Abstract
The genome of the nitrogen-fixing symbiont, Rhizobium fredii USDA257, contains nine copies of repetitive sequences known as the R. fredii repetitive sequence (RFRS) family. We previously sequenced RFRS3, which is linked to symbiosis plasmid-borne nodulation genes of this organism and has substantial homology to the T-DNA of Agrobacterium rhizogenes and lesser homology to reiterated sequences of Bradyrhizobium japonicum. Here we characterize a second family member, RFRS9. The EcoRI fragment containing RFRS9 is 1,248 bp in length and contains a single 666-bp open reading frame that is flanked by perfect 8-bp inverted repeats. Nucleic and amino acid sequences corresponding to the C terminus of the putative RFRS9 protein are nearly identical to those of RFRS3, and they retain homology to DNA from A. rhizogenes. The central portion of the RFRS9 protein also appears to be related to the S locus-specific glycoprotein family of pollen stigma incompatibility glycoproteins from Brassica oleracea, which are involved in signal perception. Sequences that define the RFRS family are restricted to the open reading frame of RFRS9 and associated upstream sequences. These regions also contain a second group of repetitive sequences, which is present in four copies within the genome of USDA257. Both families of repetitive sequences are ubiquitous in R. fredii, and they are preferentially localized on symbiosis plasmids. Southern hybridization confirms that sequences homologous to RFRS9 are present in broad-host-range Rhizobium sp. strain NGR234, in A. rhizogenes, and in two biotype 3 strains of Agrobacterium tumefaciens.
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- Better M., Lewis B., Corbin D., Ditta G., Helinski D. R. Structural relationships among Rhizobium meliloti symbiotic promoters. Cell. 1983 Dec;35(2 Pt 1):479–485. doi: 10.1016/0092-8674(83)90181-2. [DOI] [PubMed] [Google Scholar]
- Dusha I., Kovalenko S., Banfalvi Z., Kondorosi A. Rhizobium meliloti insertion element ISRm2 and its use for identification of the fixX gene. J Bacteriol. 1987 Apr;169(4):1403–1409. doi: 10.1128/jb.169.4.1403-1409.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flores M., González V., Brom S., Martínez E., Piñero D., Romero D., Dávila G., Palacios R. Reiterated DNA sequences in Rhizobium and Agrobacterium spp. J Bacteriol. 1987 Dec;169(12):5782–5788. doi: 10.1128/jb.169.12.5782-5788.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gay P., Le Coq D., Steinmetz M., Berkelman T., Kado C. I. Positive selection procedure for entrapment of insertion sequence elements in gram-negative bacteria. J Bacteriol. 1985 Nov;164(2):918–921. doi: 10.1128/jb.164.2.918-921.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Györgypal Z., Kiss G. B., Kondorosi A. Transduction of plant signal molecules by the Rhizobium NodD proteins. Bioessays. 1991 Nov;13(11):575–581. doi: 10.1002/bies.950131106. [DOI] [PubMed] [Google Scholar]
- Hahn M., Hennecke H. Conservation of a symbiotic DNA region in soybean root nodule bacteria. Appl Environ Microbiol. 1987 Sep;53(9):2253–2255. doi: 10.1128/aem.53.9.2253-2255.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hahn M., Hennecke H. Mapping of a Bradyrhizobium japonicum DNA Region Carrying Genes for Symbiosis and an Asymmetric Accumulation of Reiterated Sequences. Appl Environ Microbiol. 1987 Sep;53(9):2247–2252. doi: 10.1128/aem.53.9.2247-2252.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heron D. S., Pueppke S. G. Mode of infection, nodulation specificity, and indigenous plasmids of 11 fast-growing Rhizobium japonicum strains. J Bacteriol. 1984 Dec;160(3):1061–1066. doi: 10.1128/jb.160.3.1061-1066.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jarvis B. D., Downer H. L., Young J. P. Phylogeny of fast-growing soybean-nodulating rhizobia support synonymy of Sinorhizobium and Rhizobium and assignment to Rhizobium fredii. Int J Syst Bacteriol. 1992 Jan;42(1):93–96. doi: 10.1099/00207713-42-1-93. [DOI] [PubMed] [Google Scholar]
- Kaluza K., Hahn M., Hennecke H. Repeated sequences similar to insertion elements clustered around the nif region of the Rhizobium japonicum genome. J Bacteriol. 1985 May;162(2):535–542. doi: 10.1128/jb.162.2.535-542.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krishnan H. B., Pueppke S. G. Repetitive sequences with homology to Bradyrhizobium japonicum DNA and the T-DNA of Agrobacterium rhizogenes are closely linked to nodABC of Rhizobium fredii USDA257. Mol Plant Microbe Interact. 1991 Sep-Oct;4(5):521–529. doi: 10.1094/mpmi-4-521. [DOI] [PubMed] [Google Scholar]
- Krishnan H. B., Pueppke S. G. Sequence and analysis of the nodABC region of Rhizobium fredii USDA257, a nitrogen-fixing symbiont of soybean and other legumes. Mol Plant Microbe Interact. 1991 Sep-Oct;4(5):512–520. doi: 10.1094/mpmi-4-512. [DOI] [PubMed] [Google Scholar]
- Masterson R. V., Atherly A. G. The presence of repeated DNA sequences and a partial restriction map of the pSym of Rhizobium fredii USDA193. Plasmid. 1986 Jul;16(1):37–44. doi: 10.1016/0147-619x(86)90077-6. [DOI] [PubMed] [Google Scholar]
- Ogawa J., Brierley H. L., Long S. R. Analysis of Rhizobium meliloti nodulation mutant WL131: novel insertion sequence ISRm3 in nodG and altered nodH protein product. J Bacteriol. 1991 May;173(10):3060–3065. doi: 10.1128/jb.173.10.3060-3065.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otten L., Canaday J., Gérard J. C., Fournier P., Crouzet P., Paulus F. Evolution of agrobacteria and their Ti plasmids--a review. Mol Plant Microbe Interact. 1992 Jul-Aug;5(4):279–287. doi: 10.1094/mpmi-5-279. [DOI] [PubMed] [Google Scholar]
- Panagopoulos C. G., Psallidas P. G. Characteristics of Greek Isolates of Agrobacterium tumefaciens (E. F. Smith & Townsend) Conn. J Appl Bacteriol. 1973 Jun;36(2):233–240. doi: 10.1111/j.1365-2672.1973.tb04096.x. [DOI] [PubMed] [Google Scholar]
- Perret X., Broughton W. J., Brenner S. Canonical ordered cosmid library of the symbiotic plasmid of Rhizobium species NGR234. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1923–1927. doi: 10.1073/pnas.88.5.1923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pomponi M., Spanò L., Sabbadini M. G., Costantino P. Restriction endonuclease mapping of the root-inducing plasmid of Agrobacterium rhizogenes 1855. Plasmid. 1983 Sep;10(2):119–129. doi: 10.1016/0147-619x(83)90064-1. [DOI] [PubMed] [Google Scholar]
- Ramakrishnan N., Prakash R. K., Shantharam S., Duteau N. M., Atherly A. G. Molecular cloning and expression of Rhizobium fredii USDA 193 nodulation genes: extension of host range for nodulation. J Bacteriol. 1986 Dec;168(3):1087–1095. doi: 10.1128/jb.168.3.1087-1095.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ramseier T. M., Göttfert M. Codon usage and G + C content in Bradyrhizobium japonicum genes are not uniform. Arch Microbiol. 1991;156(4):270–276. doi: 10.1007/BF00262997. [DOI] [PubMed] [Google Scholar]
- Renalier M. H., Batut J., Ghai J., Terzaghi B., Gherardi M., David M., Garnerone A. M., Vasse J., Truchet G., Huguet T. A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol. 1987 May;169(5):2231–2238. doi: 10.1128/jb.169.5.2231-2238.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Risuleo G., Battistoni P., Costantino P. Regions of homology between tumorigenic plasmids from Agrobacterium rhizogenes and Agrobacterium tumefaciens. Plasmid. 1982 Jan;7(1):45–51. doi: 10.1016/0147-619x(82)90025-7. [DOI] [PubMed] [Google Scholar]
- Rodriguez-Quiñones F., Judd A. K., Sadowsky M. J., Liu R. L., Cregan P. B. Hyperreiterated DNA regions are conserved among Bradyrhizobium japonicum serocluster 123 strains. Appl Environ Microbiol. 1992 Jun;58(6):1878–1885. doi: 10.1128/aem.58.6.1878-1885.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruvkun G. B., Long S. R., Meade H. M., van den Bos R. C., Ausubel F. M. ISRm1: A Rhizobium meliloti insertion sequence that transposes preferentially into nitrogen fixation genes. J Mol Appl Genet. 1982;1(5):405–418. [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwedock J., Long S. R. Nucleotide sequence and protein products of two new nodulation genes of Rhizobium meliloti, nodP and nodQ. Mol Plant Microbe Interact. 1989 Jul-Aug;2(4):181–194. doi: 10.1094/mpmi-2-181. [DOI] [PubMed] [Google Scholar]
- Slightom J. L., Durand-Tardif M., Jouanin L., Tepfer D. Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid. Identification of open reading frames. J Biol Chem. 1986 Jan 5;261(1):108–121. [PubMed] [Google Scholar]
- Vanderleyden J., Desair J., De Meirsman C., Michiels K., Van Gool A. P., Chilton M. D., Jen G. C. Nucleotide sequence of an insertion sequence (IS) element identified in the T-DNA region of a spontaneous variant of the Ti-plasmid pTiT37. Nucleic Acids Res. 1986 Aug 26;14(16):6699–6709. doi: 10.1093/nar/14.16.6699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker J. C., Zhang R. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature. 1990 Jun 21;345(6277):743–746. doi: 10.1038/345743a0. [DOI] [PubMed] [Google Scholar]
- Wheatcroft R., Laberge S. Identification and nucleotide sequence of Rhizobium meliloti insertion sequence ISRm3: similarity between the putative transposase encoded by ISRm3 and those encoded by Staphylococcus aureus IS256 and Thiobacillus ferrooxidans IST2. J Bacteriol. 1991 Apr;173(8):2530–2538. doi: 10.1128/jb.173.8.2530-2538.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wheatcroft R., Watson R. J. Distribution of insertion sequence ISRm1 in Rhizobium meliloti and other gram-negative bacteria. J Gen Microbiol. 1988 Jan;134(1):113–121. doi: 10.1099/00221287-134-1-113. [DOI] [PubMed] [Google Scholar]
- White F. F., Nester E. W. Relationship of plasmids responsible for hairy root and crown gall tumorigenicity. J Bacteriol. 1980 Nov;144(2):710–720. doi: 10.1128/jb.144.2.710-720.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Bruijn F. J. Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol. 1992 Jul;58(7):2180–2187. doi: 10.1128/aem.58.7.2180-2187.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]