Mol Gen Genet (2992) 235:389-396
© Springer-Verlag 1992
Effect of T-DNA configuration on transgene expression
Peter Breyne, Godelieve Gheysen, Anni Jacobs, Marc Van Montagu, and Ann Depicker
Laboratorium voor Genetica, UniversiteitGent, K.L. Ledeganckstraat35, B-9000 Gent, Belgium
Received May 13, 1992 / AcceptedJune 12, 1992
Summary. T-DNA vectors were constructed which carry
a /~-glucuronidase (gusA) gene fused to the promoter
of the nopaline synthase (nos) gene and the 3' end of
the octopine synthase (ocs) gene. This reporter gene was
cloned at different locations and orientations towards
the right T-DNA border. For each construct, between
30 and 60 stably transformed calli were analysed for
/?-glucuronidase activity. Depending on the T-DNA con-
figuration, distinct populations of gusA-expressing calli
were obtained. Placing the reporter gene in the middle
of the T-DNA results in relatively low expression levels
and a limited inter-transformant variability. Placing the
gene with its promoter next to the right border led to
an increase in both the mean activity and the variability
level. With this construct, some of the calli expressed
the gusA gene at levels four to five times higher than
the mean. In all these series, at least 30% of the calli
contained reporter gene activities that were less than
half of the mean expression level. Separating the gusA
gene from the right T-DNA border by an additional
3'-untranslated region, derived from the nos gene, re-
sulted in an increase in the mean expression to a level
almost four times higher than that of constructions car-
rying the reporter gene in the middle of the T-DNA.
Moreover, the number of transformants with extremely
low activities decreased by at least 50% and this resulted
in significantly lower inter-transformant variability inde-
pendently of the orientation of the reporter gene on the
T-DNA.
Key words: Agrobacterium tumefaciens - Inter-transfor-
mant variability - Nicotiana tabacum - Position effect
- Transcription interference
Introduction
Agrobacterium-mediated plant cell transformation usu-
ally results in the stable integration of one or a few
Correspondence to : M. Van Montagu
copies of a well-defined T-DNA region (reviewed in
Gheysen et al. 1989). Most often, the expression pattern
of the transgenes that are in the plant genome is qualita-
tively correct (e.g. Okamuro et al. 1986; Bogusz et al.
1990). However, the quantitative expression levels can
vary widely between independent transformants (Dean
et al. 1988; Gendloff et al. 1990; Peach and Velten 1991)
and there is usually no positive correlation between the
T-DNA copy number and the expression level of the
transgenes, when limited numbers of individual transfor-
mants are compared (e.g. Odell et al. 1987; Shirsat et al.
1989; Gendloff et al. 1990; Hobbs et al. 1990).
Inter-transformant variability may be caused by sev-
eral molecular and genetic phenomena: the T-DNA that
enters the plant nucleus upon transformation lacks a
predetermined chromatin structure and DNA modifica-
tion pattern; random methylation (reviewed by Selker
1990), mutation, rearrangements (Gheysen et al. 1990)
or interactions with host cell factors, occurring prior
to, during or after integration might greatly influence
the expression of the transgene, independently of the
site of insertion (discussed in Peach and Velten 1991).
On the other hand, however, inter-transformant vari-
ability is explained in many cases by position effects:
transgene expression will be variably affected by the
structural and functional properties of the chromatin
region flanking the T-DNA integration site. Firstly, the
local chromatin structure and modification pattern of
the flanking DNA can determine the state of the inte-
grated T-DNA (e.g. Coates et al. 1987; Peerbolte et al.
1986). Secondly, the higher-order chromatin structure
of the region surrounding the integration site might in-
fluence gene expression. Since eukaryotic DNA seems
to be organized in looped domains, which function as
independent genomic units (Eissenberg and Elgin 1991),
the specific loop in which the T-DNA has inserted may
partially determine the DNA structure and the overall
expression level of the present genes. Thirdly, transgene
expression can be influenced directly by neighbouring
plant regulatory sequences; it is thought that the T-
DNA preferentially integrates in transcribed DNA re-