Abstract
The expression of specific mitochondrial, chloroplast and nuclear genes has been investigated in leaves of 7-d-old light-grown wheat (Triticum aestivum cv. Maris Dove). In the wheat leaf there is a spatial separation of a temporal sequence of development from the basal meristem to the distal mature, photosynthetically competent cells. This sequence of cellular differentiation is paralleled by a functional differentiation in which the energy supply changes from oxidative phosphorylation in the non-green meristematic cells to a combined dependence on oxidative and photophosphorylation in the photosynthesizing cells. The changes in copy number per cell and expression of mitochondrial genes have been investigated in successive sections of the wheat leaf using quantitative DNA-DNA and DNA-RNA filter and protein-binding techniques. The abundance of specific mitochondrial genes (cox II.cob andatp A) per cell was found to decrease between five- and tenfold within the basal (1 cm) section of the leaf and then remain constant to the distal tip. The relative abundances of specific mitochondrial transcripts (cox I,cox II,cob andatp A) were found to decrease in successive sections from the basal meristem to the distal tip (from a relative value of 100% to 5–40%). In contrast, transcripts of chloroplast genes and nuclear genes encoding chloroplast polypeptides (psb A,rbc L andrbc S) were found to increase steadily in progressive leaf sections (from a relative value of 0–2% to 100%). The steady-state level of the α-subunit of the mitochondrial F1 ATPase was found to remain constant along the length of the leaf. Possible sites at which the regulation of organellar gene expression is coordinated during the development of photosynthetic competence within the wheat leaf are discussed.
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Abbreviations
- kb:
-
kilobase
- kDa:
-
kilodalton
- mtDNA:
-
mitochondrial DNA
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase
References
Arron, G.P., Edwards, G.E. (1980) Light-induced development of glycine oxidation by mitochondria from sunflower cotyledons. Plant Sci. Lett.18, 229–235
Bagshaw, V., Brown, R., Yeoman, M.M. (1969) Changes in the mitochondrial complex accompanying callus growth. Ann. Bot.33, 35–44
Batschauer, A., Mösinger, E., Kreuz, K., Dörr, I., Apel, K. (1986) The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b binding protein. Eur. J. Biochem.154, 625–634
Becker, W.M., Leaver, C.J., Weir, E.M., Riezman, H. (1978) Regulation of glyoxysomal enzymes during germination of cucumber. I. Developmental changes in cotyledonary protein, RNA and enzyme activities during germination. Plant Physiol.62, 542–549
Bonen, L., Boer, P.H., Gray, M.W. (1984) The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize. EMBO J.3, 2531–2536
Brown, R., Rickless, P.A. (1949) A new method for the study of cell division and cell extension with preliminary observations on the effect of temperature and nutrients. Proc. R. Soc. London Ser. B136, 110–125
Burgess, D.G., Taylor, W.C. (1987) Chloroplast photooxidation affects the accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta170, 520–527
Clowes, F.A.L., Juniper, B.E. (1964) The fine structure of the quiescent centre and neighbouring tissues in root meristems. J. Exp. Bot.15, 622–630
Dawson, A.J., Jones, V.P., Leaver, C.J. (1984) The apocytochrome b gene in maize mitochondria does not contain introns and is preceded by a potential ribosome binding site. EMBO J.3, 2107–2113
Dean, C., Leech, R.M. (1982) Genome expression during normal leaf growth. Plant Physiol.69, 904–910
Feiler, H.s., Newton, K.J. (1987) Altered mitochondrial gene expression in the nonchromosomal stripe 2 mutant of maize. EMBO J.6, 1535–1539
Feinberg, A.P., Vogelstein, B. (1984) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem.137, 266–267
Fox, T.D. (1986) Nuclear gene products required for translation of specific mitochondrially coded mRNAs in yeast. Trends Genet.2, 97–100
Fox, T.D., Leaver, C.J. (1981) TheZea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell26, 315–323
Godson, G.N., Vapriek, D. (1973) A simple method of preparing large amounts of ϕX174 RF1 supercoiled DNA. Biochim. Biophys. Acta.299, 516–520
Gunning, B.E.S., Steer, M.W. (1975) Ultrastructure and biology and plant cells, pp. 88–90. Arnold, London
Hack, E., Leaver, C.J. (1983) The alpha-subunit of the maize F1-ATPase is synthesized in the mitochondrion. EMBO J.2, 1783–1789
Isaac, P.G., Jones, V.P., Leaver, C.J. (1985a) The maize cytochromec oxidase subunit I gene: sequence, expression and rear-rangement in cytoplasmic male sterile plants. EMBO J.4, 1617–1623
Isaac, P.G., Brennicke, A., Dunbar, S.M., Leaver, C.J. (1985b) The mitochondrial genome of fertile maize (Zea mays L.) contains two copies of the gene encoding the α-subunit of the F1 ATPase. Curr. Genet.10, 321–328
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature227, 680–685
Leaver, C.J., Ingle, J. (1971) The molecular integrity of chloroplast rRNA. Biochem. J.123, 235–243
Lee, J.S.-L., Warmke, H.E. (1979) Organelle size and number in fertile and T-cytoplasmic male-sterile corn. Am. J. Bot.60, 141–148
Leech, R.M. (1985) The synthesis of cellular components in leaves. In: Control of leaf growth (SEB Seminar Series Vol. 27) pp. 93–114, Baker, N.R., Davies, W.D., Ong, C. eds. Cambridge University Press, Cambridge
Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem.193, 265–275
Maniatis, T., Fritsch, E.F., Sambrook, J. (1982) Molecular cloning. Cold Spring Harbor Laboratories, Cold Spring Harbor, NY
Martineau, B., Taylor, W.C. (1985) Photosynthetic gene expression and cellular differentiation in developing maize leaves. Plant Physiol.78, 399–404
Mayfield, S.P., Taylor, W.C. (1984) The appearance of photosynthetic proteins in developing maize leaves. Planta161, 481–486
Newton, K.J., Coe, E.H., Jr. (1986) Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize. Proc. Natl. Acad. Sci. USA83, 7363–7366
Parikh, V.S., Morgan, M.M., Scot, R., Clements, L.S., Butow, R.A. (1987) The mitochondrial genotype can influence nuclear gene expression in yeast. Science235, 576–580
Peterson, G.L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem.83, 346–356
Tobin, E.M., Silverthorne, J. (1985) Light regulation of gene expression in higher plants. Annu. Rev. Plant Physiol.36, 569–593
Towbin, H., Staehelin, I., Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA76, 4350–4354
Viro, M., Kloppstech, K. (1980) Differential expression of the genes for ribulose, 1,5-bisphosphate carboxylase and light-harvesting chlorophyll a/b protein in the developing barley leaf. Planta150, 41–45
Walker, J.L., Oliver, D.J. (1986) Light-induced increases in the glycine decarboxylase multienzyme complex from pea mitochondria. Arch. Biochem. Biophys.248, 626–638
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Topping, J.F., Leaver, C.J. Mitochondrial gene expression during wheat leaf development. Planta 182, 399–407 (1990). https://doi.org/10.1007/BF02411391
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DOI: https://doi.org/10.1007/BF02411391