Abstract
To better understand the regulatory roles of nuclear genes in chloroplast genomic expression during leaf development in maize (Zea mays L.), we studied a striped mutant, ii1 (iojap 1), two albino mutants, w1 (white 1) and w2 (white 2), and their double mutants with l (luteus). Homozygous ij1 plants as a female parent produce albino seedlings, called maternal exceptions, among their progeny, even when the nuclear genotype of the male parent is normal (+/+). In contrast to albinos that are blocked in the biosynthetic pathway of carotenoids, w1 and w2 seedlings fail to accumulate chlorophyll and carotenoids up to the normal level even under dim light conditions. In ij1-affected plastids, the plastid-encoded proteins and nuclear-encoded proteins that are associated with thylakoid membranes were not detecable. However, the 33-kDa protein of the oxygen-evolving complex and ferredoxin: NADP oxidoreductase, which are localized extrinsically, were accumulated even though the level of the proteins was decreased. Both ij1 and w1 albino seedlings contain a normal level of plastid DNA. However, both show similar aberrant patterns among the transcripts of all the plastid genes examined (psbB, psbH, petB, petD, atpA, psaB, psbA, and rbcL). Not only were additional transcripts detected but some of the normal transcripts were not detectable or were barely detectable by Northern hybridization. These facts indicate that the transcripts of ij1- and w1-affected plastids may have altered synthesis, processing or stability. Therefore, the block in expression of the plastid genome by the nuclear mutants ij1 and w1 may be due to alterations in the transcriptional or post-transcriptional processes. The fact that ij1 and maternal-exception progeny show almost identical patterns of transcripts indicates that the effects of ij1 on plastid gene expression persist in the subsequent generation even after the nuclear gene, Ij1, restores the normal function. In contrast to ij1 and w1, the levels of all plastid transcripts in w2 seedlings, whether l or +, are uniformly reduced. Compared to normal sibling seedlings, the patterns of the RNA species are relatively unaltered. Relative to the level of a nuclear rDNA, the plastid DNA content of w2 is decreased 20-fold. Therefore, the limited expression of the w2-affected plastids may be due to failure to maintain the copy number of plastid genomes. Thus, albinisms of these mutants result from limiting of expression of plastids due to alteration of transcripts on the one hand, or to lowered DNA content on the other.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- FNR:
-
ferredoxin: NADP oxidoreductase
- OEC-33:
-
33-kDa protein of the oxygen-evolving complex
- Rubisco:
-
ribulose-1,5-bisphopsphate carboxylase-oxygenase
References
Bachmann, M.D., Robertson, D.S., Bowen, C.C., Anderson, I.C. (1968) Chloroplast development in pigment deficient mutants of maize. J. Ultrastruct. Res. 21, 41–60
Barkan, A. (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 7, 2637–2644
Barkan, A. (1989) Tissue-dependent plastid RNA splicing in maize: transcripts from four plastid genes are predominantly unspliced in leaf meristems and roots. Plant Cell 1, 437–445
Barkan, A., Miles, D., Taylor, W.C. (1986) Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J. 5, 1421–1427
Baumgartner, B.J., Rapp, J.C., Mullet, J.E. (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol. 89, 1011–1018
Bendich, A.J. (1987) Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays 6, 279–282
Boffey, S.A., Leech, R.M. (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol. 69, 1387–1391
Börner, T., Sears, B.B. (1986) Plastome mutants. Plant Mol. Biol. Rep. 4, 69–92
Britton, G., Goodwin, T.W. (1971) Biosynthesis of carotenoids. Methods Enzymol. 18, 654–700
Coe, E.H., Jr., Neuffer, M.G., Hoisington, D.A. (1988a) The genetics of corn. In: Corn and corn improvement, pp. 81–258. Sprague, G.F., Dudley, J., eds. American Society of Agronomy, Madison, USA
Coe, E. H., Jr., Thompson, D. L., Walbot, V. (1988b) Phenotypes mediated by the iojap genotype in maize. Am. J. Bot. 75, 634–644
Cozens, A.L., Walker, L.E., Phillips, A.L., Huttly, A.K., Gray, J.C. (1986) A sixth subunit of ATP synthase, an Fo component, is encoded in the pea chloroplast genome. EMBO J. 5, 217–222
Crossland, L.D., Rodermel, S.R., Bogorad, L. (1984) Single gene for the large subunit of ribulose bisphosphate carboxylase in maize yields two differentially regulated mRNAs. Proc. Natl. Acad. Sci. USA 81, 4060–4063
Demerec, M. (1923) Inheritance of white seedlings in maize. Genetics 8, 561–593
Deng, X.-W., Gruissem, W. (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49, 379–387
Deng, X.-W., Stern, D.B., Tonyn, J.C., Gruissem, W. (1987) Plastid run-on transcription: application to determine the transcriptional regulation of plastid genes. J Biol. Chem. 262, 9641–9648
Fish, L.E., Bogorad, L. (1986) Identification and analysis of the maize P700 chlorophyll a apoproteins PSI-A1 and PSI-A2 by high pressure liquid chromatography analysis and partial sequence determination. J. Biol. Chem. 261, 8134–8139
Fish, L.E., Kuck, U., Bogorad, L. (1985) Two partially homologous adjacent light inducible maize chloroplast genes encoding polypeptides of the P700 chlorophyll a protein complex of photosystem I. J. Biol. Chem. 260, 1413–1421
Goodwin, T.W. (1980) The biochemistry of the carotenoids, 2nd edn., vol I. Chapman and Hall, London
Han, C-d., Coe, E.H., Martienssen, R.A. (1992) Molecular cloning and characterization of ij (iojap), a pattern striping gene of maize. EMBO J. 11, 4037–4046
Hess, W.R., Promona, A., Fielder, B., Subramanian, A.R., Börner, T. (1993) Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J. 12, 563–572
Hosler, J.P., Wurtz, E.A., Harris, E.H., Gillham, N.W., Boynton, J.E. (1989) Relationship between gene dosage and gene expression in the chloroplast of Chlamydomonas reinhardtii. Plant Physiol. 91, 648–655
Hudson, G.S., Mason, J.G., Holton, T.A., Koller, B., Cox, G.B., Whitfeld, P.R., Bottomley, W. (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and CFO subunits of the H+-ATP synthase complex and the ribosomal protein S2. J. Mol. Biol. 196, 283–298
Kirk, J.T.O., Tilney-Bassett, R.A.E. (1978) The plastids. Elsevier/North-Holland Biomedical Press, Amsterdam, The Netherlands
Klein, R.R., Mullet, J.E. (1987) Control of gene expression during higher plant chloroplast biogenesis. J. Biol. Chem. 262, 4341–4348
Knoth, R., Hagemann, R. (1977) Structure and function of the genetic information in plastids: XVI. The ultrastructure of plastids and the electron microscopic proof of mixed cells in leaves of plastome mutants induced by the gene mutation albostrians of Hordeum vulgare L. Biol. Zentralbl. 96, 141–150
Lamppa, G., Bendich, A. (1979) Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol. 64, 126–130
Lawrence, M.E., Possingham, J.V. (1986) Microspectrofluorometric measurement of chloroplast DNA in dividing and expanding leaf cells of Spinacea oleracea. Plant Physiol. 81, 708–710
Leto, K.J., Bell, E., McIntosh, L. (1985) Nuclear mutation leads to an accelerated turnover of chloroplast-encoded 48 kd and 34.5 kd polypeptides in thylakoids lacking photosystem II. EMBO J. 4, 1645–1653
Lindstrom, E.W. (1924) Complementary genes for chlorophyll development in maize and their linkage relations. Genetics 9, 305–326
Little, M.C., Hallick, R.B. (1988) Chloroplast rpoA, rpoB and rpoC genes specify at least three components of a chloroplast DNA-dependent RNA polymerase active in tRNA and mRNA transcription. J. Biol. Chem. 263, 14302–14307
Mayfield, S.P., Nelson, T., Taylor, W.C., Malkin, R. (1986) Carotenoid synthesis and pleiotropic effects in carotenoid-deficient seedlings of maize. Planta 169, 23–32
Mullet, J.E., Klein, R.R. (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J. 6, 1571–1579
Mullet, J.E., Orozco, E.M., Chua, N.H. (1985) Multiple transcripts for higher plant rbcL and atpB genes and localization of the transcription initiation site of the rbcL gene. Plant Mol. Biol. 4, 39–54
Rau, W. (1988) The function of carotenoids other than in photosynthesis. In: Plant pigments pp. 231–255, Goodwin T.W., ed. Academic Press, New York, NY
Redei, G.P. (1973) Extra-chromosomal mutability determined by a nuclear gene locus in Arabidopsis. Mut. Res. 18, 149–162
Reiss, T., Bergeld, R., Link, G., Thien, W., Mohr, H. (1983) Photooxidative destruction of chloroplasts and its consequences for cytosolic enzyme levels and plant development. Planta 159, 518–528
Rhoades, M.M. (1943) Genic induction of an inherited cytoplasmic difference. Proc. Natl. Acad. Sci. USA 29, 327–329
Robertson, D.S. (1975) Survey of the albino and white endosperm mutants of maize: Their phenotypes and gene symbols. J. Hered. 66, 67–74
Robertson, D.S., Anderson, I.C., Bachmann, M.D. (1978) Pigmentdeficient mutants: genetic, biochemical, and developmental studies. In: Maize breeding and genetics pp. 461–494, Walden, D.B., ed. John Wiley & Sons, Inc., New York
Rochaix, J.-D., Erickson, J. (1988) Function and assembly of photosystem II: genetic and molecular analysis. Trends Biochem. Sci. 13, 56–59
Rock, C.D., Barkan, A., Taylor, W.C. (1987) The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products. Curr. Genet. 12, 69–77
Siemenroth, A., Börner T., Metzger, U. (1980) Biochemical studies on the iojap mutant of maize. Plant Physiol. 65, 1108–1110
Stroup, D. (1970) Genic induction and maternal transmission of variegation in Zea mays. J. Hered. 61, 139–141
Sugiura, M. (1989) The chloroplast genome. In: The Biochemistry of plants. A comprehensive treatise. vol. 15, pp. 133–149, Marcus, A., ed. Academic Press, New York, NY
Sutton, A., Sieburth, L.E., Bennett, J. (1987) Light-dependent accumulation and localization of photosystem II proteins in maize. Eur. J. Biochem. 164, 571–578
Thompson, D.L., Walbot, V., Coe, E.H., Jr. (1983) Plastid development in iojap and chloroplast mutator-affected maize plants. Am. J. Botany 70, 940–950
Walbot, V., Coe, E.H., Jr. (1979) Nuclear gene iojap conditions a programmed change to ribosome-less plastids in Zea mays. Proc. Natl. Acad. Sci. USA 76, 2760–2764
Westhoff, P., Herrmann, R.G. (1988) Complex RNA maturation in chloroplasts: the psbB operon from spinach. Eur. J. Biochem. 171, 551–564
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Han, Cd., Patrie, W., Polacco, M. et al. Aberrations in plastid transcripts and deficiency of plastid DNA in striped and albino mutants in maize. Planta 191, 552–563 (1993). https://doi.org/10.1007/BF00195757
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00195757