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A Chloroplast Gene Is Converted Into a Nucleargene

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A Chloroplast Gene Is Converted Into a Nucleargene Proc. Nati. Acad. Sci. USA Vol. 85, pp. 391-395, January 1988 Biochemistry Relocating a gene for herbicide tolerance: A chloroplast gene is converted into a nuclear gene (QB protein/atrazine tolerance/transit peptide) ALICE Y. CHEUNG*, LAWRENCE BOGORAD*, MARC VAN MONTAGUt, AND JEFF SCHELLt: *Department of Cellular and Developmental Biology, 16 Divinity Avenue, The Biological Laboratories, Harvard University, Cambridge, MA 02138; tLaboratorium voor Genetica, Rijksuniversiteit Ghent, B-9000 Ghent, Belgium; and TMax-Planck-Institut fur Zuchtungsforschung, D-500 Cologne 30, Federal Republic of Germany Contributed by Lawrence Bogorad, September 30, 1987 ABSTRACT The chloroplast gene psbA codes for the the gene for ribulose bisphosphate carboxylase/oxygenase photosynthetic quinone-binding membrane protein Q which can transport the protein product into chloroplasts (5). We is the target of the herbicide atrazine. This gene has been have spliced the coding region of the psbA gene isolated converted into a nuclear gene. The psbA gene from an from the chloroplast DNA of the atrazine-resistant biotype atrazine-resistant biotype of Amaranthus hybridus has been of Amaranthus to the transcriptional-control and transit- modified by fusing its coding region to transcription- peptide-encoding regions of a nuclear gene, ss3.6, for the regulation and transit-peptide-encoding sequences of a bona SSU of ribulose bisphosphate carboxylase/oxygenase of pea fide nuclear gene. The constructs were introduced into the (6). The fusion-gene constructions (designated SSU-ATR) nuclear genome of tobacco by using the Agrobacteium tumor- were introduced into tobacco plants via the Agrobacterium inducing (Ti) plasmid system, and the protein product of tumor-inducing (Ti) plasmid transformation system using the nuclear psbA has been identified in the photosynthetic mem- disarmed Ti plasmid vector pGV3850 (7). Some of the branes ofchloroplasts. Recovery of atrazine-tolerant transgen- transformed plants tolerated atrazine more than control ic plants shows that the product of the transplanted gene plants did. This indicated that the modified mutant QB functions in photosynthesis. These experiments show that it is protein produced in the cytoplasm had been taken up by the possible to modify chloroplast-gene-specified functions via chloroplasts and was functional there. Immunochemical nuclear-genome transformation and also raise evolutionary analyses of photosynthetic membrane proteins from trans- questions. formed atrazine-tolerant plants showed that they contain the imported modified QB protein. A major puzzle of eukaryotic cell biology is: Why are genes for some organelle proteins located in the nucleus, while METHODS AND MATERIALS genes for others are in the organelles (1)? One commonly entertained view is that proteins coded for by chloroplast Agrobaterium Ti Plasmid Transformation of Plants. Stan- and mitochondrial genes (e.g., photosynthetic membrane dard recombinant DNA procedures (8) were used to con- proteins) have properties that would block their passage struct plasmids. Plasmids pSSU-S-ATR and pSSU-L-ATR through the organelle's outer membrane system. We have (Fig. LA) were introduced into Agrobacterium GV3850 (7) to tested this proposition as well as the possibility ofgenetically generate strains GV3850:SSU-S-ATR and GV3850:SSU-L- altering functions normally encoded by chloroplast genes by ATR. These strains were used to inoculate wounded Nico- determining whether a modified chloroplast gene for a tiana tobaccum Wisconsin 38 or to infect leaf discs of SR1 photosynthetic membrane protein introduced into the nuclei tobacco (9). Infected plant tissues were propagated, and of tobacco plants can serve as the source of a protein that plantlets were regenerated as described (7). functions in photosynthetic electron transport. Plant DNA Analysis. DNA was isolated from leaftissues as In photosynthesis, plastoquinone molecules from the large described (10). Total restriction enzyme-digested DNA (10 pool present in the thylakoid membrane become associated ,ug) was separated electrophoretically in 0.8% agarose gels. with the quinone-binding protein, QB1 of photosystem II, The DNA was transferred to nitrocellulose, and the blot was where they are reduced. Once reduced they leave the hybridized with psbA sequences labeled with 32P by nick- binding site to be replaced by an oxidized quinone molecule translation (8). (2). Triazine herbicides compete with the plastoquinone for Protein Blot Analysis of Tobacco Thylakoid Proteins. Thy- binding and, thus, interrupt photosynthetic electron flow (3). lakoid membranes were isolated from tobacco plants (11). In situ in thylakoid membranes, the QB protein of atrazine- The membrane proteins were electrophoresed at 4°C in a sensitive plants, including Amaranthus hybridus, binds azi- NaDodSO4/polyacrylamide gel (12.5%) and electrotrans- doatrazine; QB protein from an atrazine-resistant biotype ferred to nitrocellulose paper (12). The protein blot was does not bind the herbicide because of a single amino acid treated with an antibody [QB-3 (13)] against a synthetic residue substitution (4). Thus, if this mutation in the QB oligopeptide corresponding to an internal region of the QB protein, encoded by the chloroplast psbA gene, is the basis protein. Horseradish peroxidase conjugated to second anti- of atrazine resistance, the functional integration of this bodies was used to locate the antibody. protein into the photosynthetic apparatus of a plant that is normally sensitive would confer atrazine tolerance. RESULTS Plants transformed with the bacterial neomycin phospho- transferase gene spliced behind the promoter and transit Construction of Chimeric SSU-S-ATR and SSU-L-ATR peptide-encoding sequences of the small subunit (SSU) of Genes. All known nuclear-coded, cytoplasmically synthe- sized proteins destined for chloroplasts contain amino- The publication costs of this article were defrayed in part by page charge terminal transit peptides that are removed some time during payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. Abbreviations; SSU, small subunit; Ti, tumor-inducing. 391 Downloaded by guest on October 2, 2021 392 Biochemistry: Cheung et al. Proc. Nail. Acad. Sci. USA 8S (1988) or after import of the proteins into the organelle (11). regulatory sequences and the transit-peptide-encoding se- Furthermore, chloroplast genes from maize and A. hybridus quence of a nuclear rbcS gene (for the SSU of ribulose are not transcribed from their own promoters when placed in bisphosphate carboxylase/oxygenase), ss3.6, from pea (6). the nuclei of transgenic tobacco plants (A.Y.C. and L.B. The first exon of ss3.6 encodes the entire transit peptide plus unpublished data). We have taken both of these facts into the first two amino acids of the mature SSU polypeptide. account in constructing two plasmid vectors, pSSU-L and Plasmid pSSU-S contains only this exon and has a unique pSSU-S (Fig. lA), into which the coding region of a plastid BamHI cloning site two amino acid codons behind the gene can be cloned to form translational fusion genes that are transit-peptide-processing site. The second of these two expressed in the nucleus. This allows for testing the trans- amino acid codons resulted from the construction of the portability of proteins into chloroplasts by the SSU transit cloning site. Plasmid pSSU-L carries the entire first exon, peptide because each plasmid carries the transcriptional- the first intron, and part of the second exon. A unique Bgl II A Hind m HindM Barn HI Barm HI HindM EcoRI S Eco RI \ ::9 Sal I Bam HI pssu-s h-) KMr pSSU-S-ATR Barn HI Eco RI ApaI SalI SalI EcoRI Apr\ ApaI Sal I Barn HI fragment containing ps2B Hind]H B I Hind M BamHI SI EcoRI a RI Kmr pSSU-L EcoRI ApalSalI BgIlE Kmr pSSU-I - Bglfl/BamHIfused Eco RI ApoI Eco RI Sall Sail Ap`\ ApaI B Sequence at the junction of SSU-S and ATR is: A( -TGC ATG gat ccc gGG ATA ACC - ATG-ATR- COO/ 1St -16th 1 St aaof aa of aaof n OC SSU Q08C Transit protein proteir processing J site Bam HI linker from ps2B gene Sequence at the junction of SSU -L-and ATR is: H2SSUTGCAATG CAG SSU AGa got ccc gGG ATA ACC ATG COOH t 1st 23 rd -16th 1 st aaof aaof aaof aaof SSU SSU 08 QB Transit k....J protein protein processing Bgla linker site from SSU-L vector Bam HI linker from ps2B gene FIG. 1. General cloning vectors pSSU-S and pSSU-L and chimeric gene vectors pSSU-S-ATR and pSSU-L-ATR. (A) pSSU-S was constructed by placing a unique BamHI cloning site behind a 900-base-pair (bp) fragment from ss3.6, which included the regulatory region (I3) and the coding region for the transit peptide (M) and two amino acids of the mature SSU (S) (see also ref. 5). pSSU-L was similar to pSSU-S except that the portion of ss3.6 in this plasmid extends into amino acid 23 of the SSU peptide, and a unique Bgl II cloning site has been engineered behind the ss3.6 DNA. Both pSSU-S and pSSU-L have a bacterial neomycin phosphotransferase gene (15) and a fragment (ocs 3') from the 3' end of the ocs gene (14), which includes a mRNA polyadenylylation site. Plasmids pSSU-S-ATR and pSSU-L-ATR were constructed by introducing a BamHI fragment that contained a BAL-31-modified psbA gene [from pAh484 (in) (4)] into the BamHI site of vector pSSU-S and the Bgl II site of vector pSSU-L, respectively. (ps2B is another designation for the gene psbA.) (B) The nucleotide sequence and derived amino acid positions of the fusion regions of SSU-S-ATR and SSU-L-ATR genes are shown. Kmr, kanamycin resistance; Apr, ampicillin resistance; aa, amino acid. Downloaded by guest on October 2, 2021 Biochemistry: Cheung et aL Proc. Natl. Acad. Sci. USA 85 (1988) 393 cloning site is located at the 23rd amino acid codon of the have proved to be useful for distinguishing it from the SSU in pSSU-L.
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