Mol Gen Genet (1983) 191:10-16
© Springer-Verlag 1983
A Functional Map of the Nopaline Catabolism Genes
on the Ti Plasmid of Agrobacterium tumefaciens C58
C.L. Schardl* and C.I. Kado
Davis Crown Gall Group, Department of Plant Pathology, University of California, Davis, CA 956/6, USA
Summary. The nopaline catabolism (noc) genes are located
in a 14.4 kb region on the pTiC58 plasmid ofA. tumefaciens
C58. These genes permit the bacterium to grow on nopaline
NZ-(1,3-dicarboxylpropyl) arginine, a substrate produced
in plant tumors initiated by strain C58. The functions of
the noc genes include the use of nopaline and L-ornithine
as sole carbon and nitrogen sources. Using Tn5 insertional
mutants, we have identified and mapped the positions of
the genes that are responsible for nopaline catabolism
(NopC), ornithine catabolism (OrnC) and nopaline uptake
(NopU). A polar relationship was found between these
phenotypes, which extended leftward over the noc region
to the T-region. The NopC mutants were also deficient
in nopaline oxidase, an enzyme that liberates free arginine
from nopaline.
The noc region also encodes the synthesis of a periplas-
mic protein, nl that was induced by nopaline. Tn5 inser-
tional mutations and molecular cloning were used to map
the nl production locus. The recombinant plasmids,
pSa4480 and pSa4481, containing the 8.9 kb right-hand end
of the noc region, conferred nl production when introduced
into a pTi-free strain of A. tumefaciens.' Production of nl
by the strains carrying these plasmids required nopaline
induction.
We have identified in toto three noc loci: nocB, nocC,
and nocA, which confer nl production, nopaline oxidase
production and ornithine catabolism respectively. A model
is proposed whereby the noc genes of pTiC58 are contained
on a leftward reading operon in the order nocB, nocC, and
nocA.
Introduction
Crown gall tumor induction requires the presence of the
tumor-inducing plasmid (pTi) in A. tumefaciens. A segment
of pTi called the T-region is transferred to the plant host
genome apparently as part of the crown gall tumor forma-
tion process (Chilton et al. 1977). Several research groups
have identified T-region genes that encode the production
of opines such as nopaline and octopine in transformed
plant cells. Nopaline-type Ti plasmids, such as pTiC58, con-
tain genes for both the synthesis and degradation of nopa-
* Present address. Plant Breeding Institute, Marls Lane, Trump-
ington, Cambridge CB2 2LQ, UK
Offprint requests to: C.I. Kado
line (Bomhoffet al. 1976). The nopaline synthesis (nos) gene
is contained on the T-region and functions in the plant
cell (Holsters et al. 1980). The nopaline catabolism (noc)
genes, which map adjacently to the right of the T-region
of pTiC58 (Holsters et al. 1980), also confer ornithine ca-
tabolism on the bacterium (Ellis et al. 1979). The noc genes
allow the bacterium to use these substrates as sole nitrogen
and carbon sources in vitro and, presumably, in the crown
gall tumor.
The analogous octopine N2-(1-carboxyethyl) arginine
catabolism (occ) system has been partly characterized. Oc-
topine uptake is induced by octopine in strain A. tumefa-
ciens B6S3 (Klapwijk et al. 1977). Arginine and glutamate
are intermediates of octopine catabolism (Petit et al. 1970.
Klapwijk et al. (1978) and Bomhoff (1974) have described
an octopine oxidase, which degrades octopine to arginine
and pyruvate. A related activity, lysopine oxidase, has also
been described (Jubier 1975).
In this paper we have identified and mapped the pheno-
types of the pTiC58 noc-region, which includes nopaline
uptake (NopU), utilization of nopaline as a carbon source
(NopC), or as a nitrogen source (NopN) and ornithine cata-
bolism (OrnC). In addition, nopaline oxidase (Nox) and
an inducible periplasmic protein nl were found to be en-
coded by this region. We present evidence that the loci
affecting these phenotypes are contained on a single operon.
Materials and Methods
Chemicals. [3H]-nopaline, labeled in the arginine moiety,
was prepared by the method of J. Temp6 (personal commu-
nication) and Bomhoff (1974). Crown gall tobacco callus
tissue samples, designated CG-1CTer and originally ob-
tained from Milton Gordon, were placed onto fresh MS
agar without hormones (Murashige and Skoog 1962) and
grown for 3 weeks in the dark at room temperature. One
mCi [3H]-L-arginine (sp. act. > 300 mCi/mmol, New En-
gland Nuclear) was added to each tissue sample and further
incubated for 2 days. The tissues were ground in 60% etha-
nol yielding an extract that was filtered and concentrated
by flash evaporation at 50 ° C. Nopaline was separated from
arginine by preparative electrophoresis (Liu and Kado
1979). The product was quantified by a diacetyl method
(Bomhoff et al. 1976).
Unlabeled nopaline was chemically synthesized by the
method of Jensen et al. (1977) with slight modifications as
follows: After cyanoborohydride reduction, the reaction