr FA, Burr B (1982) Three mutations in Zea mays affecting zein accumulation: A comparison of zein polypeptides, in vitro synthesis and processing, mRNA levels, and genomic organization. J Cell Biol 94:201–206

    Google Scholar 

  • Burr B, Burr FA, St. John TP, Thomas M, Davis RD (1982) Zein storage protein gene family of maize. J Mol Biol 154:33–49

    Google Scholar 

  • Chestnut RS, Shotwell MA, Boyer SK, Larkins BA (1989) Analysis of avenin proteins and the expression of their mRNAs in developing oat seeds. The Plant Cell 1:913–924

    Google Scholar 

  • Das OP, Messing JW (1987) Allelic variation and differential expression at the 27-kilodalton zein locus in maize. Mol Cell Biol 7:4490–4497

    Google Scholar 

  • Das OP, Cruz-Alvarez M, Chaudhuri S, Messing J (1990) Molecular methods for genetic analysis of maize. Methods Mol Cell Biol 1:213–222

    Google Scholar 

  • Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387

    Google Scholar 

  • Dennis ES, Sachs MM, Gerlach WL, Finnegan EJ, Peacock WJ (1985) Molecular analysis of the alcohol dehydrogenase-2 gene of maize. Nucleic Acids Res 13:727–743

    Google Scholar 

  • Ernst D, Pfeiffer F, Schefbeck K, Weyrauch C, Oesterhelt D (1987) Phytochrome regulation of mRNA levels of ribulose-1,5-bisphosphate carboxylase in etiolated seedlings. Plant Mol Biol 10:21–33

    Google Scholar 

  • Gallie DR, Lucas WJ, Walbot V (1989) Visualizing mRNA expression in plant protoplasts: factors influencing efficient mRNA uptake and translation. The Plant Cell 1:301–311

    Google Scholar 

  • Geraghty DE (1987) Structure and organization of the zein multigene family. PhD thesis, University of Minnesota, St Paul, Minn

    Google Scholar 

  • Gruissem W (1989) Chloroplast gene expression: how plants turn their plastids on. Cell 56:161–170

    Google Scholar 

  • Heidecker G, Messing J (1987) Structural analysis of plant genes. Annu Rev Plant Physiol 37:439–466

    Google Scholar 

  • Ingelbrecht ILW, Herman LMF, Dekeyser RA, Van Montagu MC, Depicker AG (1989) Different 3′ end regions strongly influence the level of gene expression in plant cells. The Plant Cell 1: 671–680

    Google Scholar 

  • Kirihara JA, Hunsperger JP, Mahoney WC, Messing JW (1988a) Differential expression of a gene for a methionine-rich storage protein in maize. Mol Gen Genet 211:477–484

    Google Scholar 

  • Kirihara JA, Petri JB, Messing J (1988b) Isolation and sequence of a gene encoding a methionine-rich 10 kDa zein protein from maize. Gene 71:359–370

    Google Scholar 

  • Kodrzycki R, Boston RS, Larkins BA (1989) The opaque-2 mutation of maize differentially reduces zein gene transcription. The Plant Cell 1:105–114

    Google Scholar 

  • Labarca C, Paigen K (1980) A simple, rapid and sensitive DNA assay procedure. Anal Biochem 102:344–352

    Google Scholar 

  • Langridge P, Pintor-Toro JA, Feix G (1982) Transcriptional effect of the opaque-2 mutation of Zea mays L. Planta 156:166–170

    Google Scholar 

  • Maier U-G, Brown JWS, Toloczyki C, Feix G (1987) Binding of a nuclear factor to a consensus sequence in the 5′ flanking region of zein genes from maize. EMBO J 6:17–22

    Google Scholar 

  • Maier U-G, Brown JWS, Schmitz LM, Schwall M, Dietrich G, Feix G (1988) Mapping of tissue-dependent and independent protein binding sites to the 5′ upstream region of a zein gene. Mol Gen Genet 212:241–245

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Marks MD, Lindell JS, Larkins BA (1985) Quantitative analysis of the accumulation of zein mRNA during maize endosperm development. J Biol Chem 260:16445–16450

    Google Scholar 

  • Mertz ET, Bates LS, Nelson OE (1964) Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145:279–280

    Google Scholar 

  • Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78

    Google Scholar 

  • Messing J, Carlson J, Hagen G, Rubenstein I, Oleson A (1984) Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. DNA 3:31–40

    Google Scholar 

  • Mösinger E, Batschauer A, Schäfer E, Apel K (1985) Phytochrome control of in vitro transcription of specific genes in isolated nuclei from barley. Eur J Biochem 147:137–142

    Google Scholar 

  • Nielsen NC, Dickinson CD, Cho T-J, Thanh VH, Scallon BJ, Fischer RL, Sims TL, Drews GN, Goldberg RB (1989) Characterization of the glycinin gene family in soybean. The Plant Cell 1: 313–328

    Google Scholar 

  • Pedersen K, Argos P, Naravana SVL, Larkins BA (1986) Sequence analysis and characterization of a maize gene encoding a high-sulfur zein protein of Mr 15000. J Biol Chem 261:6279–6284

    Google Scholar 

  • Phillips RL, McClure BA (1985) Elevated protein-bound methionine in seeds of a maize line resistant to lysine plus threonine. Cereal Chem 62:213–218

    Google Scholar 

  • Phillips RL, Morris PR, Wold F, Gengenbach BG (1981) Seedling screening for lysine plus threonine resistant maize. Crop Sci 21:601–607

    Google Scholar 

  • Reeves CD, Krishnan HB, Okita TW (1986) Gene expression in developing wheat endosperm. Plant Physiol 82:34–40

    Google Scholar 

  • Schmidt RJ, Burr FA, Aukerman MJ, Burr B (1990) Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper” motif that binds to zein DNA. Proc Natl Acad Sci USA 87:4650

    Google Scholar 

  • Vieira J, Messing J (1987) Production of single-stranded plasmid DNA. Methods Enzymol 153:3–11

    Google Scholar 

  • Walling L, Drews GN, Goldberg RB (1986) Transcriptional and post-transcriptional regulation of soybean seed protein mRNA levels. Proc Natl Acad Sci USA 83:2123–2127

    Google Scholar 

  • Wilson DR, Larkins BA (1984) Zein gene organization in maize and related grasses. J Mot Evol 20:330–340

    Google Scholar 

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Communicated by H. Saedler

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Cruz-Alvarez, M., Kirihara, J.A. & Messing, J. Post-transcriptional regulation of methionine content in maize kernels. Molec. Gen. Genet. 225, 331–339 (1991). https://doi.org/10.1007/BF00269866

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  • DOI: https://doi.org/10.1007/BF00269866

Key words

  • Maize
  • Storage protein
  • Run-on transcription
  • Post-transcriptional regulation
  • Trans-acting factors