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Bradyrhizobium Sp Proc. Nad. Acad. Sci. USA Vol. 82, pp. 7379-7383, November 1985 Genetics Isolation and characterization of modulation genes from Bradyrhizobium sp. (Vigna) strain IRc 78 (cosmid cloning/TnS mutagenesis/functional complementation) JOHN D. NOTI, BRIGITTA DUDAS* AND ALADAR A. SZALAYt Boyce Thompson Institute for Plant Research at Cornell University, Tower Road, Ithaca, NY 14853 Communicated by H. E. Umbarger, July 8, 1985 ABSTRACT An 11.76-kilobase-pair (kb) segment of DNA slow growers. However, very little has been reported about from Bradyrhizobium sp. (Vigna) strain IRc 78 that hybridizes the structural and functional organization of nod genes in to nodulation genes ofRhizobium meliloti strain 41 was isolated. slow-growing strains. Hybridization of the 11.76-kb DNA fragment to DNA from Whereas the fast-growing Rhizobium species are generally other Bradyrhizobium species revealed a high degree of se- host-specific, the slow-growing Bradyrhizobium species are quence conservation in this region. Transfer of the 11.76-kb promiscuous and can form effective symbioses with a wide segment to nodulation-defective (Nod-) mutants of R. meliloi range of legume hosts (1). Strains of Bradyrhizobium that restored their ability to induce nodules on Medicago saiva infect legumes either by invasion of root hairs or by (alfalfa). Mutants of strain IRc 78 generated by TnS mutagen- apoplastic movement into the root cortex are of particular esis of the 11.76-kb segment fell into three classes according to interest for determining whether the same nodulation genes their symbiotic reaction with Vigna unguiculata (cowpea). are involved in both infection processes. Class I mutants ofstrain IRc 78 were unable to induce root-hair In this paper we describe the identification and cloning of curling or to nodulate; class II induced small, ineffective a region ofDNA from Bradyrhizobium sp. (Vigna) strain IRc nodules; and class III showed delayed and decreased nodula- 78 that can complement the Nod- phenotype of mutant R. tion with reduction in amount of nitrogen fixed. Furthermore, meliloti strains on Medicago sativa (alfalfa). We report that in contrast to the wild-type strain, class I mutants could not TnS mutagenesis ofthis cloned region resulted in the isolation induce nodules on Glycine mar (soybean), Cajanus cajan of mutants affected in either the ability to nodulate or the (pigeon pea), or Arachis hypogaea (peanut). This finding ability to fix nitrogen. We also present evidence that nodula- suggests a common function of the 11.76-kb region in the tion genes essential for the typical root-hair infection mode infection of host plants by Bradyrhizobium either through root are also required for crack entry. This finding suggests that hairs or by "crack entry." nodulation functions are also conserved between different infection mechanisms. The formation of nitrogen-fixing root nodules on legumes by Rhizobium, in general terms, requires the following steps: (i) MATERIALS AND METHODS recognition and invasion ofthe root, (ii) nodule development and differentiation, (iii) multiplication of Rhizobium and Strains and Plasmids. R. meliloti strains 1021 (Fix', str) bacteroid formation, and (iv) expression of nitrogenase (1). (10) and 1027 (Nod-, IsRml::nod str neo) (10) were obtained Infection of most legume species proceeds after the attach- from F. Ausubel. R. meliloti strains 41 (Fix') (6) and ZB157 ment ofRhizobiumn to root hairs, which subsequently curl and (Nod-, Anod) (6) were obtained from A. Kondorosi. B. invaginate to form infection threads. The infection thread japonicum strains 1110, USDA 123, and RCR 3407 (Fix') and grows into the root cortex, branches, and releases the Bradyrhizobium sp. (Vigna) strain IRc 78 (Fix') were pro- bacteria into the cortical cells (2). In Arachis hypogaea vided by A. Eaglesham (Boyce Thompson Institute). The (peanut), however, the bacteria enter the roots in a distinctly Escherichia coli strains used were HB101 (Smr, hsdM- different manner. No infection threads have been found in the hsdR- recA pro leuB6 thi) (11), JA221 (hsdM' hsdR- recA root hairs or the nodules of this species. The bacteria initiate leuB6) (12), NS433(X Eam4 b2 red3 cIts857 Sam7) (13), NS428 infection at the bases of root hairs in the axils of emerging (A Aamll b2 red3 cIts857 Sam7) (13), S605 (thi thr leu supF lateral roots through spaces between epidermal cells and lac met: :TnS, Km9 (14), and SM10 (recA thi thr leu supf lac, subsequently proliferate in intercellular spaces before invad- RP-4-2-Tc::Mu, TRA+) (14). Plasmids pSUP106 (Tcr Cmr ing the cortical cells ("crack entry") (3). Mob+) (14) and pSUP202 (Apr Tcr Cmr) (14) were provided Although the nodulation process is characterized by a high by A. Puhler. Plasmid pEK5121 (6) was provided by A. degree of Rhizobium/legume specificity, nodulation (nod) Kondorosi. genes in several fast-growing Rhizobium species are con- DNA Isolations. Plasmid DNA from E. coli was prepared served in function (4-6) and DNA homology (7, 8). These either on a large scale as described by Hadley and Szalay (15) genes, designated nodABC ("common" nod genes), are or on a small scale as described by Birnboim and Doly (16). required for root-hair curling and are clustered on symbiotic Total DNA from Bradyrhizobium cells was prepared accord- (sym) plasmids linked to genes required for nitrogen fixation ing to Jagadish and Szalay (17). Total DNA for construction (4-6). When DNA fragments from a slow grower, of the gene library was isolated as described by Rosenberg et Bradyrhizobium sp. (parasponia), were introduced into a al. (18). Nod& R. meliloti strain, nodulation ability was restored (9). Construction of Strain IRc 78 Gene Library. Total DNA, This finding indicates that the functional conservation of partially digested with EcoRI, was fractionated by centrifu- some nodgenes in fast-growing strains may also extend to the Abbreviations: kb, kilobase pair(s); Fix, nitrogen fixation; Nod, nodulation. The publication costs of this article were defrayed in part by page charge *Present address: Attila Jozsef University, Department of Genetics, payment. This article must therefore be hereby marked "advertisement" Szeged, Hungary. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 7379 Downloaded by guest on September 25, 2021 7380 Genetics: Nod et al. Proc. Natl. Acad. Sci. USA 82 (1985) gation in 10-40% sucrose gradients to enrich for fractions in as described (17). Activities from M. sativa were determined the size range 20-40 kilobase pairs (kb), as described by from the combined root systems in each DiSPo bottle (5-6 Morris et al. (19). Plasmid pSUP106 was ligated to fraction- roots per jar). ated strain IRc 78 DNA and packaged in vitro (19). E. coli Root-Hair Curling Assay. Root-hair curling assays were transductants containing plasmids were screened by colony done in two ways. In the first method, root-hair curling was hybridization as described by Hanahan and Meselson (20). assayed on seedlings from surface-sterilized seeds germinat- Hybridization Conditions. DNA fragments were twice pu- ed between moist filter papers. The seedlings were inoculated rified from agarose gels (21), labeled with [a-32P]dTTP by after 2 days imbibition and examined by light microscopy 2 nick-translation (22), and hybridized under either high- days later. In the second method, root hairs of seedlings stringency conditions [0.3 M NaCl/0.03 M sodium citrate, pH grown in sand were examined 7, 9, 11, 13, and 16 days after 7/50% (vol/vol) formamide/0.2% Ficoll/0.2% polyvinylpyr- inoculation. rolidone/0.2% bovine serum albumin/0.1% NaDodSO4/ salmon sperm DNA (100 g/ml)] or low-stringency condi- tions (3-fold higher NaCl and sodium citrate concentrations, RESULTS formamide reduced to 33%) at 370C for 18-24 hr. Isolation of a Putative nod Region from Strain IRc 78. An Conjugation Experiments. Plasmid DNA was transferred 8.5-kb EcoRI fragment isolated from pEK5121 (6), a cosmid from E. coli SM10 cells to Rhizobium orBradyrhizobium cells clone containing the nod genes from R. meliloti 41, was as described by Jagadish and Szalay (17). Transconjugants hybridized with EcoRI-digested total DNA from Brady- were selected on plates supplemented with the appropriate rhizobium sp. (Vigna) strain IRc 78 and B. japonicum strains antibiotics as described (17, 23). I110, USDA 123, and RCR 3407 (Fig. lA). Prolonged expo- Site-Directed TnS Mutagenesis. Isolated fragments ofstrain sure (96 hr) of the autoradiogram revealed several major IRc 78 DNA were ligated into pSUP202 made linear with bands and a number of less intense bands of hybridization EcoRI. TnS mutagenesis was performed in E. coli S605 present in the total DNA digests of each strain. When the according to Jagadish and Szalay (17), and the mutated same digests were hybridized to a 3.5-kb BamHI-EcoRI fragments were transferred from E. coli SM10 to strain IRc fragment (6, 7) isolated from the 8.5-kb EcoRI fragment, only 78 and exchanged for the corresponding wild-type DNA by the major bands (arrowheads, Fig. 1A) remained. The 3.5-kb double-reciprocal crossover as described (17). BamHI-EcoRl subfragment contains the nodA, -B, and -C Plant Growth and Isolation of Bacteria from Nodules. The genes (7). Two clones, pJN78-19 and pJN78-24, were isolated procedures described by Jagadish and Szalay (17) were from a cosmid library of strain IRc 78 total DNA probed by followed for all plant-growth experiments with modification colony hybridization with the 3.5-kb BamHI-EcoRI frag- for the growth ofM. sativa. M. sativa seeds were germinated ment. Hybridization ofthe 3.5-kb BamHI-EcoRI fragment to for 5-7 days at 22TC in 6-ounce DiSPo bottles (Scientific EcoRI-digested pJN78-19 and pJN78-24 showed the presence Products) (5-6 seeds per bottle) containing vermiculite and of two bands, at 7.08 kb and 4.68 kb (Fig.
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