Current Biology, Vol. 12, 1557–1565, September 17, 2002, 2002 Elsevier Science Ltd. All rights reserved. PII S0960-9822(02)01125-9
The Gibberellin Pathway Mediates
KNOTTED1-Type Homeobox Function
in Plants with Different Body Plans
mato leaf and implicate this interaction in regulation of
the dissected leaf form.
Conclusions: We suggest that repression of GA activity
by KNOX transcription factors is a key component of
meristem function. Transfer of the KNOX/GA regulatory
Angela Hay,
1
Hardip Kaur,
2
Andrew Phillips,
3
Peter Hedden,
3
Sarah Hake,
1,4
and Miltos Tsiantis
2,5
1
Plant and Microbial Biology Department
University of California, Berkeley
Berkeley, California 94720 module from the meristem to the leaf may have contrib-
uted to the generation of the diverse leaf morphologies
2
Plant Sciences Department
University of Oxford observed in higher plants.
South Parks Road
Oxford OX1 3RB
Introduction
United Kingdom
3
Long Ashton Research Station
In Arabidopsis, two KNOX genes, STM and KNAT1
Department of Agricultural Sciences
(KNOTTED1-LIKE in ARABIDOPSIS THALIANA1), are
University of Bristol
expressed in partially overlapping domains of the SAM.
Bristol BS41 9AF
Transcripts for both genes, however, are excluded from
United Kingdom
incipient leaf primordia, leading to the hypothesis that
4
Plant Gene Expression Center
KNOX gene products are required for meristem function,
United States Department of Agriculture
whereas their absence is required for leaf initiation [1, 2].
Agricultural Research Service
Genetic evidence supports this hypothesis; loss-of-
800 Buchanan Street
function mutations in STM result in a failure to initiate
Albany, California 94710
or maintain a SAM [2]. Double mutant analysis between
weak stm alleles and the KNAT1 loss of function muta-
tion brevipedicellus (bp) demonstrates that KNAT1 as-
sumes a redundant role with STM in the SAM [3]. Con-
Summary
versely, ectopic expression of KNAT1 results in the
formation of meristems on leaves and the alteration of
Background: The shoot apical meristem (SAM) is an
leaf shape [1, 4]. Ectopic expression of STM results in
indeterminate structure that gives rise to the aerial parts
meristem formation on the adaxial surface of the cotyle-
of higher plants. Leaves arise from the differentiation of
dons and growth arrest [5].
cells at the flanks of the SAM. Current evidence suggests
Recent data suggest that certain KNOX misexpres-
that the precise regulation of KNOTTED1-like homeobox
sion phenotypes may be mediated by growth regulators.
(KNOX) transcription factors is central to the acquisition
Ectopic expression of KNOX genes from a number of
of leaf versus meristem identity in a wide spectrum of
species results in reduced GA levels [6, 7]. In tobacco the
plant species. Factors required to repress KNOX gene
KNOX protein NTH15 directly represses transcription of
expression in leaves have recently been identified. Addi-
Ntc12, a gene encoding a GA 20-oxidase required for GA
tional factors such as the CHD3 chromatin remodeling
biosynthesis [8]. Also, plants with increased cytokinin
factor PICKLE (PKL) act to restrict meristematic activity
levels are partially phenocopied by KNOX misexpres-
in Arabidopsis leaves without repressing KNOX gene
sion, and cytokinin levels increase in response to regu-
expression. Less is known regarding downstream tar-
lated misexpression of the maize KNOX gene KN1 in
gets of KNOX function. Recent evidence, however, has
tobacco leaves [9–11].
suggested that growth regulators may mediate KNOX
In contrast to the simple leaves of species such as
activity in a variety of plant species.
Arabidopsis and tobacco, the dissected leaves of to-
Results: Here we show that reduced activity of the gib-
mato plants express KNOX genes. This expression pat-
berellin (GA) growth regulator pathway promotes meri-
tern, combined with the increased leaf dissection ob-
stematic activity, both in the natural context of KNOX
tained by overexpression of KNOX genes in tomato, has
function in the SAM and upon ectopic KNOX expression
led to the suggestion that differential regulation of KNOX
in Arabidopsis leaves. We show that constitutive signal-
genes is involved in the generation of dissected leaf
ing through the GA pathway is detrimental to meristem
morphology [12, 13]. This idea has been reinforced by
maintenance. Furthermore, we provide evidence that
a recent study demonstrating that KNOX expression
one of the functions of the KNOX protein SHOOTMERI-
early in leaf development correlates with the generation
STEMLESS (STM) is to exclude transcription of the GA-
of a complex leaf body plan across a broad spectrum
biosynthesis gene AtGA20ox1 from the SAM. We also
of vascular plants [14].
demonstrate that AtGA20ox1 transcript is reduced in
Here we show that a reduction in GA signaling or
the pkl mutant in a KNOX-independent manner. More-
biosynthesis promotes KNOX-dependent ectopic meri-
over, we show a similar interaction between KNOX pro-
stematic activity in Arabidopsis leaves. Conversely, ele-
teins and GA-biosynthesis gene expression in the to-
vated GA signaling antagonizes KNOX function both
upon ectopic expression in leaves and in the natural
domain of KNOX expression in the SAM. We also dem-
5
Correspondence: miltos.tsiantis@plant-sciences.oxford.ac.uk