Summary
A cDNA libary prepared using mRNA isolated from red-light irradiated maize seedlings was screened by a difference procedure for clones that represent red-light regulated mRNA. Two such clones were found to represent mRNA for a chlorophyll a/b binding protein (CAB), and one of these (pAB1084) was used to screen a maize genomic library. One positive genomic clone (λAB1084) was isolated and sequenced. The gene represented by λAB1084, which we designate maize cab-1, contains extensive nucleotide homology within its protein coding region to CAB genes from other species. The boundaries of the transcribed region of the cab-1 gene were determined by S1 nuclease mapping. The 5′ terminus of cab-1 mRNA is located 52–54 nucleotides (nt) upstream of the translation start site and 34 nt downstream of a TATA box. As in the case of petunia CAB genes, several poly(A) addition sites are present in mRNA from the cab-1 gene. The 5′ flanking DNA of cab-1 contains sequences related to elements that have been implicated in the light-regulated expression of CAB and rccS genes in other plant systems. Quantitative Northern blot hybridization analysis using a gene specific probe for cab-1 indicates that the mRNA for this gene is present at 0.4% of the total mRNA and up to 80% of the total CAB mRNA in the leaves of dark-grown seedlings. In consequence, although the degree of up-regulation by white light is only moderate (3- to 6-fold), cab-1 transcripts account for approximately 2% of the mRNA in the leaves of light-grown seedlings.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
An G (1987) Organ specific and light dependent expression of all three chlorophyll a/b binding protein genes of Arabidopsis thaliana in transformed tobacco cells. Mol Gen Genet 207:210–216
Anderson JM (1986) Photoregulation of the composition, function and structure of the thylakoid membranes. Annu Rev Plant Physiol 37:93–136
Apel K (1979) Phytochrome-induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare). Eur J Biochem 97:183–188
Batschauer A, Mosinger E, Krenz 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 protein. Eur J Biochem 154:625–634
Battula N, Loeb LA, (1974) The infidelity of avian myeloblastosis virus deoxyribonucleic acid polymerase in polynucleotide replication. J Biol Chem 249:4086–4093
Benoist C, O'Hare K, Breathnach R, Chambon P (1980) The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res 8:127–142
Benton WD, Davis RW (1977) Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196:180–183
Berk AJ, Sharp PA (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell 12:721–732
Biggin MD, Gibson TJ, Hong GF (1983) Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965
Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Broglie R, Coruzzi G, Keith B, Chua N-H (1984) Molecular biology of C4 photosynthesis in Zea Mays: Differential localization of protein and mRNAs in the two leaf cell types. Plant Mol Biol 3:431–444
Carlson DP, Ross J (1983) Human β-globin promoter and coding sequences transcribed by RNA polymerase III. Cell 34:857–864
Cashmore AR (1984) Structure and expression of a pea nuclear gene encoding a chlorophyll a/b-binding polypeptide. Proc Natl Acad Sci USA 81:2960–2964
Castresana C, Garcia-Luque I, Alonso E, Malik VS, Cashmore AR (1988) Both positive and negative regulatory elements mediate expression of a photoregulated CAB gene from Nicotiana plumbaginifolia. EMBO J 7:1929–1936
Colbert JT, Hershey HP, Quail PH (1983) Autoregulatory control of translatable phytochrome mRNA levels. Proc Natl Acad Sci USA 80:2248–2252
Dean C, Tamaki S, Dunsmuir P, Favreau M, Katayama C, Dooner H, Bedbrook J (1986) mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucleic Acids Res 12:2229–2240
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Dunsmuir P (1985) The petunia chlorophyll a/b binding protein genes: A comparison of CAB genes from different gene families. Nucleic Acids Res 13:2503–2518
Fluhr R, Chua N-H (1986) Developmental regulation of two genes encoding ribulose-bisphosphate carboxylase small subunit in pea and transgenic petunia plants: Phytochrome response and blue-light induction. Proc Natl Acad Sci USA 83:2358–2362
Gallagher TF, Ellis RF (1982) Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J 1:1493–1498
Green PJ, Kay SA, Chua N-H (1987) Sequence specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J 6:2543–2549
Greenland AJ, Thomas MV, Walden RM (1987) Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings. Planta 170:99–110
Harpster M, Apel K (1985) The light-dependent regulation of gene expression during plastid development in higher plants. Physiol Plant 64:147–152
Hershey HP, Colbert JT, Lissemore, JL, Barker, RF, Quail PH (1984) Molecular cloning of cDNA for Avena phytochrome. Proc Natl Acad Sci USA 81:2332–2336
Karlin-Neumann GA, Tobin EM (1986) Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5:9–13
Karlin-Neumann GA, Kohorn BD, Thorber JP, Tobin EM (1985) A chlorophyll a/b-protein encoded by a gene containing an intron with characteristics of a transposable element. J Mol Appl Genet 3:45–61
Kohorn BD, Harel E, Chitnis PR, Thornber JP, Tobin E (1986) Functional and mutational analysis of the light-harvesting chlorophyll a;b protein of thylakoid membranes. J Cell Biol 102:972–981
Kuhlemeier C, Fluhr R, Green PJ, Chua N-H (1987a) Sequences in the pea rbc-3A gene have homology to constitutive mammalian enhancers but function as negative regulatory elements. Genes Devel 1:247–255
Kuhlemeier C, Green PJ, Chua N-H (1987b) Regulation of gene expression in higher plants. Annu Rev Plant Physiol 38:221–257
Lamppa GK, Morelli G, Chua N-H (1985) Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol Cell Biol 5:1370–1378
Leutwiler LS, Meyerowitz EM, Tobin EM (1986) Structure and expression of three light-harvesting chlorophyll a/b binding protein genes in Arabidopsis thaliana. Nucleic Acids Res 14:4051–4064
Lissemore JL, Colbert JT, Quail PH (1987) Cloning of cDNA for phytochrome from etiolated Cucurbita and coordinate photoregulation of the abundance of two distinct phytochrome transcripts. Plant Mol Biol 8:485–496
Loenen WAM, Blattner FR (1983) Lamdba Charon vectors (CH32, 33, 34 and 35) adapted for DNA cloning in recombination-deficient hosts. Gene 26:171–179
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York
Manzara T, Gruissem W (1988) Organization and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase in higher plants. Photosyn Res 16:117–139
Maquat LE, Kinniburgh AJ, Rachmilewitz EA, Ross J (1981) Unstable β-globin mRNA in mRNA-deficient β° thalassemia. Cell 27:543–553
Matsuoka M, Kano-Murakami Y, Yamamoto N (1987) Nucleotide sequence of cDNA encoding the light-harvesting chlorophyll a/b binding protein from maize. Nucleic Acids Res 15:6302
Maxam AM, Gilbert W (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Method Enzymol 65:499–560
Mayfield SP, Taylor WC (1984) Carotenoid-deficient maize seed-lings fail to accumlate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur J Biochem 144:79–84
Mohr H (1966) Differential gene activation as a mode of action of phytochrome 730. Photochem Photobiol 5:469–483
Morelli G, Nagy F, Fraley RT, Rogers SG, Chua N-H (1985) A short conserved sequence is involved in light-inducibility of a gene encoding ribulose-1,5-bisphosphate carboxylase small subunit of pea. Nature 315:200–204
Murray MG (1986) Use of sodium trichloroacetate and mung bean nuclease to increase sensitivity and precision during transcript mapping. Anal Biochem 158:165–170
Murray MG, Kennard WC, Drong RF, Slightom, JL (1984) Use of a recombination-deficient phage lambda system to construct wheat genomic libraries. Gene 30:237–240
Myers RM, Tilly K, Maniatis T (1984) Fine structure genetic analysis of a β-globin promoter. Nature 232:613–618
Myers RM, Lumelsky N, Lerman LS, Maniatis T (1985) Detection of single base substitutions in total genomic DNA. Nature 313:495–497
Nagy F, Fluhr R, Kuhlemeier C, Kay S, Boutry M, Green P, Poulsen C, Chua N-H (1986) Cis-acting elements for selective expression of two photosynthetic genes in, transgenic plants. Philos Trans R Soc London 314:493–500
Nagy F, Boutry M, Hsu M-Y, Wong M, Chua N-H (1987) The 5′-proximal region of the wheat Cab-1 gene contains a 268-bp enhancer-like sequence for phytochrome response. EMBO J 6:2537–2542
Nelson T, Harpster MH, Mayfield SP, Taylor WC (1984) Light-regulated gene expression during maize leaf development. J Cell Biol 98:558–564
Pichersky E, Bernatzky R, Tanksley SD, Breidenbach RB, Kausch AP, Cashmore AR (1985) Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (Tomato). Gene 40:247–258
Pichersky E, Hoffman NE, Malik VS, Bernatsky SD, Tanksley SD, Szabo L, Cashmore AR (1987) The tomato Cab-4 and Cab-5 genes encode a second type of CAB polypeptide localized in Photosystem II. Plant Mol Biol 9:109–120
Quail PH, Colbert JT, Peters NK, Christensen AH, Sharrock RA, Lissemore JL (1986) Phytochrome and the regulation of the expression of its genes. Philos Trans R Soc London Ser B 314:469–480
Sassone-Corsi P, Borelli E (1986) Transcriptional regulation by trans-acting factors. Trends Genet 2:215–219
Schmidt GW, Bartlett SG, Grossman AR, Cashmore AR, Chua N-H (1981) Biosynthetic pathways of two polypeptide subunits of light-harvesting chlorophyll a/b protein complex. J Cell Biol 91:468–478
Sheen J, Bogorad L (1986) Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci USA 83:7811–7815
Shropshire W Jr, Mohr H (1983) Photomophogenesis, Encyclopaedia Plant Physiol, vols 16A, B. Springer-Verlag, Berlin Heidelberg New York
Simpson J, Timko MP, Cashmore AR, Schell J, Van Montagu M, Herrera-Estrella L (1985) Light inducible and tissue-specific expression of a chimaeric gene under control of the 5′-flanking sequence of a pea chlorophyll a/b-binding protein gene. EMBO J 4:2723–2729
Simpson J, Schell J, Van Montagu M, Herrera-Estrella L (1986) Light-inducible and toissue-specific pea lhcp gene expression involves an upstream element combining enhancer and silencer-like properties. Nature 323:551–554
Stayton MM, Back M, Bedbrook J, Dunsmuir P (1986) A novel chlorophyll a/b binding (Cab) protein gene from petunia which encodes the lower molecular weight Cab precursor protein. Nucleic Acids Res 14:9781–9786
Thompson WF Kaufman LS, Watson JL (1985) Induction of plant gene expression by light. BioEssays 3:153–159
Timko MP, Kausch AP, Castresana C, Fassler J, Herrera-Estrella L, Van den Brockk G, Van Montagu M, Schell J, Cashmore AR (1985) Light regulation of plant gene expression by an upstream enhancer-like element. Nature 318:579–582
Tobin EM (1981) Phytochrome-mediated regulation of messenger RNAs for the small subunit of ribulose 1,5-bisphosphate carboxylase and the light-harvesting chlorophyll a/b-protein in Lemna gibba. Plant Mol Biol 1:35–51
Tobin EM, Silverthorne J (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36:569–593
Weaver RF, Weissmann C (1979) Mapping of RNA by a modification of the Berk-Sharp procedure. The 5′ termini of 15S β-globin mRNA precursor and mature 10S β-globin mRNA have identical map coordinates. Nucleic Acids Res 7:1175–1193
Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119
Author information
Authors and Affiliations
Additional information
Communicated by R.G. Hermann
Rights and permissions
About this article
Cite this article
Sullivan, T.D., Christensen, A.H. & Quail, P.H. Isolation and characterization of a maize chlorophyll a/b binding protein gene that produces high levels of mRNA in the dark. Molec. Gen. Genet. 215, 431–440 (1989). https://doi.org/10.1007/BF00427040
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00427040