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Genes for the Eight Ribosomal Proteins Are Clustered on the Chloroplast Genome of Tobacco (Nicotiana Tabacum): Similarity To

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Genes for the Eight Ribosomal Proteins Are Clustered on the Chloroplast Genome of Tobacco (Nicotiana Tabacum): Similarity To Proc. Nati. Acad. Sci. USA Vol. 83, pp. 6030-6034, August 1986 Genetics Genes for the eight ribosomal proteins are clustered on the chloroplast genome of tobacco (Nicotiana tabacum): Similarity to the S10 and spc operons of Escherichia coli (molecular cloning/DNA sequence/open reading frame/intron/blot hybridization) MINORU TANAKA*, TATSUYA WAKASUGI*, MAMORU SUGITAt, KAZUO SHINOZAKI*, AND MASAHIRO SUGIURA*t *Center for Gene Research, Nagoya University, Chikusa, Nagoya 464, Japan; and tDepartment of Botany, Hokkaido University, Sapporo 060, Japan Communicated by Dan L. Lindsley, April 21, 1986 ABSTRACT The nucleotide sequence of a tobacco in 6x SSC at 37°C for 2 hr. (1x SSC = 0.15 M NaCi, 0.015 (Nicotiana tabacum) chloroplast gene duster that encodes eight M sodium citrate, pH 7.0.) proteins homologous to Escherichia coli ribosomal proteins Recombinant plasmids pTBal, pTBa7, pTBa8, and pTP10 L23, L2, S19, L22, S3, L16, L14, and S8 has been determined. containing 19.3-, 5.0-, and 4.8-kilobase-pair (kbp) BamHI RNA gel blot hybridization revealed that all eight coding fragments and a 2.9-kbp Pst I fragment ofNicotiana tabacum regions are expressed in the chloroplasts. The arrangement of var. Bright Yellow 4 chloroplast DNA, respectively, were the eight genes resembles that found in the E. coUl S10 and spc constructed as described using pBR322 (ref. 10 and Fig. 1). operons. Among the eight genes, the L2 and L16 genes contain The DNA sequence was determined by a combination of the 666- and 1020-base-pair introns, respectively. These intron chemical method (11) and the dideoxy chain-termination boundary sequences are consistent with the conserved bound- method (12) using mplO/11 and E. coli JM109. DNA se- ary sequences of the chloroplast group m introns [Shinozaki, quences were analyzed using the GENETYX software sys- K., Deno, H., Sugita, M., Kuramitsu, S. & Sugiura, M. (1986) tem (Software Development, Tokyo). RNA gel blot hybrid- Mol. Gen. Genet. 202, 1-5]. ization was carried out as described (13). Chloroplast ribosomes in higher plants are 70S in size and RESULTS contain 23S, 16S, SS, and 4.5S RNAs and =60 ribosomal proteins (1). Analyses of the synthesis of ribosomal proteins DNA Sequence. BamHI digests of tobacco chloroplast in isolated chloroplasts have shown that a chloroplast DNA blotted to nylon filter sheets were hybridized with genome encodes about one-third ofthe ribosomal proteins in nick-translated Xfus3 DNA fragments that carried portions of higher plant species (2, 3). Since the identification and the E. coli S10 and spc operons. The DNA probes hybridized sequencing of the first tobacco chloroplast small subunit strongly to the 5.0-kbp BamHI fragment (Ba7), moderately to ribosomal protein (CS) gene for CS19 (4), several additional the 19.3- and 4.8-kbp BamHI fragments (Bal and Ba8, genes for chloroplast ribosomal proteins located in respectively), and weakly to several other fragments (data chloroplast DNAs have been identified through their homol- not shown). A part of the Ba7 fragment has previously been ogy with Escherichia coli ribosomal protein genes (5-9). sequenced and shown to contain the gene for the ribosomal Because of the success of this approach, we searched for protein CS19 (rps 19 gene product) (4), and thejunction (JLB) further ribosomal protein genes in tobacco chloroplast DNA between the inverted repeat B (IRB) and the large single-copy by hybridization with Afus3 DNA, which contains fourE. coli region (14). ribosomal protein operons (e.g., ref. 25). We sequenced the For the present study, we sequenced the entire Ba7 DNA region that hybridized strongly with the E. coli probe fragment and its adjacent part of the Bal fragment by the and found open reading frames (ORF) whose amino acid strategy shown in Fig. 2. We used the 2.9-kbp Pst I fragment sequences resemble those of E. coli ribosomal proteins. (PslO) to confim that there were no small BamHI pieces Here we describe a gene cluster encoding eight ribosomal between the Bal and Ba7 fragments (see Fig. 1). Fig. 3 shows proteins in tobacco chloroplast DNA. The organization ofthe the DNA sequence of a 6207-bp portion (the left end of Ba7 eight tobacco chloroplast genes is similar to that found in to the Taq I site in S11, see Fig. 2). The Ba8 fragment lies in corresponding order in the E. coli S10 and spc operons. a symmetrical position to Ba7 on the circular chloroplast Nevertheless, two of the above eight genes contain long DNA (see Fig. 1) and has been shown to contain thejunction introns in spite of their homologies with genes encoding the (JLA) between the inverted repeat A (IRA) and the large corresponding E. coli ribosomal proteins. single-copy region, trnH (14), psbA (15), and the 3' exon of trnK (16). We also sequenced the remaining portion (within MATERIALS AND METHODS IRA) of the Ba8 fragment by the same strategy shown in Fig. 2. The 2098-bp sequence (JLA to the first BamHI site) of IRA The transducing phage Xfus3 was kindly provided by K. was found to be completely identical to the corresponding Isono, and its 10 and 4.6% EcoRI fragments that contain parts sequence (JLB to the first BamHI site) of IRB. Determination of the S10 and spc operons of E. coli were used as probes. of the 6207-bp sequence revealed that there is a gene for Southern blot hybridization was performed in 28% (vol/vol) tRNAIIC (details will be published elsewhere) and 11 ORFs on formamide, 1 M NaCl, 10 mM Tris-HCl (pH 7.5), and lx the same DNA strand (strand B). Denhardt's solution at 37°C for 24 hr, and filters were washed Abbreviations: bp, base pairs; CL, chloroplast large subunit ribo- The publication costs of this article were defrayed in part by page charge somal protein: CS, chloroplast small subunit ribosomal protein; payment. This article must therefore be hereby marked "advertisement" ORF, open reading frame. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 6030 Genetics: Tanaka et al. Proc. Natl. Acad. Sci. USA 83 (1986) 6031 LSC sequence, shows 85, 82, and 48% sequence homologies with the deduced N. debneyi CL2, spinach CL2, and E. coli L2 (g proteins, respectively (all protein sequences are deduced from the DNA sequences hereafter). The proteins predicted from ORF1, ORF6, and ORF7 show 23, 26, and 38% sequence homologies with the E. coli L23, L22, and S3 proteins, respectively. In the case ofS3 proteins, several gaps were introduced to maximize the homology. The E. coli S10 operon consists ofthe genes for S10, L3, L4, L23, L2, S19, L22, S3, L16, L29, and S17 in this order (18). The order of ORF1, ORF2-4 (rpl2), ORF5 (rpsl9), ORF6, and ORF7 is the same as that of the S10 operon. Therefore, we propose that ORF1, ORF6, and ORF7 are the genes for the CL23, CL22, and CS3 proteins (rp123, rp122, and rps3), respectively. The deduced polypeptide for ORF9 showed a sequence homology with the E. coli L16 protein. When ORF9 is combined with the short 3-codon ORF (positions 3690-3698) between ORF7 and ORF8 and a 1020-bp insertion is introduced, it is more similar to the E. coli L16 protein (56% homology). We, therefore, propose that the short ORF plus FIG. 1. Positions of the cloned fragments and the genes for the ORF9 is the gene for CL16 (rpll6). The intron sequence was ribosomal proteins on the Sal I cleavage map of tobacco chloroplast assigned to be the positions 3699-4718 by comparing the DNA. The genes for the large subunit of ribulose bisphosphate conserved intron-exon boundary sequences of the chloro- carboxylase (rbcL), the 32-kDa thylakoid membrane protein (psbA), and the rRNA operons (rrnA and rrnB) are marked. JLA and JLB are plast group III introns (9) and the E. coli L16 sequence. The thejunctions between the inverted repeats A and B (IRA and IRB) and intron is 1020 bp long, which is the longest intron so far the large single-copy region (LSC). analyzed in chloroplast genes for proteins. The 80-codon ORF8 is in this intron and showed no homology with any of the E. coli ribosomal proteins nor with ORF3 in the rpl2 Gene Cluster Coding for Proteins Homologous to E. coli intron. Ribosomal Proteins. We have reported the sequence of the The proteins derived from ORF10 and ORF11 have 55 and rpsl9 gene in tobacco chloroplast DNA (4). ORF5 shown 42% (with gaps) sequence homologies with the E. coli L14 here corresponds to rpsl9 (Fig. 3). rpsl9 has been reported and S8 proteins, respectively, suggesting that ORF10 and in spinach (7), Nicotiana debneyi (7), and duckweed (17). The ORF11 are the genes for CL14 and CS8 (rpll4 and rps8). The gene for the chloroplast large subunit ribosomal protein (CL) E. coli spc operon contains the genes for L14, L24, L5, S14, CL2 (rpl2) has been found upstream from rpsl9 in spinach S8, and so on in this order (19). The order of ORF10 (rp1l4) and N. debneyi chloroplast DNAs, and the N. debneyi rpl2 and ORF11 (rps8) is similar to the spc operon when the genes has been found to contain a 666-bp intron (7). Based on their for L24, L5, and S14 are deleted. The gene for CS14 has been high homology with the N. debneyi rpl2, ORF2 and ORF4 found before the tRNAfMet gene in the middle of the large represent the tobacco (N. tabacum) rpl2 that also contains a single-copy region of liverwort chloroplast DNA (8) and 666-bp intron (positions 943-1608).
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