Mol Gen Genet (1989) 219:289-298
© Springer-Verlag 1989
Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans:
Nucleotide sequence and plant-inducible expression
K. Goethals, M. Gao*, K. Tomekpe**, M. Van Montagu, and M. Holsters
Laboratorium voor Genetica, Rijksuniversiteit Gent, B-9000 Gent, Belgium
Summary. Azorhizobium caulinodans strain ORS571 induces
nitrogen-fixing nodules on roots and stem-located root pri-
mordia of Sesbania rostrata. Two essential Nod loci have
been previously identified in the bacterial genome, one of
which (Nod locus 1) shows weak homology with the com-
mon nodC gene of Rhizobium meliloti. Here we present the
nucleotide sequence of this region and show that it contains
three contiguous open reading frames (ORFA, ORFB and
ORFC) that are related to the nodABC genes of Rhizobium
and Bradyrhizobium species. ORFC is followed by a fourth
(ORF4) and probably a fifth (ORF5) open reading frame.
ORF4 may be analogous to the nodI gene of R. legumino-
sarum, whereas ORF5 could be similar to the rhizobial nodF
genes. Coordinated expression of this set of five genes seems
likely from the sequence organization. There is no typical
nod promoter consensus sequence (nod box) in the region
upstream of the first gene (ORFA) and there is no nodD-like
gene. LacZ fusions constructed with ORFA, ORFB,
ORFC, and ORF4 showed inducible /~-galactosidase ex-
pression in the presence of S. rostrata seedlings as well
as around stem-located root primordia. Among a series of
phenolic compounds tested, the flavanone naringenin was
the most efficient inducer of the expression of this ORS571
nod gene cluster.
Key words: Azorhizobium caulinodans - Common nod genes
DNA sequencing - Plant-inducible expression - Sesbania
rostrata nodulation
Introduction
Bacteria belonging to the genera Rhizobium and Bradyrhizo-
bium can cause the formation of nitrogen-fixing nodules
on the roots of several leguminous plants. During the last
decade a considerable amount of information has been
gained on the bacterial genes that are important for the
interaction with the plant (for recent reviews, see Djordjevic
et al. 1987; Long 1989). Large Sym plasmids in rhizobia
and the chromosome of bradyrhizobia have been shown
to carry gene clusters that are involved in nodule induction
* Present address: Institute for Application of Atomic Energy, P.O.
Box 5109, Beijing, China
** Present address: Laboratoire de Biologie des Sols,
O.R.S.T.O.M., P.B. 1386, Dakar, S6n6gal
Offprint requests to: M. Holsters
(nod genes). Three major types of nod genes have been iden-
tified. The "common nod" genes are functionally and struc-
turally conserved among all rhizobia and bradyrhizobia
thus far studied. Although their exact biochemical role has
not yet been elucidated, strong evidence has been obtained
that the common nodA and nodB genes are essential for
the production of a bacterial factor that can induce plant
meristem formation, whereas the common nodC gene codes
for an outer membrane protein that may function in signal
exchange between bacteria and plant cells (John et al. 1988;
Schmidt et al. 1988). The "host specificity" (hsn) genes
function in determining the host range of a particular bacte-
rial strain. Finally, the nodD genes encode regulatory pro-
teins that in conjunction with plant-derived phenolic com-
pounds - activate the transcription of the other nod operons
(Mulligan and Long 1985; Rossen etal. 1985; Horvath
et al. 1987). This transcriptional activation requires the
presence of strongly conserved eis-acfing regulatory se-
quences (nod boxes) upstream from the inducible nod genes
(Rostas et al. 1986; Fisher et al. 1988).
More recently, a novel bacterium, Azorhizobium caulino-
dans gen. nov., sp. nov. strain ORS571, has been isolated
from aerial nodules on the stem of the tropical leguminous
plant Sesbania rostrata (Dreyfus et al. 1984, 1988). This
strain differs from Bradyrhizobium and Rhizobium species
by its taxonomic position and its unique capacity for both
symbiotic and free-living nitrogen fixation. A. caulinodans
induces effective nodules on the roots of its host and also
on the stem, at the sites of dormant root primordia, the
abundant occurrence of which is a characteristic feature
of the S. rostrata species. We are interested in this particular
symbiosis and have focused on the identification of bacteri-
al genes involved in early interactions with the host. In
a previous paper we have described the cloning of two
ORS571 genomic loci that are essential for root and stem
nodulation (Van den Eede et al. 1987). One of these (Nod
locus 1) shows weak homology with the nodC gene of R.
meliloti. Here, we report the further characterization of Nod
locus 1. By DNA sequencing and laeZ-mediated expression
studies we show the presence of genes related to the com-
mon nodABC genes of Rhizobium and Bradyrhizobium.
These A. eaulinodans genes seem to be organized in one
operon together with a nodI-like and, unexpectedly, a nodF-
like cistron. In all cases studied thus far, nodF has been
described as the first gene of an hsn operon further contain-
ing the nodE gene (Shearman et al. 1986; Schofield and
Watson 1986; Debell6 and Sharma 1986). The expression