Mol Gen Genet (1996) 252:631-639 © Springer-Verlag t996
Victor Kusnetsov • Cordelia Bolle • Thomas Liibberstedt
Sudhir Sopory • Reinhold G. Herrmann • Raif Oelmiiller
Evidence that the plastid signal and light operate via the same cis.acting
elements in the promoters of nuclear genes for plastid proteins
Received: 22 March 1996/Accepted: 28 June 1996
Abstract Nuclear-encoded genes for proteins of the
photosynthetic maschinery represent a particular
subset of genes. Their expression is cooperatively
stimulated by discrete factors including the
developmental stage of plastids and light. We have
analyzed in transgenic tobacco the plastid- and
light-dependent expression of a series of 5' promoter
deletions of various nuclear genes from spinach,
of fusions of defined promoter segments with the
90-bp 35S RNA CaMV minimal promoter, as
well as with mutations in sequences with homologies
to characterized cis-elements, to address the
question of whether the plastid signal and light
operate via the same or different cis-acting ele-
ments. In none of the 160 different transgenic
lines (representing 32 promoter constructs from
seven genes) analyzed, could significant differences
be identified in the responses to the two regula-
tory pathways. The data are compatible with the
idea that both signals control the expression of
nuclear genes for plastid proteins via the same cis-
acting elements.
Key words Gene expression - Light regulation •
Photosynthesis' Plastid signal
Communicated by R. Hagemann
V. Kusnetsov • C. Bolle 1 - T. Ltibberstedt - S. Sopory 2
R. G. Herrmann • R. Oelmiiller (I~)
Botanisches Institut der Ludwig-Maximilians-Universit~it,
Menzingerstrasse 67, D-80638 Munich, Germany
Present address:
1 Rockefeller University Plant Laboratory, 1230 York Avenue,
NY 10021-6399, USA
Permanen~ address:
2 Plant Research Laboratory, School of Life Sciences,
Jawaharlal Nehru University, New Dehli 110 067, India
Introduction
Light is one of the most crucial factors for plant growth
and development (Kendrick and Kronenberg 1994).
Among the most intensively studied effects of this
factor are its influence on the regulation of nuclear gene
transcription (Thompson and White t991; Bowler and
Chua 1994; Terzaghi and Cashmore 1995) and on the
differentiation of etioplasts or proplastids into chloro-
plasts (Herrmann et al. 1992). Microinjection studies in
particular have recently facilitated the identification of
components involved in light-signal transduction
(Neuhaus et al. 1993; Bowler et at. 1994a, b). Light
(phytochrome) activates heterotrimeric G protein(s)
(Ma 1994), which, in turn, appear to trigger three sub-
sequent pathways: one involving cGMP, a second
Ca2+/calmodulin, and a third route that seems to re-
quire both components. Refined studies indicate that
this separation is not strict and that the two pathways
interact considerably (summarized in Barnes et al.
1995). In addition to the stimulation of nuclear gene
expression, injection of phytochrome and non-
hydrolyzable GTP analogs, which activate G proteins,
also stimulate plastid biogenesis (Shacklock et al. 1992;
Neuhaus et al. 1993). Activation of the Ca2+/cal -
modulin pathway alone directs only partial chloroplast
development; complete development of the organetle
also requires the activation of the cGMP-dependent
pathway. The partially developed chloroplasts contain
photosystem II and antenna components, while other
components of the photosynthetic membrane, such as
photosystem I, are missing. In agreement with these
observations, activation of the Ca 2 ÷/calmodulin path-
way alone suffices to stimulate Lhcb gene expression,
while activation of both pathways is required for
the expression of Peril, which encodes the photo-
system I-associated ferredoxin-NADP ÷ oxidoreduc-
tase (Barnes et al. 1995). This suggests a tight coupling
between light-induced developmental processes in the
plastid and the expression of the required nuclear genes.