Mol Gen Genet (1994) 244:391400 © Springer-Verlag1994
P. Gallusci • F. Salamini • R. D. Thompson
Differences in cell type-specific expression of the gene Opaque2
in maize and transgenic tobacco
Received: 16 November 1993 / Accepted: 15 February 1994
Abstract The Opaque 2 (02) gene encodes a transcrip-
tional activator of the basic region/leucine zipper fami-
ly, which controls the synthesis of a major storage
protein class in maize endosperm, the 22 kDa ~-zeins,
and of several other non-zein polypeptides including
b32. We demonstrate, by analysing 02 mRNAs in differ-
ent organs of maize plants, that the 02 gene is only
active in the endosperm. Its transcription is precisely
controlled during seed development: 02 mRNAs are
first detected 10 days after pollination and accumulate
in the endosperm over a period of 20 days. When intro-
duced into tobacco plants, the 02 promoter directs the
expression of the 13-glucuronidase (GUS) reporter gene
in endosperm, but also in the embryo, cotyledons and
pollen. The first 185 bp of the 02 promoter is sufficient
for developmentally regulated expression in tobacco
seeds. A distinct cis-acting element, located between po-
sitions -185 and -520, directs expression in the
cotyledons of tobacco seedlings. The possible origins of
this breakdown in promoter specificity in the het-
erologous host are discussed.
Key words Opaque2 • Maize endosperm • Transgenic
tobacco • Promoter
Introduction
Zeins, the major seed storage proteins of maize, are al-
cohol-soluble proteins that accumulate in the en-
dosperm during seed maturation. The most abundant
zeins have molecular weights of 20-22 kDa (~-zeins),
and are encoded by a large multigene family comprising
about 100 genes (Hagen and Rubenstein 1981; Wilson
and Larkins 1984). Zein gene expression is tissue specif-
Communicated by J. Schell
P. Gallusci • F. Salamini - R.D. Thompson ([~)
Max-Planck-Institut ffir Ziichtungsforschung,
Carl-von-Linn~-Weg 10, D-50829 K61n, Germany
ically and developmentally controlled, and occurs in the
endosperm between 10 and 45 days after pollination
(Murphy and Dalby 1971). Several mutants affect speci-
fically either the accumulation of one group of a-zeins,
such as opaque 7 and opaque 2, or of all ~-zeins, such as
opaque 6 andfloury 2 (for review see Motto et al. 1989).
The opaque 2 (o2) mutation reduces the accumula-
tion of the 22 kDa zeins (Jones et al. 1977a, b), by lower-
ing the rate of transcription of the corresponding genes
(Kodrzycki et al. 1989). The mutation also affects the
accumulation of a few other non-zein polypeptides, in-
cluding the b32 protein (Soave and Tardani 1981),
which is an endosperm-specific ribosome-inactivating
protein (Bass et al. 1992). The 02 gene has been cloned
(Schmidt et al. 1987; Motto et al. 1988) and shown to
encode a transcriptional activator of the basic domain/
leucine zipper family (Hartings etal. 1989; Schmidt
et al. 1990). In transient expression assays, the 02
protein activates transcription from the b32 gene pro-
moter (Lohmer et al. 1991) and from a 22 kDa zein pro-
moter (Ueda et al. 1992), most probably by interacting
with specific binding sites (Lohmer et al. 1991 ; Schmidt
et al. 1992). However, additional proteins may be re-
quired for the activation in vivo of the zein and b32
promoters (Pysh et al. 1993). The 02 gene product does
not influence cell-type determination but enhances the
expression of a set of genes in a very specific type of cells.
Therefore, the transcription of the 02 gene must be pre-
ceded by a series of developmental decisions leading to
formation of distinct cell types of the triploid endosperm
lineage, such as the aleurone, subaleurone and central
endosperm cells. To identify factors involved in early
steps of endosperm development, a study of mecha-
nisms controlling the transcription of the 02 gene was
initiated.
The functional analysis of maize gene promoters is
difficult due to the lack of a routine transformation sys-
tem for this species. To circumvent this problem, tran-
sient expression systems based on endosperm cell cul-
tures have been proposed and adopted (Ueda and Mess-
ing 1991; Manzocchi et al. 1989). In these cell cultures,