Current Biology, Vol. 13, 627–637, April 15, 2003, 2003 Elsevier Science Ltd. All rights reserved. DOI 10.1016/S0960-9822 ( 0 3 )0024 3 - 4
ATX-1, an Arabidopsis Homolog of Trithorax,
Activates Flower Homeotic Genes
transiently expressed transcription factors. Later, most
of these factors cease to be expressed, but the activity
of genes established at the initial stage is faithfully prop-
Raul Alvarez-Venegas,
1
Stephane Pien,
2,4
Monther Sadder,
1,5
Xiaohong Witmer,
3
Ueli Grossniklaus,
2
and Zoya Avramova
1,
*
1
School of Biological Sciences
agated during subsequent cellular divisions. This is
University of Nebraska, Lincoln
achieved through the activity of genes belonging to two
Lincoln, Nebraska 68588-0118
families of antagonistically acting regulators, proteins
2
Institute of Plant Biology
of the trithorax group (trxG) and the Polycomb group
University of Zu
¨
rich
(PcG), implicated in activating and repressing functions,
CH-8008 Zu
¨
rich
respectively. The product of the Drosophila trx gene
Switzerland
has been identified genetically as a positive regulator
3
Department of Pathology and Laboratory Medicine
of homeotic genes [1], and the mammalian homolog,
University of Pennsylvania
MLL (ALL-1), positively regulates the clustered Hox
Philadelphia, Pennsylvania 19104-4283
genes [2]. In animals, trxG and PcG proteins are involved
in regulating homeotic genes as well as genes involved
in cell proliferation and growth (reviewed in [3]).
Summary
In plants, the lateral organs (leaves), the reproductive
organs (flowers), and the seeds originate from the same
Background: The genes of the trithorax (trxG) and Poly-
undifferentiated meristem that is active throughout the
comb groups (PcG) are best known for their regulatory
life cycle [4, 5]. Because organ development in plants
functions in Drosophila, where they control homeotic
is not restricted to the embryonic stage and because
gene expression. Plants and animals are thought to have
differentiation and organogenesis occur throughout the
evolved multicellularity independently. Although ho-
life span of the organism, it was not anticipated that
meotic genes control organ identity in both animals and
genes of either the trxG or PcG would be involved in
plants, they are unrelated. Despite this fact, several plant
developmental decisions in plants. However, the discov-
homeotic genes are negatively regulated by plant genes
ery of several Arabidopsis genes with similarity to animal
similar to the repressors from the animal PcG. However,
regulators of the PcG challenged this view. For instance,
plant-activating regulators of the trxG have not been
CURLY LEAF (CLF) encodes a repressor of the flower
characterized.
homeotic gene AG [6], MEDEA (MEA), FERTILIZATION
Results: We provide genetic, molecular, functional, and
INDEPENDENT ENDOSPERM (FIE), and FERTILIZA-
biochemical evidence that an Arabidopsis gene, ATX1,
TION-INDEPENDENT SEED2 (FIS2) encode maternally
which is similar to the Drosophila trx, regulates floral
acting factors regulating seed development [7–10], while
organ development. The effects are specific: structurally
EMBRYONIC FLOWER2 (EMF2) and VERNALIZATION2
and functionally related flower homeotic genes are un-
(VRN2) are involved in the transition to flowering [11,
der different control. We show that ATX1 is an epigenetic
12]. CLF and MEA encode proteins similar to the PcG
regulator with histone H3K4 methyltransferase activity.
protein Enhancer of Zeste (E(Z)), FIE is similar to the
This is the first example of this kind of enzyme activity
Extra Sex Combs (ESC), while FIS2, VRN2, and EMF2
reported in plants, and, in contrast to the Drosophila
share domains with the Suppressor of Zeste12 (SU(Z)12)
and the yeast trithorax homologs, ATX1 can methylate
proteins from Drosophila. Like their animal counterparts,
in the absence of additional proteins. In its ability to
they act as negative regulators of plant homeotic genes,
methylate H3K4 as a recombinant protein, ATX1 is simi-
which are structurally unrelated to homeotic genes in
lar to the human homolog.
animals, and may control cell proliferation and growth
Conclusions: ATX1 functions as an activator of homeo-
(reviewed in [13–15]).
tic genes, like Trithorax in animal systems. The histone
In contrast to the relatively well-characterized PcG
methylating activity of the ATX1-SET domain argues that
proteins in plants, characterization of plant homologs
the molecular basis of these effects is the ability of ATX1
with activating functions similar to the animal trxG genes
to modify chromatin structure. Our results suggest a
have not been reported. Recently, we have cloned and
conservation of trxG function between the animal and
sequenced an Arabidopsis cDNA with similarity to the
plant kingdoms despite the different structural nature
Drosophila trx gene, ARABIDOPSIS TRITHORAX1 (ATX1,
of their targets.
AF329273). Its conceptual translation revealed the pres-
ence of a SET (SU(VAR)3-9, E(Z), Trithorax) domain and
Introduction
other architectural motifs characteristic of the TRX fam-
ily of proteins [16, 17]. While sequence similarity of the
In animals, the pattern of the body plan is established
Arabidopsis genes may suggest functions similar to
early in embryonic development through the activity of
those of the animal trxG genes, supportive evidence has
been missing. Here, we show that ATX1 is expressed
*Correspondence: zavramova2@unl.edu
during floral organ initiation and plays an important role
4
Present address: Department of Plant Systems Biology, Ghent Uni-
in the development of all floral organs, their spatial ar-
versity, B-9000 Ghent, Belgium.
rangement, and their morphology. ATX1 positively and
5
Present address: Department of Biology, University of Amman,
Amman, 11121, Jordan.
specifically affects the expression of several flower ho-