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The Plant Journal (2008) 54, 608–620
doi: 10.1111/j.1365-313X.2008.03461.x
HARNESSING PLANT BIOMASS FOR BIOFUELS AND BIOMATERIALS
Deciphering gene regulatory networks that control seed
development and maturation in Arabidopsis
Monica Santos-Mendoza†, Bertrand Dubreucq, Sébastien Baud, François Parcy‡, Michel Caboche and Loı̈c Lepiniec*
INRA, AgroParitech, UMR204, Institut Jean-Pierre Bourgin (IJPB), Seed Biology Laboratory, 78026 Versailles Cedex, France
Received 31 October 2007; revised 12 February 2008; accepted 14 February 2008.
*
For correspondence (fax +33 1 3083 3111; e-mail [email protected]).
Present addresses:
†
Departamento de Biologı́a Molecular de Plantas, Instituto de Biotecnologı́a, Universidad Nacional Autónoma de México, Apdo.
Postal 510-3, Cuernavaca, Morelos 62250, Mexico.
‡
Laboratoire de Physiologie Cellulaire Végétale, UMR CNRS 5168, CEA, INRA, UJF, CEA 17 rue des Martyrs, Bâtiment C2, 38054 Grenoble Cedex 9, France.
Summary
Seeds represent the main source of nutrients for animals and humans, and knowledge of their biology provides
tools for improving agricultural practices and managing genetic resources. There is also tremendous interest in
using seeds as a sustainable alternative to fossil reserves for green chemistry. Seeds accumulate large
amounts of storage compounds such as carbohydrates, proteins and oils. It would be useful for agro-industrial
purposes to produce seeds that accumulate these storage compounds more specifically and at higher levels.
The main metabolic pathways necessary for oil, starch or protein accumulation are well characterized.
However, the overall regulation of partitioning between the various pathways remains unclear. Such
knowledge could provide new molecular tools for improving the qualities of crop seeds (Focks and Benning,
1998, Plant Physiol. 118, 91). Studies to improve understanding of the genetic controls of seed development
and metabolism therefore remain a key area of research.
In the model plant Arabidopsis, genetic analyses have demonstrated that LEAFY COTYLEDON genes,
namely LEC1, LEC2 and FUSCA3 (FUS3), are key transcriptional regulators of seed maturation, together with
ABSCISIC ACID INSENSITIVE 3 (ABI3). Interestingly, LEC2, FUS3 and ABI3 are related proteins that all contain a
‘B3’ DNA-binding domain. In recent years, genetic and molecular studies have shed new light on the intricate
regulatory network involving these regulators and their interactions with other factors such as LEC1, PICKLE,
ABI5 or WRI1, as well as with sugar and hormonal signaling. Here, we summarize the most recent advances in
our understanding of this complex regulatory network and its role in the control of seed maturation.
Keywords: Arabidopsis, network, regulation, seed, transcription.
Introduction to seed development and maturation
Evolutionary aspects
Seed development and maturation represent an evolutionary advantage that allows most plants to cope with unfavorable environmental conditions by interrupting their life
cycle and resuming growth when placed under favorable
conditions (Bentsink and Koornneef, 2002; Bewley, 1997).
There is considerable variability among plants in terms of
seed morphology, physiology and maturation, leading to
the accumulation of various compounds such as oil, seed
608
storage proteins (SSPs) and starch in the various tissues of
the seed. In fact, seed maturation is not even a compulsory
step in the plant life cycle. Lower plants (bryophytes, pteridophytes or algae) do not produce seed, and embryo
maturation is consequently alleviated in these species
(Harada, 1997; Vicente-Carbajosa and Carbonero, 2005).
Even among angiosperms, several species produce
embryos that are able to grow when excised in an immature
state from the maternal tissues. Similarly, viviparous
mutants that are defective in seed maturation can produce
viable seedlings. Together with phylogenetic analyses,
these observations strongly suggest that seed maturation
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Journal compilation ª 2008 Blackwell Publishing Ltd
Seed transcriptional regulatory network 609
Figure 1. Proposed model of genetic and molecular interactions in the regulatory network involved in the control of seed development and maturation in
Arabidopsis thaliana. Arrows and T bars indicate positive and negative effects, respectively. The factors that induce and/or maintain seed maturation are shown in
red. The factors that promote cell growth and differentiation are shown in blue. The numbers indicate the various targets of the regulators.
constitutes an intrusive developmental and metabolic
phase introduced into the ancestral plant life cycle,
i.e. uninterrupted embryo growth and seedling development
(Figure 1). It may be hypothesized that pre-existing physiological responses and developmental processes allowing
plants to cope with unfavorable environmental conditions
such as dehydration have been retained to develop this
pathway and permit seed maturation. Indeed, several seed
proteins such as late embryogenesis-abundant (LEA), oleosins and SSPs are also found in angiosperm pollen (Huang,
1996; Wise and Tunnacliffe, 2004; Zakharov et al., 2004) or in
spores of bryophytes (Schallau et al., 2008). In addition,
molecular analyses support the conservation of regulatory
pathways controlling gene expression in fern spores and in
seeds of both gymnosperms and angiosperms (Schallau
et al., 2008).
Genetic control of the maturation phase
The maturation processes occurring in various seed tissues
(i.e. seed coat, endosperm and embryo) contribute to seed
quality, allowing efficient dispersal and establishment of the
seedlings (Welbaum et al., 1998). Seed quality relies, therefore, on the tight control of embryo morphogenesis, maturation and germination. This raises the question of the
genetic and molecular relationships that exist between the
various developmental and metabolic phases. Several
observations suggest that the various processes can be
disconnected to some extent. Various mutants affected in
embryogenesis can express seed maturation-specific genes
and accumulate some storage compounds (Devic et al.,
1996; Lepiniec et al., 2005; Yadegari et al., 1994). It has also
been suggested that maturation and post-germinative
growth could occur simultaneously in the embryo (Finkelstein and Crouch, 1986), although expression of maturationand germination-specific genes may not overlap at the
cellular level. Furthermore, we do not know whether the
maturation processes occurring in angiosperms have arisen
progressively during evolution through the elaboration of
several intricate regulatory mechanisms or whether they
have arisen from a small number of pleiotropic modifications such as the mutation of homeotic genes. Simple
genetic switches may exist to shift from embryogenesis to a
maturation program, and subsequently to germination.
These genetic programs may be exclusive at the cellular
level but could occur simultaneously in the same embryo.
Finally, the nature and origin of the molecular mechanisms
that control both the entrance into the maturation phase and
those that prevent cell growth and division remain to be
elucidated.
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610 Monica Santos-Mendoza et al.
Arabidopsis as a model to study seed
development and maturation
In Arabidopsis, seed development and maturation are well
documented (Baud et al., 2002; Goldberg et al., 1994;
Harada, 1997; Laux and Jurgens, 1997; Laux et al., 2004;
Lehti-Shiu et al., 2005; Lepiniec et al., 2005, 2006; Mansfield
and Briarty, 1991; Mansfield et al., 1991; Mayer et al., 1991;
Weijers and Jurgens, 2005; West and Harada, 1993). Briefly,
embryo morphogenesis is initiated by double fertilization of
the embryo sac, giving rise to the endosperm and the
zygote. The zygote divides asymmetrically to form apical
and basal cells leading to the embryo proper and the suspensor, respectively. A precise order of events ensures the
correct relative positioning of the various tissues and organs
(meristems, cotyledons and hypocotyl) and the arrangement
of cell types within each tissue of the embryo. At the heart
stage of embryo development (about 7 days after fertilization), most of the cell division and differentiation events
have already occurred, i.e. the protoderm has differentiated
into the epidermis, the pro-vascular bundles are ready to
form the vascular system, and the overall shape of the
embryo is determined with organization of both the
apico-basal (shoot and root meristems) and lateral (cotyledons) symmetries. During this first phase, the triploid
endosperm develops through a syncytial phase that is
followed by cellularization and differentiation events.
Starch and hexoses accumulate only transiently during
seed development and very low amounts remain in dry
seed. In contrast, sucrose and some oligosaccharides
gradually accumulate at the end of the maturation phase
(Baud et al., 2002; Focks and Benning, 1998). Interestingly,
the decrease in the hexose to sucrose ratio correlates with
transition to the maturation phase. This observation is
consistent with the recently demonstrated role of the
AtSUC5 sucrose transporter in the Arabidopsis endosperm (Baud et al., 2005) and of APETALA2 in the control
of the hexose to sucrose ratio and seed mass (Ohto et al.,
2005). Taken together, these data suggest a signaling
function for sugars during the transition from embryo
morphogenesis to maturation in Arabidopsis, as already
suggested for other plant species (Gutierrez et al., 2007;
Weber et al., 2005). However, the role of the hexose to
sucrose ratio in oilseeds remains under debate (Tomlinson et al., 2004). Trehalose-6-phosphate is also thought
to play a critical role in triggering seed maturation, but
the molecular mechanism involved remains unclear
(Eastmond et al., 2002; Gomez et al., 2006).
During the maturation phase, embryo growth and cell
cycle activities are stopped (Raz et al., 2001). The embryo
goes through a period of cellular expansion and differentiation, concomitant with reduction of the endosperm to
one cell layer and the onset of maturation (until around
17–20 days after fertilization). The embryo accumulates
nitrogen compounds (proteins) and carbohydrate storage
compounds (lipids) that each account for 30–40% of the
seed dry matter (Baud et al., 2002; Mansfield and Briarty,
1992). Lipids accumulate in the form of triacylglycerols
(TAG) in cytosolic oil bodies, which occupy about 60% of
the cell volume in the cotyledons of mature embryos.
During late maturation, the seed becomes metabolically
quiescent and tolerant to desiccation. The metabolic
pathways leading to accumulation of the main storage
compounds, including oil, are well characterized (Baud
et al., 2002; Fait et al., 2006; Ruuska et al., 2002; Schwender et al., 2004a,b). The tremendous interest in using
oils for industrial applications is emphasized and
reviewed elsewhere in this special issue (Durrett et al.,
2008; Dyer et al., 2008). However, genetic engineering has
routinely resulted in only a low accumulation of the
desired fatty acids (Dyer and Mullen, 2008), and the
genetic, cellular and molecular mechanisms that regulate
the accumulation and partitioning between various pathways remain unclear. Nevertheless, a few transcription
factors that appear to collectively control the various
facets of seed maturation have been characterized during
recent years and are described below.
Characterization of ABI3, FUS3, LEC2 and LEC1
Identification of the loci
Mutations of ABI3 (Giraudat et al., 1992; Koornneef et al.,
1984), LEC1 (Lotan et al., 1998; Meinke, 1992; West et al.,
1994), LEC2 (Meinke et al., 1994; Stone et al., 2001) and FUS3
(Baumlein et al., 1994; Gazzarrini et al., 2004; Keith et al.,
1994; Luerssen et al., 1998) genes lead to similar pleiotropic
effects on seed phenotype (Harada, 2001; Holdsworth et al.,
1999; Parcy et al., 1997; Vicient et al., 2000). Early during
embryogenesis, the LEC1, LEC2 and FUS3 genes are
required to maintain embryonic cell fate and to specify cotyledon identity. Mutant cotyledons display some of the
characteristics of young leaves, exhibiting both trichomes
on their surface and a complex vascular pattern. The mutant
embryos may also present abnormal suspensor phenotypes, precocious cell-cycle activation, and growth of apical
and root meristems. Later during embryogenesis, these
genes, together with ABI3, are also involved in initiation and
maintenance of the maturation phase. Mutant seeds are less
tolerant to desiccation, accumulate lower levels of storage
compounds, and instead accumulate anthocyanin pigments
and/or are affected in chlorophyll breakdown. The dormancy
of mutant seeds is also modified. In a humid environment,
they can display precocious germination, and mutant
combinations show extreme viviparity.
Nevertheless, the mutant phenotypes are not identical.
For instance, abi3 is the only mutant that is highly resistant
to abscisic acid (ABA) and the mutation does not affect
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Journal compilation ª 2008 Blackwell Publishing Ltd, The Plant Journal, (2008), 54, 608–620
Seed transcriptional regulatory network 611
cotyledon identity (Giraudat et al., 1992). However, abi3
mutations strongly affect the accumulation of SSPs (more so
than fus3), and both the quantity and quality of seed lipids
are also modified. The lec2 phenotype is the least severe.
The mutant seeds are less sensitive to desiccation and only
slightly affected in the accumulation of storage compounds
(Meinke et al., 1994; Stone et al., 2001). There are also
differences in the tissues affected (To et al., 2006). ABI3 is
important for the expression of some SSP genes (e.g. At2S3)
in the embryo axis, the center of the cotyledons and the
endosperm. FUS3 is necessary in the axis and the endosperm. Although the lec2 mutant lacks SSPs in some
sectors of the cotyledons, LEC2 is required throughout the
embryo. Finally, analyses of mutant combinations have
demonstrated that these regulatory proteins can act at least
partially redundantly and sometimes synergistically,
depending on the traits and the tissues studied (Meinke
et al., 1994; Parcy et al., 1997; Raz et al., 2001; To et al.,
2006).
Structure of the LEC and ABI3 genes
Consistent with their partial functional redundancy, the
three genes LEC2, FUS3 and ABI3 encode related transcription factors of the B3 domain family (Giraudat et al., 1992;
Luerssen et al., 1998; Stone et al., 2001). The B3 DNA-binding domain of 120 amino acid residues was originally identified as the third basic region of the ABI3 protein and of its
maize homolog VP1 (McCarty et al., 1991). This domain is
also found in other classes of transcription factors (Qu and
Zhu, 2006), namely the ARFs (auxin response factors;
Ulmasov et al., 1997), the RAVs (‘related to ABI3/VP1’;
Kagaya et al., 1999) and the HSI2/VAL family (Suzuki et al.,
2007; Tsukagoshi et al., 2005, 2007). This domain shares
some similarities with the DNA-binding domain of a prokaryotic endonuclease. The structure of the domain has
been determined, allowing a model of its interaction with
DNA to be proposed (Yamasaki et al., 2004). LEC1 belongs to
a different class of proteins and is homologous to HAP3
subunits of the CAAT box-binding factors (CBFs), a family of
heteromeric transcription factors (Lee et al., 2003; Lotan
et al., 1998).
Expression of the LEC and ABI3 genes
Expression patterns have been characterized for these four
genes (Figure 2). LEC1 is specifically expressed in seed and
is detected in both the embryo and the endosperm, early
during embryogenesis (Lee et al., 2003; Lotan et al., 1998).
LEC2 is mainly expressed during early embryo development, although it is also detected occasionally in vegetative tissues (Kroj et al., 2003; Stone et al., 2001).
Expression of FUS3 has mainly been detected in the protodermal tissue of the embryo (Gazzarrini et al., 2004;
Figure 2. Tissue-specificity of the B3 regulatory network in the developing
embryo of Arabidopsis thaliana. The areas where gene expression is detected
are indicated in red. The expression patterns were determined using a
promoter:GUS fusion for LEC2, a promoter:cDNA:GFP fusion for FUS3, and
in situ hybridization (ISH) for both ABI3 and LEC1.
Tsuchiya et al., 2004). Consistent with this localization,
specific expression of FUS3 in the protodermal cell layer
can rescue most of the fus3 phenotypes, including accumulation of SSPs in various cell layers of the embryo
(Gazzarrini et al., 2004). This L1-specific expression pattern
is difficult to reconcile with a direct effect of FUS3 on the
promoter of SSP genes throughout the embryo. It has
been proposed that FUS3 acts indirectly through the regulation of TTG1 expression and hormonal levels. Recent
data have shown that ABI3 is expressed in the whole
embryo, which is consistent with the expression pattern of
its target genes (To et al., 2006). ABI3 is also detected in
vegetative organs, and has a role in lateral meristem
development (Rohde et al., 2000). However, the level of
gene expression is very low for all the regulatory genes
studied, making it difficult to characterize mRNA accumulation by using in situ hybridization. Most of the data
available to date have been obtained using reporter genes
controlled by native promoters in transgenic plants.
Although these approaches have given consistent results
(To et al., 2006), complementary experiments are required
to describe more comprehensively the tissue and cellular
expression of these regulatory genes and take into account
possible post-transcriptional regulation. To date, only a
pFUS3:FUS3:GFP construct has been used, providing
results consistent with epidermal localization of the protein
(Gazzarrini et al., 2004). The site of protein accumulation at
the tissue and intracellular levels remains to be investigated or confirmed for the other factors.
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Journal compilation ª 2008 Blackwell Publishing Ltd, The Plant Journal, (2008), 54, 608–620
612 Monica Santos-Mendoza et al.
A complex and intricate regulatory network
Cross-talk and feedback regulation
Although lec2, fus3 and abi3 mutants display similar alterations of the maturation process, they also exhibit some
specific phenotypes that appear to be additive in double
mutants, suggesting that the three proteins belong to parallel regulatory pathways that partially overlap (Keith et al.,
1994; Meinke et al., 1994; West et al., 1994). Various genetic
analyses have established the existence of interactions
between these genes, but their true nature remains to be
elucidated at the molecular level (Brocard-Gifford et al.,
2003; Nambara et al., 2000; Parcy et al., 1997; Raz et al.,
2001). FUS3 and LEC2 were shown to act in partially
redundant pathways to locally regulate FUS3 expression
(Kroj et al., 2003). In addition, analyses of double mutants
with lec1, lec2 and fus3 suggested that LEC1 could act
upstream of LEC2 and FUS3 (Meinke et al., 1994). Finally, a
recent exhaustive genetic analysis of the regulation of gene
expression in single and multiple mutant backgrounds (To
et al., 2006) demonstrated that expression of both FUS3 and
ABI3 is controlled by a complex network of local and
redundant regulations involving LEC1 and LEC2, and also
FUS3 and ABI3 themselves (Figure 3). For instance, FUS3
expression is regulated by LEC2 and FUS3 itself in the root
tip, by LEC2 and ABI3 in the embryo axis, and by the four
regulators in cotyledons. The expression of ABI3 is also
controlled by the four regulatory proteins in cotyledons.
However, ABI3 expression is independent of any of these
regulators in the embryo axis. These results are in agreement with molecular studies demonstrating that ectopic
expression of LEC1 or LEC2 can induce FUS3 and ABI3
expression (Kagaya et al., 2005b; Santos Mendoza et al.,
2005). It would be interesting to know to what extent ABI3
and FUS3 can complement lec1 mutation, as previously
tested for the lec2 mutant (To et al., 2006). Nevertheless,
such experiments cannot prevent non-specific ‘B3’ effects
due to constitutive (non-physiological) expression of FUS3
or ABI3 that would alter their binding specificity. Additional
experiments conducted in mutant backgrounds are necessary to confirm these results (e.g. ectopic expression of
FUS3 in abi3 lec2 double mutants or ABI3 in a lec2 fus3
background). Similarly, direct induction of various target
genes by LEC2 (Braybrook et al., 2006; Kroj et al., 2003;
Santos Mendoza et al., 2005) should be confirmed in the
fus3 abi3 mutant background. Interestingly, at least two
members of the recently characterized HIS/VAL family of
transcriptional repressors (i.e. HSI2 and HSL1) redundantly
inhibit the B3 maturation network in seedlings (Suzuki et al.,
2007; Tsukagoshi et al., 2005, 2007). The fact that these
regulators may function by repressing sugar-inducible
genes is consistent with a role of sugar signaling in the
maturation process (see above and Figure 1).
Figure 3. A complex network of local and redundant regulations. Schematic
representation of the local genetic controls in various embryo tissues (Lotan
et al., 1998; To et al., 2006; Tsuchiya et al., 2004, and references therein).
Hormonal signaling
The key role of auxin in plant embryogenesis has been well
described (Jenik and Barton, 2005; Weijers and Jurgens,
2005). Nonetheless, only minor auxin-related phenotypes
have been observed during early embryogenesis of the lec
mutants, such as the abnormal development of the suspensor detected occasionally in lec1 and lec2 (Lotan et al.,
1998; Stone et al., 2001) and reduced length of the axis.
Nevertheless, recent data suggest that auxin signaling may
interfere with the B3 regulatory network. The ability of lec1
and lec2 mutants to form somatic embryos is strongly
reduced (Gaj et al., 2005). Conversely, ectopic expression of
LEC1 and LEC2 in vegetative cells can trigger the formation
of embryo-like structures (Lotan et al., 1998; Stone et al.,
2001). Interestingly, some key proteins in auxin signaling
(i.e. ARFs) also belong to the B3 family, and an ABI3
homolog of bean (Phaseolus vulgaris) is able to bind the
auxin-responsive element (Nag et al., 2005). Consistent with
the latter result, ABI3 appears to be involved in auxin signaling as well as lateral root development (Brady et al.,
2003). Additionally, ectopic expression of LEC2 causes rapid
activation of an auxin-responsive gene (Braybrook et al.,
2006). Ectopic expression of FUS3 in the epidermal cells
leads to a reduced venation pattern in cotyledons, and auxin
can induce FUS3 expression (Gazzarrini et al., 2004). Finally,
it has been proposed that the role of LEC1 in the promotion
of embryonic cell identity and division requires auxin and
sucrose (Casson and Lindsey, 2006). Despite this wealth of
potential links between auxin signaling and seed maturation
regulators, their roles remain to be established.
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Seed transcriptional regulatory network 613
Mutant analyses have not been sufficient to demonstrate
the role of both ABA and gibberellin (GA) during embryo
morphogenesis. Indeed, either some traces of ABA are
found in the mutant seeds or the supply of GA is required for
obtaining flowers and seeds. Nevertheless, ABA immunomodulation in transgenic tobacco seeds (Phillips et al., 1997)
and ectopic expression of a pea GA2 oxidase in Arabidopsis
(Singh et al., 2002) support an essential role for ABA during
maturation and for GA in seed development, respectively. In
addition, it has been firmly established that the ABA/GA ratio
is a key regulator of both maturation and germination
processes (Bentsink and Koornneef, 2002; Debeaujon and
Koornneef, 2000; Dubreucq et al., 1996; Finkelstein et al.,
2002; Giraudat et al., 1994; Karssen et al., 1983; Koornneef
et al., 1982, 2002; Ogawa et al., 2003). As the embryo enters
the maturation phase, ABA content increases in seed, and
the resulting high ABA/GA ratio promotes maturation,
induces dormancy and inhibits cell-cycle progression,
embryo growth and germination. FUS3 and LEC2 have been
shown to inhibit GA biosynthesis by repressing the expression of GA biosynthetic genes (Curaba et al., 2003; Gazzarrini et al., 2004). Consequently, in lec2 and fus3 mutants, the
ABA/GA ratio is lower than in wild-type seeds. This is fully
consistent with the defects observed during the maturation
phase and with the precocious cell differentiation and
growth of mutant embryos. Lack of GA biosynthesis was
shown to be epistatic to the lec mutations for the formation
of trichomes, suggesting that GAs act downstream of the
LEC genes. Similarly, ABA is required for the induction of
some SSPs in seedlings ectopically expressing FUS3
(Kagaya et al., 2005a,b) or ABI3 (Parcy et al., 1994).
Conversely, it has been shown that the activity of ABI3 and
FUS3 can be regulated at the post-translational level by ABA
and/or GA. AIP2 (ABI3-interacting protein 2) is an E3 ligase,
whose expression is under the control of ABA, that can
trigger the degradation of ABI3 (Zhang et al., 2005). This
regulation could ensure rapid degradation of ABI3 during
imbibition, thus promoting germination. Similarly, it has
been suggested that ABA and GA could regulate the stability
of FUS3 (Gazzarrini et al., 2004).
epigenetic mechanisms (i.e. histone modifications) could
repress the expression of seed-specific genes during Arabidopsis seed germination (Tai et al., 2005) or control the
activation of maturation-specific genes by an ABI3 homolog
in bean (Ng et al., 2006). This type of regulation has been
recently confirmed by the demonstration that two histone
deacetylases, namely HDA6 and HDA19, redundantly inhibit
embryonic properties during germination via the repression
of LEC1, FUS3 and ABI3 (Tanaka et al., 2008). It has also been
demonstrated that the expression of FUS3 could be regulated by some members of the polycomb protein family
involved in the epigenetic control of seed and plant development (Makarevich et al., 2006). LEC1-like (L1L) is closely
related to LEC1, but it has a different function during
embryogenesis due to its specific pattern of gene expression
(Kwong et al., 2003). In effect, L1L is expressed earlier than
LEC1 during embryo development and is necessary for early
embryogenesis. Mutations of ABI4 and ABI5 also affect seed
maturation, although the effects of such mutations are limited compared to those of abi3 (Finkelstein and Lynch, 2000;
Finkelstein et al., 1998, 2002). The ABI4 protein belongs to a
family of transcription regulators that contain a plant-specific APETALA2 (AP2) domain (Finkelstein et al., 1998) and
acts downstream of ABI3 (Brocard-Gifford et al., 2003;
Soderman et al., 2000). ABI5 is a transcription factor of the
bZIP family (Finkelstein and Lynch, 2000; Lopez-Molina and
Chua, 2000) that acts in the same signaling pathway as ABI4
(see below). The TAN gene encodes a protein with a WDR
motif that could interact with other proteins to control various aspects of both early and late phases of embryo development (Yamagishi et al., 2005). The tan mutant shares
many characteristics with the lec mutants, suggesting that
these genes may have overlapping roles during embryogenesis. Finally, the homeobox GLABRA2, which is known
to regulate the formation of trichomes and root hairs, has
recently been shown to also be involved in the control of oil
accumulation in seeds (Shen et al., 2006), but its role in the
regulatory network is still unknown.
Other regulators of seed maturation
Target promoters and the role of RY motifs
Other important regulators for seed development and/or
maturation have been identified by genetic analyses. Interestingly, PICKLE (PKL), a chromatin-remodeling factor
(CHD3), acts in concert with GA to repress embryonic traits
during and after germination, including the expression of
LEC1, LEC2 and FUS3 in roots (Dean Rider et al., 2003;
Henderson et al., 2004; Li et al., 2005; Ogas et al., 1997, 1999;
Rider et al., 2004). Consistent with these results, it has been
shown recently that PKL is also necessary to repress ABI3
and ABI5 expression during germination, in response to
ABA (Perruc et al., 2007). Some reports have suggested that
It has been shown that B3-type transcription factors can act
directly on the expression of genes encoding storage proteins (Vicente-Carbajosa and Carbonero, 2005). LEC2 has
been shown to exert direct control over At2S1–S4 and 2Slike gene expression (Braybrook et al., 2006; Kroj et al.,
2003). FUS3 and ABI3 can also directly contribute to the
induction of storage protein gene expression (Ezcurra et al.,
2000; Reidt et al., 2000). The three B3-type regulatory proteins directly activate the target genes by binding to RY
motifs present in the promoters (Ezcurra et al., 2000; Monke
et al., 2004; Reidt et al., 2000; Reinders et al., 2002). Indeed,
Identifying the targets of the B3 regulatory network
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Journal compilation ª 2008 Blackwell Publishing Ltd, The Plant Journal, (2008), 54, 608–620
614 Monica Santos-Mendoza et al.
the RY box (CATGCA) is necessary for the correct expression
of several seed-specific genes in Arabidopsis (Baumlein
et al., 1986, 1992; Conceicao Ada and Krebbers, 1994; Ellerstrom et al., 1996; Stalberg et al., 1993), legumes (Bobb
et al., 1997; Dickinson et al., 1988) and maize (Suzuki et al.,
1997), for example. Furthermore, it has been shown that
FUS3, LEC2 and ABI3 can bind an RY motif in vitro
(Braybrook et al., 2006; Monke et al., 2004; Reidt et al., 2000),
and that LEC2 and FUS3 bind an RY motif in a yeast
one-hybrid assay (Kroj et al., 2003).
However, RY elements probably do not act alone in seed
promoters (i.e. they may not be sufficient to confer the
correct expression of target genes). It has been shown that
other DNA motifs (e.g. G-box) and factors binding these
motifs are required for the correct expression of target genes
during seed maturation (Bensmihen et al., 2002; BrocardGifford et al., 2003; Ezcurra et al., 1999; Hobo et al., 1999;
Kurup et al., 2000; Nakashima et al., 2006; Sakata et al.,
1997; Vicente-Carbajosa and Carbonero, 2005; Wobus and
Weber, 1999). Several bZIP transcription factors have been
shown to play a role during seed development. ABI5, for
example, affects ABA sensitivity and controls the expression
of some LEA genes in seeds (Carles et al., 2002; Finkelstein
and Lynch, 2000; Lopez-Molina and Chua, 2000). The ABI5
protein binds to abscisic acid-responsive element (ABRE)
cis-elements that are present in the promoters of several LEA
genes such as AtEM1 or AtEM6. Interestingly, ABI5 expression is itself regulated by ABI3, and both proteins interact in
yeast two-hybrid assays, suggesting that ABI3 induces the
expression of one of its partners in a transcriptional complex
(Lopez-Molina et al., 2002; Nakamura et al., 2001). ABI5
belongs to a bZIP subfamily (Jakoby et al., 2002) that
includes other members involved in seed maturation or
ABA signaling in vegetative tissues (Bensmihen et al., 2002;
Brocard-Gifford et al., 2003; Choi et al., 2000; Finkelstein
et al., 2005; Johnson et al., 2002). Some bZIP proteins from
another subgroup (i.e. bZIP10 and bZIP25) that are homologous to maize OPAQUE2 also play a role during seed
maturation. These transcription factors act together with
ABI3 to regulate the expression of SSP genes (Lara et al.,
2003).
Limitations of genetic approaches and
interest in inducible systems
It is important to note that, due to partial functional redundancy, the intricate regulatory network and conservation of
the B3 domain in the three proteins LEC2, FUS3 and ABI3, it
is difficult to draw conclusions from genetic analyses
regarding the precise mechanisms and specific function for
each regulatory protein in planta. Ectopic expression of a
regulatory protein can also lead to misinterpretation of the
real network (providing an non-specific B3 effect). In order to
decipher the specific effects of the various regulators,
several groups have taken advantage of inducible systems
to control the expression of LEC1, LEC2 and FUS3 to identify
direct target genes (Braybrook et al., 2006; Kagaya et al.,
2005a,b; Santos Mendoza et al., 2005; Wang et al., 2007).
These methods, coupled to quantitative PCR experiments
and/or transcriptomic analyses, have confirmed some
previously identified putative direct targets and revealed a
set of new potential target genes.
Among the target genes identified using an inducible
system (and confirmed in vitro) is AGAMOUS-LIKE15
(AGL15; Braybrook et al., 2006), which encodes a MADS
box protein that is expressed preferentially in seed (LehtiShiu et al., 2005). Although the agl15 mutant does not
display abnormal seed phenotypes, ectopic expression of
AGL15 affects the embryonic program and enhances the
competency of shoot apical meristems to undergo somatic
embryogenesis (Adamczyk et al., 2007). Interestingly, it has
been shown that AGL15 directly regulates expression of a
gene encoding an enzyme that is involved in the oxidation of
active gibberellin (Wang et al., 2004), providing some clues
about the putative role of AGL15 in seed development.
Other direct target genes include oleosins, which are
involved in the formation of oil bodies. Nevertheless, none
of the genes required for the synthesis of TAGs stored in
these oil bodies appeared to be regulated by LEC2. This
result was all the more intriguing as the induction of LEC2 in
maturing embryos correlates well with the onset of oil
deposition. Moreover, the ectopic expression of LEC2 in
developing leaves was shown to be sufficient to trigger TAG
accumulation in these tissues (Santos Mendoza et al., 2005).
These results suggested that intermediate regulators might
be involved in the control of TAG biosynthesis. Indeed, it has
been shown that ectopic expression of FUS3 can trigger the
expression of fatty acid biosynthetic genes (Wang et al.,
2007). In addition, we have recently demonstrated that the
transcriptional activator WRINKLED1 (WRI1), a direct target
of LEC2, is necessary for the regulation of oil biosynthesis by
LEC2 (Baud et al., 2007a).
Control of WRI1 and the TAG biosynthetic pathway
In contrast to the B3-type master regulators that exhibit a
broad control on seed maturation, WRI1, a transcription
factor of the AP2/EREB family, has an impact on more specific aspects of the maturation process (Cernac and Benning,
2004). wri1 mutants produce wrinkled seeds with severe
depletion of TAGs (Baud et al., 2007a; Cernac and Benning,
2004). In this seed mutant, which has a low oil content,
carbohydrate metabolism is compromised (Baud and
Graham, 2006; Focks and Benning, 1998), rendering maturing embryos unable to efficiently convert sucrose into TAGs.
Microarray experiments and quantitative RT-PCR analyses
on mutant wri1 seeds and Pro35Sdual:WRI1 lines led to isolation of some putative targets of WRI1 (Andre et al., 2007;
ª 2008 The Authors
Journal compilation ª 2008 Blackwell Publishing Ltd, The Plant Journal, (2008), 54, 608–620
Seed transcriptional regulatory network 615
Figure 4. Control of storage compound synthesis and accumulation in maturing seeds of Arabidopsis thaliana. The precursors for de novo fatty acid synthesis in
maturing embryos are derived from sucrose through the glycolytic pathway and/or the OPPP. Plastidial pyruvate kinases (PKps) play a key role in provision of these
precursors. Fatty acids produced in the plastids are then exported towards the cytosol in the form of acyl CoAs and used to form triacylglycerols, ultimately stored in
oil bodies. The amino acids required for the synthesis of storage proteins during the maturation process are either directly imported from the maternal tissues or
synthesized/modified in the embryonic tissues. Storage proteins are ultimately stored in specific vacuoles. Solid arrows represent positive transcriptional
regulations. Target genes encoding members of the metabolic network leading to storage compound synthesis/accumulation are indicated in italics. FA, fatty acids;
OPPP, oxidative pentose phosphate pathway; SSP, seed storage proteins; TAG, triacylglycerides; TCA cycle, tricarboxylic acid cycle.
Baud et al., 2007a,b; Ruuska et al., 2002). These include
several genes encoding enzymes from glycolysis and the
fatty acid biosynthetic network (Figure 4). Taken together,
these data indicate that WRI1 specifies the regulatory action
of LEC2 towards the metabolic network involved in the
production of storage fatty acids. These results exemplify
how metabolic and developmental processes affecting the
maturing embryo can be coordinated at the molecular level.
Further analyses are now required to identify the cis-regulatory element recognized by WRI1 and determine both the
transcriptional and post-transcriptional regulation of this
factor. At the transcriptional level, LEC1 may participate in
regulation of WRI1 expression (Casson and Lindsey, 2006).
Likewise, sucrose may play a role in triggering the induction
of WRI1, as well as of LEC2, FUS3 and ABI3 (Masaki et al.,
2005; Tsukagoshi et al., 2007).
Conclusions
As exemplified in this special issue, there is a strong interest
in using plant storage compounds for industrial applications
(biomass for biofuels and biomaterials). For instance, plant
oil is one of the most energy-rich and abundant forms of
reduced carbon available from nature and represents a
possible substitute for conventional diesel (Durrett et al.,
2008). However, for industrial and economic reasons, the
accumulation of specific storage compounds needs to be
increased. Interestingly, master seed regulators can directly
control the expression of SSPs and/or activate secondary
transcription factors that are able to trigger other transcription programs. Among the latter, WRI1 is specifically
involved in the regulation of oil biosynthesis and is therefore
an interesting candidate for biotechnology applications.
However, our understanding of the gene regulatory
networks that control seed development and maturation is
still limited. Several transcription factors, their interactions
and their target genes remain to be characterized. In addition, other levels of regulation (e.g. post-translational or
metabolic) will have to be taken into account for efficient
metabolic engineering. Finally, the model network will have
to be extended to other plant species.
The current data indicate a complex regulatory scheme in
which LEC1 and LEC2 initiate and control seed maturation
and prevent germination, together with FUS3 and ABI3.
Recent genetic and molecular analyses have shed new light
on this intricate regulatory network and led to the elaboration of a model that seems to be fully coherent with
phenotypic analyses of single and double mutants (Figure 1). The four regulators act in concert with hormones
(auxin, ABA and GA), epigenetic mechanisms (e.g. PKL
protein) and target regulatory proteins such as WRI1, ABI5 or
AGL15. In addition, other master regulatory genes have
been identified (e.g. TAN and L1L), although their exact
function in the network is not known.
It may be hypothesized that this complex network provides robust and tight control of seed maturation. These
results also emphasize that phenotypic analyses must be
carried out at the cellular level to unravel complex regulatory
ª 2008 The Authors
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616 Monica Santos-Mendoza et al.
traits. Furthermore, they highlight some of the limitations
and drawbacks of the various analyses carried out so far,
making additional experiments necessary to firmly establish
the specificity and precise function (i.e. identification of their
target genes) of the various factors in planta. The use of
inducible systems coupled to transcriptomic analyses, as
well as analyses of the molecular interactions (protein–
protein and protein–DNA) in planta using, for instance,
chromatin immunoprecipitation (ChIP) or bimolecular fluorescence complementation (BiFC) could provide interesting
data to reinforce the model.
An interesting and still open question is the origin of this
complex regulatory network. It is possible that the three
B3-type regulators (LEC2, FUS3 and ABI3) derive from a
common ancestor with auto-regulatory properties (To
et al., 2006). ABI3 is present in various vegetative tissues
and fulfils several functions related to plastid development,
control of flowering time, outgrowth of axillary meristems
and lateral root formation (De Meutter et al., 2005; Horvath
et al., 2003). ABI3 also appears to be conserved among
plants, as homologous genes have been found in monocots
(Hattori et al., 1994; McCarty et al., 1991), gymnosperms
(Zeng and Kermode, 2004) and in the moss Physcomitrella
(Marella et al., 2006). Interestingly, the homologous maize
protein (VP1) has been shown to complement the abi3
mutation (Suzuki et al., 2001), suggesting that ABI3 is
closely related to the ancestral B3 protein. Interestingly,
recent findings strongly support the conservation of regulatory pathways controlling gene expression in fern spores
and in seeds of both gymnosperms and angiosperms
(Schallau et al., 2008). Nevertheless, despite the recent
identification of a putative FUS3 homolog in monocots
(Moreno-Risueno et al., 2008), data from more distantly
related plants (e.g. gymnosperms and lower plants) are still
lacking, impeding a robust phylogenetic analysis of the
evolutionary history of the B3 factors involved in the control
of seed maturation.
Acknowledgements
We wish to acknowledge several colleagues: F. Berger, M. Delseny,
M. Devic, J. Giraudat, A. Marion-Poll, M. Miquel, C. Rochat and
T. Roscoe for discussions about seed development and maturation;
N. Berger, E. Harscoët, J. Kronenberger and A. To, for their invaluable contribution to parts of the work presented here; and finally
H. North and the reviewers for helpful comments and correcting the
manuscript. Part of our work on Arabidopsis seed development and
transcriptional regulation is supported by grants from the Agence
Nationale pour la Recherche (ANR) Genoplante ‘Arabidoseed’
(TRIL-033) and the ANR ‘TF code’ (ANR-07-BLAN-0211-02). S.B. is a
Chargé de Recherche at CNRS.
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