Journal of Experimental Botany, Vol. 64, No. 6, pp. 1427–1437, 2013
doi:10.1093/jxb/ert025 Advance Access publication 11 February, 2013
Flowering Newsletter Review
Control of flower size
Beth A. Krizek* and Jill T. Anderson
Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA
*To whom correspondence should be addressed. E-mail: [email protected]
Received 31 October 2012; Revised 10 January 2013; Accepted 15 January 2013
Abstract
Flowers exhibit amazing morphological diversity in many traits, including their size. In addition to interspecific flower
size differences, many species maintain significant variation in flower size within and among populations. Flower
size variation can contribute to reproductive isolation of species and thus has clear evolutionary consequences.
In this review we integrate information on flower size variation from both evolutionary and developmental biology
perspectives. We examine the role of flower size in the context of mating system evolution. In addition, we describe
what is currently known about the genetic basis of flower size based on quantitative trait locus (QTL) mapping in
several different plant species and molecular genetic studies in model plants, primarily Arabidopsis thaliana. Work in
Arabidopsis suggests that many independent pathways regulate floral organ growth via effects on cell proliferation
and/or cell expansion.
Key words: Arabidopsis, floral evolution, floral organ growth, flower size, natural variation, selection.
Introduction
Flowers can vary dramatically in size with the gigantic flowers
of Rafflesia arnoldii measuring almost one meter across compared with the tiny microscopic flowers of the genus Wolffia
(Davis et al., 2008). Such extreme floral sizes may only be
possible in plants with specialized life strategies (Davis et al.,
2008; Endress, 2011). Flower size can also vary widely between
related plants species with similar growth habits (Fig. 1) and
even within species (Andersson, 2012; Delph et al., 2010;
Hermann and Kuhlemeier, 2011; Mojica and Kelly, 2010;
Spigler et al., 2011; Williams and Conner, 2001; Wu et al.,
2008) with immediate consequences on reproductive success (Bradshaw et al., 1995; Goodwillie et al., 2006; Hodges
et al., 2002; Schiestl and Schluter, 2009; Venail et al., 2010).
Divergent selection on floral traits such as flower size imposed
by variable abiotic and/or biotic conditions can drive population differentiation (Brunet, 2009; Galen, 1996) and could
potentially contribute to reproductive isolation (Bradshaw
et al., 1995; Hodges et al., 2002; Schiestl and Schluter, 2009;
Venail et al., 2010). A recent review suggests that variation in
floral morphology (including flower size) is a more important
reproductive barrier than flower colour in the Orchidaceae
(Schiestl and Schluter, 2009).
Ecologists and evolutionary biologists have extensively
investigated the environmental causes and evolutionary
consequences of floral trait variation in nonmodel organisms (Fenster et al., 2004; Galen, 2000; Gong and Huang,
Fig. 1. Comparison of flower size in Brassica rapa (left) and
Arabidopsis thaliana (right). Size bar is 4 mm.
Abbreviations: ChIP-Seq, chromatin immunoprecipitation with high-throughput sequencing; QTL, quantitative trait locus/loci; SI, self-incompatible.
© The Author [2013]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For permissions, please email: [email protected]
1428 | Krizek and Anderson
2009; Stanton and Preston, 1988; Williams and Conner,
2001). Developmental biologists have identified the genetic
basis of flower size in model species under controlled conditions (Sicard and Lenhard, 2011). Ultimately, integrating
these approaches will enable a more thorough examination
of the evolution of phenotypic variation, the co-evolutionary dynamics of plants and their pollinators, the tempo
and mechanism of reproductive isolation and perhaps the
genetic architecture of speciation (Bradshaw et al., 1995;
Hodges et al., 2002; Langlade et al., 2005; Schiestl and
Schluter, 2009; Venail et al., 2010). Furthermore, interdisciplinary investigations will enable researchers to test
the mechanisms that maintain genetic variation in natural
populations and examine how selection operates at the level
of the gene (Anderson et al., 2011; Olson-Manning et al.,
2012). Here we seek to review the evolution and developmental genetics of flower size variation, uniting disparate
bodies of literature. To that end, we briefly discuss floral
size in the context of mating system evolution, examine constraints on the evolution of flower size and explore studies
that address the genetics of flower size via quantitative trait
locus (QTL) mapping. We then focus on advancements that
have been made possible through detailed genetic analyses
of the model organism Arabidopsis thaliana in the laboratory and growth chamber.
Mating system evolution and selection on
flower size
Flower size is a key ecological trait as it influences mating
system evolution and reproductive success (Goodwillie et al.,
2010; Sargent et al., 2007). In outcrossing plants, floral traits,
including flower size, are thought to co-evolve with pollinators. To attract pollinators, sex allocation theory predicts that
outcrossing species should invest more resources in floral display than self-pollinating species (Goodwillie et al., 2010). The
origin of selfing from an outcrossing ancestor has occurred
independently many times during angiosperm evolution
and is often associated with characteristic changes in floral
morphology that include reductions in flower size (reviewed
in Sicard and Lenhard, 2011). Species that self-pollinate
autonomously tend to have smaller flowers than both outcrossers and selfing species that require pollinator visitation
(Goodwillie et al., 2010). This pattern holds even within species when populations vary in mating system (reviewed in
Goodwillie et al., 2010). Small-flowered genotypes capable of
autonomous selfing can have a fitness advantage over larger
outcrossing genotypes when pollinators are rare (Elle and
Carney, 2003). Indeed, reproductive assurance can offset the
fitness costs of self-fertilization, resulting in populations with
mixed mating systems (Kalisz et al., 2004).
Flower size is often correlated with other floral traits that
increase pollinator visitation rates (Fenster et al., 2006). For
example, large flowers generally contain more nectar rewards
and are more conspicuous than smaller flowers (Blarer et al.,
2002; Fenster et al., 2006). Thus, pollinators tend to be more
attracted to larger than smaller flowers both within and
between plant species, and pollinator behaviour can impose
strong directional selection favouring large flowers in outcrossing plants (e.g., Bell, 1985; Conner and Rush, 1996; Dudash
et al., 2011; Elle and Carney, 2003; Galen, 1996; Glaettli and
Barrett, 2008; Harder and Johnson, 2009; Kingsolver et al.,
2001; Mojica and Kelly, 2010; Parachnowitsch and Kessler,
2010; Sandring and Ågren, 2009; Schemske and Ågren, 1995;
Stanton and Preston, 1988; Venail et al., 2010). Experimental
manipulations of flowers provide powerful support for
pollinator-mediated selection on flower size and other floral characteristics through both male (pollen transfer) and
female (fruit and seed set) components of reproductive success (Dudash et al., 2011; Fenster et al., 2004; Galen and
Cuba, 2001; Parachnowitsch and Kessler, 2010; Sandring and
Ågren, 2009).
Nevertheless, floral size evolution is not necessarily a
direct response to selection exerted by pollinators. For one,
large flowers can be disadvantageous for female fitness under
stressful conditions such as drought (Galen, 2000). Consistent
directional selection should deplete populations of variation
in ecologically relevant traits, yet natural populations maintain substantial genetic variation for flower size despite pollinator-mediated selection for larger flower size (Mojica and
Kelly, 2010; Mojica et al., 2012; Stanton and Preston, 1988;
Williams and Conner, 2001). The maintenance of genetic variation in flower size could result from genetic correlations with
other traits, environmental trade-offs, selection operating at
earlier life history stages, or antagonistic selection imposed
by floral enemies (Campbell, 2009; Galen, 2000; Mojica and
Kelly, 2010; Navarro and Medel, 2009; Parachnowitsch and
Caruso, 2008).
When reproductive success is used as the fitness component, the pattern of directional selection for larger flowers
holds in a diverse array of species (reviewed in Kingsolver
et al., 2001), including the ecological model Mimulus guttatus
(Phrymaceae) (Mojica and Kelly, 2010). However, viability
selection early in the life history of M. guttatus reverses the
overall direction of selection on flower size (Mojica and Kelly,
2010). Despite their fecundity advantage, large-flowered genotypes have a greater propensity to die before flowering than
small-flowered genotypes; by integrating viability and fecundity components of fitness, Mojica and Kelly (2010) found
that natural selection actually favours small-flowered genotypes. Thus, the genetic response to selection imposed by pollinators can be constrained by selection occurring at other life
history stages.
If pre-dispersal seed predators and nectar robbers diminish plant fecundity, selection exerted by these natural enemies
can counteract selection imposed by pollinators, further constraining floral trait evolution (Irwin et al., 2001; Navarro and
Medel, 2009; Parachnowitsch and Caruso, 2008). Predispersal
seed predators rely on the activities of pollinators to produce
seeds and can be attracted to the same floral traits as pollinators, decreasing the fitness of plants that invest in attractive
flowers (Parachnowitsch and Caruso, 2008). Natural enemies
can exert selection on floral traits, including flower shape, size
and phenology (Galen and Cuba, 2001; Irwin et al., 2001;
Parachnowitsch and Caruso, 2008). However, in a recent
Control of flower size | 1429
review, Parachnowitsch and Kessler (2010) found no difference in selection on floral traits (including flower size) in the
presence and absence of seed predators, suggesting that seed
predators are not strong agents of selection on flower size.
This result should be treated cautiously, as few studies have
manipulated natural enemies to test their effects on floral trait
evolution (Parachnowitsch and Kessler, 2010). To understand
the evolution of flower size and other traits in natural populations, it will probably be necessary to investigate the interactions of different agents of selection at multiple life history
stages and across growing seasons (Brody et al., 2008; Brunet
and Holmquist, 2009; Galen, 2000; Galen and Cuba, 2001;
Irwin, 2006; Mojica and Kelly, 2010).
Quantitative trait loci and the genetic basis
of flower size
Quantitative genetics studies of flower size have revealed
how natural selection operates at the level of the QTL and
have begun to dissect the genetic basis of this trait in model
organisms, natural populations of non-model species, as well
as cultivated species and their wild relatives (Bouck et al.,
2007; Bradshaw et al., 1995; Feng et al., 2009; Frary et al.,
2004; Galliot et al., 2006; Goodwillie et al., 2006; Hodges
et al., 2002; Juenger et al., 2000, 2005; Kelly and Mojica,
2011; Meagher et al., 2005; Mojica et al., 2012; Scoville
et al., 2011; Spigler et al., 2011). For example, Mojica and
colleagues (2012) found that alleles that promote large flowers in M. guttatus increase fecundity while depressing viability, consistent with earlier genotypic selection analyses
conducted at the organismal level (Mojica and Kelly, 2010).
Furthermore, epistatic interactions among QTLs can substantially influence segregating variation within a single population (Kelly and Mojica, 2011) and between species (Frary
et al., 2004). Similar to other quantitative traits, continuous
variation in flower size is most likely to be polygenic (Galliot
et al., 2006; Meagher et al., 2005), but QTL of major effect
on flower size variation have also been uncovered (Bouck
et al., 2007; Scoville et al., 2011; Venail et al., 2010). Finally,
some flower size QTL appear to be maintained at intermediate frequencies in natural populations by balancing selection
(Scoville et al., 2011).
Co-localization of QTL for integrated aspects of floral
organ size such as petal width and length as well as QTL
underlying the size of multiple floral organs have been
reported (Bouck et al., 2007; Fishman et al., 2002; Goodwillie
et al., 2006; Juenger, 2000). However, work in Lycopersicum
suggests that distinct genes regulate the size of sepals and petals (Frary et al., 2004). In addition, several studies document
co-localization of flower size QTL with QTL for other floral
and life history characteristics (Bouck et al., 2007; Fishman
et al., 2002; Goodwillie et al., 2006; Hermann and Kuhlemeier,
2011), including traits associated with sexual dimorphism
and male sterility on a proto-sex chromosome in Fragaria
virginiana (Spigler et al., 2011) and sex-determining loci in
Silene latifolia (Delph et al., 2010). Co-localization could
result from pleiotropy or tightly linked causal genes, either of
which could produce genetic correlations that constrain floral
trait evolution, such as the trade-off between flower size and
the number of flowers (Delph et al., 2004; Goodwillie et al.,
2010; Sargent et al., 2007; Spigler et al., 2011). Future endeavours that identify causal loci underlying key QTL will help
to elucidate the genetic architecture and basis of trait correlations, sexual dimorphism and perhaps even reproductive
isolation (Delph et al., 2010; Goodwillie et al., 2006; Hodges
et al., 2002; Schiestl and Schluter, 2009; Spigler et al., 2011).
Arabidopsis flower size control
Although A. thaliana is a selfing plant with relatively small
flowers, we believe that studies of this model species can
contribute to a general understanding of the genetic basis
of flower size. Most close relatives of Arabidopsis in the crucifer (Brassicaceae) family are self-incompatible (SI), and
selfing in Arabidopsis is thought to have arisen relatively
recently, approximately 1 million years ago (Tang et al.,
2007). Introduction of the male and female specificity determinants of self-incompatibility from SI Arabidopsis lyrata or
Capsella grandiflora into Arabidopsis confers self-incompatibility (reviewed in Rea et al., 2010). Using this transgenic
SI A. thaliana model, several genes have been identified that
influence both the self-incompatibility response and carpel
morphology, specifically enhanced elongation of the carpel
resulting in stigma exsertion (Tantikanjana and Nasrallah,
2012; Tantikanjana et al., 2009). Thus, factors involved in the
coordinated evolution of selfing and flower size appear to be
present within the Arabidopsis genome.
Furthermore, Arabidopsis ecotypes possess significant
genetic variation in flower size (Juenger et al., 2000, 2005).
Juenger et al. (2000) detected 18 QTL affecting at least one
aspect of flower size using Arabidopsis recombinant inbred
lines; several of these QTL mapped to regions containing
known regulators of organ size. In addition, several studies investigating the function of Arabidopsis genes in other
plants suggest conserved functions in regulating flower size.
For example, Antirrhinum majus flowers downregulated for
the growth-promoting gene AINTEGUMENTA (Am-ANT)
produce smaller floral organs, while the larger flowers of formosa (fo) mutants are associated with increased expression
of Am-ANT (Delgado-Benarroch et al., 2009; Kim et al.,
2011).
Genetic studies, primarily in Arabidopsis, suggest that many
different pathways act independently to determine flower
size, and that plant hormones and transcriptional regulation
play important roles in these pathways (Fig. 2) (reviewed in
Breuninger and Lenhard, 2010; Weiss et al., 2005). Many
of the identified size regulators control the growth of both
vegetative (leaves) and reproductive (flowers) lateral organs
that are formed on the flanks of the dome-shaped shoot apical meristem. Several excellent reviews on the genetic basis
of lateral organ size in general and leaves in particular have
been published recently (Gonzalez et al., 2012; Johnson and
Lenhard, 2011; Powell and Lenhard, 2012). Here we focus on
the genes that control floral organ size.
1430 | Krizek and Anderson
Fig. 2. Pathways regulating floral organ size in Arabidopsis. Top pictures show different stages of Arabidopsis flower development from
the time of sepal initiation (leftmost) to flower opening (rightmost). Bars representing the cell-proliferation and cell-elongation phases of
growth are shown below the corresponding stages of flower development. The known factors and pathways regulating cell proliferation
and/or cell expansion are summarized. Arrows indicate positive interactions while bars represent negative interactions. ca, carpel; pe,
petal, se, sepal; st, stamen; for gene and factor names see text.
Typical eudicot flowers are composed of four types of floral
organ – sepals, petals, stamens and carpels – with the size of
each organ dependent on both the number and size of the constituent cells. Founder cells give rise to floral organ primordia
at precise positions within the flower primordium. Growth of
these primordia into mature floral organs is thought to consist
of two partially overlapping phases (Fig. 2). Initial growth is
a result of cell proliferation with cells growing in size with
the synthesis of new cytoplasmic material and then dividing.
Later, cell proliferation often becomes restricted to particular
regions within a developing organ. During the second growth
phase, increases in floral organ size are largely a result of cell
expansion due to increases in the size of the plant vacuole.
Extremely large cell sizes present in some floral organs are
often a result of endoreduplication, in which cells undergo
multiple rounds of mitosis but do not divide, resulting in
polyploid cells (reviewed in Sugimoto-Shirasu and Roberts,
2003). In Arabidopsis, endoreduplication occurs in epidermal cells of sepals but has not been observed in other floral
organs (Galbraith et al., 1991; Roeder et al., 2010). However
in some species petal epidermal cells undergo endoreduplication, resulting in the production of very large cells (Kudo and
Kimura, 2001; Lee et al., 2004). Examination of Arabidopsis
mutants has revealed that changes in the rate and/or duration
of either the cell proliferation or cell expansion phases of
growth can be responsible for alterations in floral organ size
(reviewed in Powell and Lenhard, 2012).
Regulation of cell proliferation in
floral organs
One mechanism controlling final flower size involves the timing of cell proliferation arrest within developing floral organ
primordia. Extending the period in which cells are competent
to undergo cell division can result in larger floral organs as
seen in Arabidopsis plants constitutively expressing the auxininducible gene AUXIN-REGULATED GENE INVOLVED
IN ORGAN SIZE (ARGOS) or the gene encoding the AP2/
ERF type transcription factor AINTEGUMENTA (ANT)
(Hu et al., 2003; Krizek, 1999; Mizukami and Fischer, 2000).
Conversely, floral organs reach a smaller final size in plants
lacking ARGOS or ANT function (Elliott et al., 1996; Hu
et al., 2003; Klucher et al., 1996; Krizek, 1999; Mizukami
and Fischer, 2000). ARGOS and ANT appear to act in a
common auxin pathway regulating growth with ANT acting
downstream of ARGOS (Hu et al., 2003). ANT may act by
regulating the expression of cell-cycle genes such as CYCLIN
Control of flower size | 1431
D3;1 (CYCD3;1) but other targets are likely to be involved as
overexpression of CYCD3 does not result in the production
of larger floral organs (Dewitte et al., 2003; Mizukami and
Fischer, 2000).
Both ARGOS and ANT are members of gene families and
related proteins contribute to floral organ growth although
not always via effects on cell proliferation. Two proteins that
share a small motif and endoplasmic reticulum-localization
with ARGOS are ARGOS-LIKE (ARL) and ORGAN SIZE
RELATED1 (OSR1) (Feng et al., 2011). ARL promotes
organ growth through effects on cell expansion (Hu et al.,
2006). OSR1 primarily affects cell proliferation via maintenance of ANT expression in maturing lateral organs but
also promotes cell expansion independently of ANT (Feng
et al., 2011). Despite having overlapping functions in organ
growth, ARGOS, ARL and OSR1 are regulated by different
hormones, suggesting that these genes may integrate distinct
signals during organ growth (Fig. 2) (Feng et al., 2011; Hu
et al., 2003, 2006). At least two transcription factors of the
AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) family, which share high sequence similarity within the DNAbinding AP2 repeat region of ANT, can act redundantly with
ANT to regulate floral organ growth. ant ail6 double mutants
make smaller sepals (Krizek, 2009); conversely, misexpression
of AIL5 and AIL6 can result in the production of larger floral
organs (Krizek and Eaddy, 2012; Nole-Wilson et al., 2005).
Arabidopsis KLUH (KLU/CYP78A5), a cytochrome P450
monooxygenase, promotes floral growth by preventing the
premature arrest of cell proliferation within developing floral organs (Anastasiou et al., 2007). klu mutants produce
smaller floral organs with fewer cells while overexpression of
KLU results in larger flowers with more cells. Because KLU
expression during petal development does not match the spatial patterns of cell proliferation, KLU is thought to function
non-cell-autonomously through generation of a novel mobile
growth signal (Anastasiou et al., 2007). A KLU-derived signal
appears to move both within a flower and between flowers to
regulate organ growth at the whole flower or even whole inflorescence level (Eriksson et al., 2010). In this way, floral organ
growth may be coordinated in self-fertilizing Arabidopsis to
promote reproductive success.
The plant hormone cytokinin also affects the duration of
cell division within developing floral organs. Mutations in the
genes for two cytokinin degrading enzymes in Arabidopsis,
cytokinin oxidase/dehydrogenase CKX3 and CKX5, result in
larger floral organs due to the presence of more cells (Bartrina
et al., 2011). In transgenic petunia, expression of a cytokinin
biosynthetic gene under the control of a flower-specific promoter results in larger flowers primarily due to increased cell
number (Verdonk et al., 2008). These results indicate that
cytokinin promotes floral organ growth but the downstream
effectors in this pathway have not been identified. While high
cytokinin levels promote floral organ growth, no effect on
flower size was observed in Arabidopsis plants in which cytokinin levels were reduced, even though these plants produce
smaller leaves than the wild-type (Holst et al., 2011).
Cell division within floral organs is also promoted by
GROWTH-REGULATING FACTORS (GRFs) and
GRF-INTERACTING FACTORs (GIFs), which function
as transcription factors and co-activators, respectively, that
physically interact (Kim et al., 2003; Kim and Kende, 2004).
Mutations in these genes result in smaller petals owing to
reduced numbers of cells (Horiguchi et al., 2005; Kim and
Kende, 2004; Lee et al., 2009). These proteins appear to have
partly overlapping functions in floral organ growth as higherorder mutants generally show more severe defects. Kinematic
analyses of leaf growth in gif single and higher-order mutants
indicates that GIFs regulate both the rate and duration of cell
proliferation but once again this has not been examined in
floral organs (Lee et al., 2009).
Several genes have been identified that restrict the duration
of the cell proliferation phase of floral organ growth. These
include the Arabidopsis genes BIG BROTHER (BB), which
encodes an E3 ubiquitin-ligase, as well as DA1 and DAR1,
which encode putative ubiquitin receptors (Disch et al., 2006;
Li et al., 2008). Mutations in these genes result in larger floral organs while increased expression of these genes results
in floral organs that reach a smaller final size. The identification of these proteins suggests that the ubiquitin-proteasome
protein-degradation pathway plays a role in organ size control and that BB and DA1 act via proteolysis of growth-promoting factors, but no substrates of BB activity have been
identified.
Members of the TCP (TEOSINTE BRANCHED/
CYCLOIDEA/PCF) transcription factor family regulate
growth within developing plant organs (reviewed in MartinTrillo and Cubas, 2009). There are two major groups of TCP
genes with class I genes acting as promoters of leaf growth
and class II genes repressing leaf growth. Mutations in class II
genes result in larger leaves that have a crinkled appearance
resulting from altered cell proliferation patterns during leaf
development (Nath et al., 2003; Schommer et al., 2008). While
the class II Antirrhinum gene CINCINNATA (CIN) restricts
growth in leaves, it promotes cell division and growth of the
petal lobe as well as the differentiation of conical cells on the
epidermal surface (Crawford et al., 2004). Thus, some TCP
genes can have opposite effects on growth in different tissues.
In contrast to CIN, Arabidopsis TCP4 represses petal growth.
This role was revealed by the isolation of a loss of function
mutation in miR319a129, which downregulates five TCP genes
(TCP2, TCP3, TCP4, TCP10 and TCP24) in flowers (Nag
et al., 2009). The narrow-petal phenotype of miR319a129 was
partly suppressed by expression of a tcp4 allele containing
a mutation in the miRNA-binding site complementary to
the miR319a129 mutation. The cellular basis for the narrowpetal phenotype has not been reported but may result from a
reduced number of cells based on the known involvement of
TCP genes in cell proliferation.
Regulation of cell expansion in
floral organs
Besides the previously mentioned organ growth promoter
ARL, several other factors are known to regulate floral organ
size primarily by affecting cell size. Two of these factors are
1432 | Krizek and Anderson
components of Mediator, a multiprotein complex involved
in transcription regulation that acts as an adapter between
transcription factors bound to regulatory elements and the
general transcription machinery. MED25 acts to restrict
floral organ growth via effects primarily on cell expansion but with some effects on cell proliferation (Xu and Li,
2011). Increased cell growth in med25 mutants may be due
to increased expression of several expansin genes (Xu and
Li, 2011) that mediate cell wall loosening during cell expansion (Cosgrove, 2000). Petunia plants downregulated for the
expansin gene PhEXPA1 produce flowers with smaller petal
limbs due to smaller cells while overexpression of PhEXPA1
leads to larger petal limbs as a result of larger cells (Zenoni
et al., 2004, 2011).
While MED25 is a repressor of floral organ growth, two
other Mediator subunits – MED8 and STRUWWELPETER
(SWP)/MED14 – promote growth (Autran et al., 2002; Xu
and Li, 2012). MED8 regulates organ growth via cell expansion while SWP regulates cell proliferation during early
stages of organogenesis. It is possible that distinct Mediator
complexes regulate the transcription of different sets of
growth-regulatory genes in response to different signals (Xu
and Li, 2012).
Floral organ-specific regulators of growth
Few factors that regulate growth in a specific floral organ
have been identified. BIGPETAL (BPE), a basic helix-loophelix (bHLH) transcription factor, restricts the expansion
of petal cells (Szecsi et al., 2006). BPE undergoes alternate
splicing to generate two transcripts: a ubiquitously expressed
BPEub and a petal-specific BPEp transcript. Both transcripts
encode proteins containing the bHLH domain but with distinct C-terminal regions that appear to be functionally important. The C-terminal domain of BPEp interacts with AUXIN
RESPONSE FACTOR8 (ARF8) and mutations in ARF8
also result in larger petals (Varaud et al., 2011). The increased
size of arf8 petals appears to result from both increases in
cell size and cell number (Varaud et al., 2011). bpe arf8 double mutants produce petals larger than either single mutant
alone; this does not result from further increases in cell size
but an increased number of cells. Thus BPEp and ARF8 may
work in distinct pathways early in petal development to limit
the period of cell proliferation but later work together to limit
cell expansion (Varaud et al., 2011).
Floral organ identity proteins and the
regulation of floral organ growth
Primordia on the flanks of the Arabidopsis reproductiveshoot apical meristem adopt a floral fate due to the activity
of a transcription factor called LEAFY (LFY) (Weigel et al.,
1992). Within a flower primordium, LFY acts in combination
with other factors to establish the spatially restricted expression patterns of four classes of floral organ identity genes
(also called floral homeotic genes) that specify the distinct
identities of floral organ primordia (reviewed in Siriwardana
and Lamb, 2012). The ABCE model describes the distinct
combination of floral organ identity gene activities that
specify sepal (A+E), petal (A+B+E), stamen (B+C+E) and
carpel (C+E) identities in each whorl of the flower (reviewed
in Krizek and Fletcher, 2005). The class A gene APETALA1
(AP1), class B genes APETALA3 (AP3) and PISTILLATA
(PI), class C gene AGAMOUS (AG) and class E SEPALLATA
genes (SEP1–4) encode MADS domain transcription factors
while the class A gene APETALA2 (AP2) encodes an AP2/
ERF transcription factor. These transcription factors are
expressed throughout floral organ development and identification of their regulatory targets reveals that these proteins control distinct processes during floral organogenesis
(Gomez-Mena et al., 2005; Ito et al., 2004, 2007; Wuest et al.,
2012).
Genome-wide approaches such as chromatin immunoprecipitation in combination with high-throughput sequencing
(ChIP-Seq) have identified many floral organ size regulators
as targets of LFY and the floral organ identity proteins AP1,
AP3, PI and SEP3 (Table 1). In addition to specifying a floral fate, LFY appears to regulate early growth of the flower
primordium by directly binding to growth-regulatory targets
(Moyroud et al., 2011; Winter et al., 2011). LFY also activates expression of the floral homeotic genes whose proteins
themselves regulate floral organ size factors during flower
development (Kaufmann et al., 2009, 2010; Moyroud et al.,
2011; Winter et al., 2011; Wuest et al., 2012). The identification of target genes that encode factors regulating both cell
proliferation and cell expansion is consistent with the floral
homeotic proteins controlling growth during both early and
late stages of flower development. Genetic support for this
role in organ growth is provided by Antirrhinum compacta
(co) mutants that produce smaller petals due to reduction
in class B activity during late stages of petal development
(Manchado-Rojo et al., 2012). Growth within floral organ
primordia is thus tightly coupled with the establishment of
organ identity and the elaboration of floral form (reviewed in
Dornelas et al., 2010).
Conclusions and future directions
Flower size is an important trait that affects mating system
evolution and fitness. Within a species, variation in flower
size and other floral traits can promote reproductive isolation and ultimately speciation. Although pollinators often
prefer larger flowers, the evolution of flower size can be constrained by selection imposed by natural enemies, selection
that occurs at earlier plant life history stages, and/or genetic
trade-offs. Identifying the complex suite of abiotic and biotic
agents of selection that sculpt floral evolution remains challenging. Another important future goal will be to elucidate
the genetic basis of flower size variation in natural plant
populations. QTL cloning in model and non-model species
as well as testing of candidate genes identified in Arabidopsis
will contribute towards achieving this goal. Such studies may
reveal genes that enable population divergence and influence
plant–pollinator interactions. Furthermore, they will begin
Control of flower size | 1433
Table 1. Growth-regulatory proteins that are targets of LFY or
the floral organ identity proteins (AP1, AP3, PI and SEP 3) as
identified in ChIP-Seq experiments. LFY
Cell proliferation
ANT
AIL5
AIL6
ARGOS
BB
DA1
DAR
GIF1 (AN3)
GIF2
GIF3
GRF1
GRF2
GRF3
GRF4
GRF5
GRF6
GRF7
GRF8
GRF9
JAG
KLU
NUB
OSR1
SWP
TCP4
Cell expansion
ARF8
ARL
BPEp
MED8
MED25
AP1
AP3
PI
X
X
X
X
X
X
X
X
X
X
X
X
X
SEP3
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Andersson S. 2012. Does inbreeding promote evolutionary
reduction of flower size? Experimental evidence from Crepis
tectorum (Asteraceae). American Journal of Botany 99,
1388–1398.
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Autran D, Jonak C, Belcram K, Beemster GTS, Kronenberger
J, Grandjean O, Inze D, Traas J. 2002. Cell numbers and
leaf development in Arabidopsis: a functional analysis of the
STRUWWELPETER gene. The EMBO Journal 21, 6036–6049.
Bartrina I, Otto E, Strnad M, Werner T, Schmulling T. 2011.
Cytokinin regulates the activity of reproductive meristems, flower
organ size, ovule formation, and thus seed yield in Arabidopsis
thaliana. The Plant Cell 23, 69–80.
Bell G. 1985. On the function of flowers. Proceedings of the Royal
Society B Biological Sciences 224, 223–265.
Blarer A, Keasar T, Shmida A. 2002. Possible mechanisms for the
formation of flower size preferences by foraging bumblebees. Ethology
108, 341–351.
Bouck AC, Wessler SR, Arnold ML. 2007. QTL analysis of floral
traits in Louisiana iris hybrids. Evolution 61, 2308–2319.
X
X
X
Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J,
Fleck C, Lenhard M. 2007. Control of plant organ size by KLUH/
CYP78A5-dependent intercellular signaling. Developmental Cell 13,
843–856.
Anderson JT, Willis JH, Mitchell-Olds T. 2011. Evolutionary
genetics of plant adaptation. Trends in Genetics 27, 258–266.
X
X
References
X
Data sets from the following references were examined (Kaufmann
et al., 2009; Kaufmann et al., 2010; Moyroud et al., 2011; Wuest
et al., 2012).
to indicate the degree to which studies in Arabidopsis contribute to a general understanding of the genetic control of
flower size. While numerous Arabidopsis genes regulating floral organ size have been identified through molecular genetic
studies, many questions remain about the pathways in which
these proteins function. A number of these growth-regulatory factors encode transcription factors, but few targets of
these transcription factors are known. Identification of such
targets will be helpful in revealing the molecular and cellular mechanisms by which these proteins control growth in
flowers.
Acknowledgements
Work in the Krizek lab is supported by National Science
Foundation (NSF) grant IOS 0922367. Work in the Anderson
lab is supported by start-up funds from the University of
South Carolina.
Bradshaw HD, Wilbert SM, Otto KG, Schemske DW. 1995.
Genetic mapping of floral traits associated with reproductive isolation
in monkeyflowers (Mimulus). Nature 376, 762–765.
Breuninger H, Lenhard M. 2010. Control of tissue and organ growth
in plants. Current Topics in Developmental Biology 91, 185–220.
Brody A, Irwin RE, McCutcheon M, Parsons E. 2008. Interactions
between nectar robbers and seed predators mediated by a shared
host plant, Ipomopsis aggregata. Oecologia 155, 75–84.
Brunet J. 2009. Pollinators of the Rocky Mountain columbine:
temporal variation, functional groups and association with floral traits.
Annals of Botany 103, 1567–1578.
Brunet J, Holmquist KGA. 2009. The influence of distinct pollinators
on female and male reproductive success in the rocky mountain
columbine. Molecular Ecology 18, 3745–3758.
Campbell DR. 2009. Using phenotypic manipulations to study
multivariate selection of floral trait associations. Annals of Botany 103,
1557–1566.
Conner J, Rush SL. 1996. Effects of flower size and number on
pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia
105, 509–516.
Cosgrove DJ. 2000. Loosening of plant cell walls by expansins.
Nature 407, 321–326.
Crawford BCW, Nath U, Carpenter R, Coen E. 2004. CINCINNATA
controls both cell differentiation and growth in petal lobes and leaves
of Antirrhinum. Plant Physiology 135, 244–253.
Davis CC, Endress PK, Baum DA. 2008. The evolution of floral
gigantism. Current Opinions in Plant Biology 11, 49–57.
1434 | Krizek and Anderson
Delgado-Benarroch L, Causier B, Weiss J, Egea-Cortines M.
2009. FORMOSA controls cell division and expansion during floral
development in Antirrhinum majus. Planta 229, 1219–1229.
Delph LF, Gehring JL, Frey FM, Arntz AM, Levri M. 2004. Genetic
constraints on floral evolution in a sexually dimorphic plant revealed by
artificial selection. Evolution 58, 1936–1946.
Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I. 2010. The
genomic architecture of sexual dimorphism in the dioecious plant
Silene latifolia. Evolution 64, 2873–2886.
Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard
A, Kilby NJ, Murray JAH. 2003. Altered cell cycle distribution,
hyperplasia, and inhibited differentiation in Arabidopsis caused by the
D-type cyclin CYCD3. The Plant Cell 15, 79–92.
Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC,
Lenhard M. 2006. The E3 ubiquitin ligase BIG BROTHER controls
arabidopsis organ size in a dosage-dependent manner. Current
Biology 16, 272–279.
Dornelas MC, Patreze CM, Angenent GC, Immink RGH. 2010.
MADS: the missing link between identity and growth. Trends in Plant
Science 16, 89–97.
Dudash MR, Hassler C, Stevens PM, Fenster CB. 2011.
Experimental floral and inflorescence trait manipulations affect
pollinator preference and function in a hummingbird-pollinated plant.
American Journal of Botany 98, 275–282.
Elle E, Carney R. 2003. Reproductive assurance varies with flower
size in Collinsia parviflora (Scrophulariaceae). American Journal of
Botany 90, 888–896.
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ,
Gerentes D, Perez P, Smyth DR. 1996. AINTEGUMENTA, an
APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule
development and floral organ growth. The Plant Cell 8, 155–168.
Endress PK. 2011. Evolutionary diversification of the flowers of
angiosperms. American Journal of Botany 98, 370–396.
Galbraith DW, Harkins KR, Knapp S. 1991. Systemic
endopolyploidy in Arabidopsis thaliana. Plant Physiology 96, 985–989.
Galen C. 1996. Rates of floral evolution: Adaptation to bumblebee
pollination in an alpine wildflower, Polemonium viscosum. Evolution
50, 120–125.
Galen C. 2000. High and dry: drought stress, sex-allocation tradeoffs, and selection on flower size in the alpine wildflower Polemonium
viscosum. American Naturalist 156, 72–83.
Galen C, Cuba J. 2001. Down the tube: pollinators, predators,
and the evolution of flower shape in the alpine skypilot, Polemonium
viscosum. Evolution 55, 1963–1971.
Galliot C, Hoballah ME, Kuhlemeier C, Stuurman J. 2006.
Genetics of flower size and nectar volume in Petunia pollination
syndromes. Planta 225, 203–212.
Glaettli M, Barrett S. 2008. Pollinator response to variation in floral
display and flower size in dioecious Sagittaria latifolia (Alismataceae).
New Phytologist 179, 1193–1201.
Gomez-Mena C, de Folter S, Costa MMR, Angenent GC,
Sablowski R. 2005. Transcriptional program controlled by the floral
homeotic gene AGAMOUS during early organogenesis. Development
132, 429–438.
Gong Y-B, Huang S-Q. 2009. Floral symmetry: pollinator-mediated
stabilizing selection on flower size in bilateral species. Proceedings of
the Royal Society B Biological Sciences 276, 4013–4020.
Gonzalez N, Vanhaeren H, Inze D. 2012. Leaf size control: complex
coordination of cell division and expansion. Trends in Plant Science
17, 332–340.
Goodwillie C, Ritland C, Ritland K. 2006. The genetic basis of
floral traits associated with mating system evolution in Leptosiphon
(Polemoniaceae): an analysis of Quantitative Trait Loci. Evolution 60,
491–504.
Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard
M. 2010. KLUH/CYP78A5-dependent growth signaling coordinates
floral organ growth in Arabidopsis. Current Biology 20, 527–532.
Goodwillie C, Sargent R, Eckert CG, Elle E, Geber M, Johnston
MO, Kalisz S, Moeller DA, Ree RH, Vallejo-Marin M, Winn AA.
2010. Correlated evolution of mating system and floral display traits
in flowering plants and its implications for the distribution of mating
system variation. New Phytologist 185, 311–321.
Feng G, Qin Z, Yan J, Zhang X, Hu Y. 2011. Arabidopsis ORGAN
SIZE RELATED1 regulates organ growth and final organ size in
orchestration with ARGOS and ARL. New Phytologist 191, 635–646.
Harder L, Johnson S. 2009. Darwin’s beautiful contrivances:
evolutionary and functional evidence for floral adaptation. New
Phytologist 183, 530–545.
Feng X, Wilson Y, Bowers J, Kennaway R, Bangham A, Hannah
A, Coen E, Hudson A. 2009. Evolution of Allometry in Antirrhinum.
The Plant Cell 21, 2999–3007.
Hermann K, Kuhlemeier C. 2011. The genetic architecture of
natural variation in flower morphology. Current Opinion in Plant Biology
14, 60–65.
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson
JD. 2004. Pollination syndromes and floral specialization. Annual
Review of Ecology and Systematics 35, 375–403.
Hodges SA, Whittall JB, Fulton M, Yang JY. 2002. Genetics
of floral traits influencing reproductive isolation between Aquilegia
formosa and Aquilegia pubescens. American Naturalist 159,
S51–S60.
Fenster CB, Cheeley G, Dudash MR, Reynolds RJ. 2006. Nectar
reward and advertisement in hummingbird-pollinated Silene virginica
(Caryophyllaceae). American Journal of Botany 93, 1800–1807.
Fishman L, Kelly AJ, Willis JH. 2002. Minor quantitative trait loci
underlie floral traits associated with mating system divergence in
Mimulus. Evolution 56, 2138–2155.
Frary A, Fritz LA, Tanksley SD. 2004. A comparative study of the
genetic bases of natural variation in tomato leaf, sepal, and petal
morphology. Theoretical and Applied Genetics 109, 523–533.
Holst K, Schmulling T, Werner T. 2011. Enhanced cytokinin
degradation in leaf primordia of transgenic Arabidopsis plants reduces
leaf size and shoot organ primordia formation. Journal of Plant
Physiology 168, 1328–1334.
Horiguchi G, Kim GT, Tsukaya H. 2005. The transcription
factor AtGRF5 and the transcription coactivator AN3 regulate cell
proliferation in leaf primordia of Arabidopsis thaliana. The Plant Journal
43, 68–78.
Control of flower size | 1435
Hu Y, Xie A, Chua N-H. 2003. The Arabidopsis auxin-inducible gene
ARGOS controls lateral organ size. The Plant Cell 15, 1951–1961.
phenotypic selection in natural populations. The American Naturalist
157, 245–261.
Hu Y, Poh HM, Chua N-H. 2006. The Arabidopsis ARGOS-LIKE
gene regulates cell expansion during organ growth. The Plant Journal
47, 1–9.
Klucher KM, Chow H, Reiser L, Fischer RL. 1996. The
AINTEGUMENTA gene of Arabidopsis required for ovule and female
gametophyte development is related to the floral homeotic gene
APETALA2. The Plant Cell 8, 137–153.
Irwin RE. 2006. Consequences of direct versus indirect species
interactions to selection on traits: pollination and nectar robbing in
Ipomopsis aggregata. American Naturalist 167, 315–328.
Irwin RE, Brody A, Waser NM. 2001. The impact of floral larceny on
individuals, populations, and communities. Oecologia 129, 161–168.
Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M,
Riechmann JL, Meyerowitz EM. 2004. The homeotic
protein AGAMOUS controls microsporogenesis by regulation of
SPOROCYTELESS. Nature 430, 356–360.
Ito T, Ng K-H, Lim T-S, Yu H, Meyerowitz EM. 2007. The homeotic
protein AGAMOUS controls late stamen development by regulating
a jasmonate biosynthetic gene in Arabidopsis. The Plant Cell 19,
3516–3529.
Johnson K, Lenhard M. 2011. Genetic control of plant organ
growth. New Phytologist 191, 319–333.
Juenger T, Purugganan M, Mackay TFC. 2000. Quantitative
trait loci for floral morphology in Arabidopsis thaliana. Genetics 156,
1379–1392.
Juenger T, Perez-Perez JM, Bernal S, Micol JL. 2005.
Quantitative trait loci mapping of floral and leaf morphology traits
in Arabidopsis thaliana: evidence for modular genetic architecture.
Evolution and Development 7, 259–271.
Kalisz S, Vogler DW, Hanley KM. 2004. Context-dependent
autonomous self-fertilization yields reproductive assurance and mixed
mating. Nature 430, 884–887.
Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C,
Krajewski P, Angenent GC. 2009. Targets of the transcription factor
SEPALLATA3: integration of developmental and hormonal pathways in
the Arabidopsis flower. PLoS Biology 7, e1000090.
Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar
V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM,
Angenent GC, Riechmann JL. 2010. Orchestration of floral initiation
by APETALA1. Science 328, 85–89.
Kelly JK, Mojica JP. 2011. Interactions among flower-size QTL of
Mimulus guttatus are abundant but highly variable in nature. Genetics
189, 1461–1471.
Kim BM, Inaba J-I, Masuta C. 2011. Virus induced gene silencing
in Antirrhinum majus using the Cucumber Mosais Virus vector:
Functional analysis of the AINTEGUMENTA (Am-ANT) gene of
A. majus. Horticulture, Environment, and Biotechnology 52, 176–182.
Kim JH, Kende H. 2004. A transcriptional coactivator, AtGIF1, is
involved in regulating leaf growth and morphology in Arabidopsis.
Proceedings of the National Academy of Sciences USA 101,
13374–13379.
Kim JH, Choi D, Kende H. 2003. The AtGRF family of putative
transcription factors is involved in leaf and cotyledon growth in
Arabidopsis. The Plant Journal 36, 94–104.
Kingsolver J, Hoekstra H, Hoekstra J, Berrigan D, Vignieri
S, Hill C, Hoang A, Gibert P, Beerli P. 2001. The strength of
Krizek BA. 1999. Ectopic expression of AINTEGUMENTA in
Arabidopsis plants results in increased growth of floral organs.
Developmental Genetics 25, 224–236.
Krizek BA. 2009. AINTEGUMENTA and AINTEGUMENTA-LIKE6 act
redundantly to regulate Arabidopsis floral growth and patterning. Plant
Physiology 150, 1916–1929.
Krizek BA, Fletcher JC. 2005. Molecular mechanisms of flower
development: an armchair guide. Nature Review Genetics 6, 688–698.
Krizek BA, Eaddy M. 2012. AINTEGUMENTA-LIKE6 regulates
cellular differentiation in flowers. Plant Molecular Biology 78,
199–209.
Kudo N, Kimura Y. 2001. Flow cytometric evidence for
endopolyploidization in cabbage (Brassica oleracea L.) flowers. Sexual
Plant Reproduction 13, 279–283.
Langlade NB, Feng X, Dransfield T, Copsey L, Hanna AI,
Thebaud C, Bangham A, Hudson A, Coen E. 2005. Evolution
through genetically controlled allometry space. Proceedings of the
National Academy of Sciences USA 102, 10221–10226.
Lee BH, Ko J-H, Lee S, Lee Y, Pak J-H, Kim JH. 2009. The
Arabidopsis GRF-INTERACTING FACTOR gene family performs an
overlapping function in determining organ size as well as multiple
developmental properties. Plant Physiology 151, 655–668.
Lee HC, Chiou DW, Chen WH, Markhart AH, Chen YH, Lin TY.
2004. Dynamics of cell growth and endoreduplication during orchid
flower development. Plant Science 166, 659–667.
Li Y, Zheng L, Corke F, Smith C, Bevan MW. 2008. Control of final
seed and organ size by the DA1 gene family in Arabidopsis thaliana.
Genes and Development 22, 1331–1336.
Manchado-Rojo M, Delgado-Benarroch L, Roca MJ, Weiss
J, Egea-Cortines M. 2012. Quantitative levels of Deficiens
and Globosa during late petal development show a complex
transcriptional network topology of B function. The Plant Journal 72,
294–307.
Martin-Trillo M, Cubas P. 2009. TCP genes: a family snapsot ten
years later. Trends in Plant Science 15, 31–39.
Meagher TR, Gillies ACM, Costich DE. 2005. Genome size,
quantitative genetics and the genomic basis for flower size evolution in
Silene latifolia. Annals of Botany 95, 247–254.
Mizukami Y, Fischer RL. 2000. Plant organ size control:
AINTEGUMENTA regulates growth and cell numbers during
organogenesis. Proceedings of the National Academy of Sciences
USA 97, 942–947.
Mojica JP, Kelly JK. 2010. Viability selection prior to trait expression
is an essential component of natural selection. Proceedings of the
Royal Society B Biological Sciences 277, 2945–2950.
Mojica JP, Lee YW, Willis J, Kelly JK. 2012. Spatially and
temporally varying selection on intrapopulation quantitative trait loci for
a life history trade-off in Mimulus guttatus. Molecular Ecology 21.
1436 | Krizek and Anderson
Moyroud E, Minguet EG, Ott F, Yant L, Pose D, Monniaux M,
Blanchet S, Bastien O, Thevenon E, Weigel D, Schmid M, Parcy
F. 2011. Prediction of regulatory interactions from genome sequences
using a biophysical model for the Arabidopsis LEAFY transcription
factor. The Plant Cell 23, 1293–1306.
Nag A, King S, Jack T. 2009. miR319a targeting of TCP4 is critical
for petal growth and development in Arabidopsis. Proceedings of the
National Academy of Sciences USA 106, 22534–22539.
Nath U, Crawford BCW, Carpenter R, Coen E. 2003. Genetic
control of surface curvature. Science 299, 1404–1407.
Navarro L, Medel R. 2009. Relationship between floral tube length
and nectar robbing in Duranta erecta L. (Verbenaceae). Biological
Journal of the Linnean Society 96, 392–398.
Nole-Wilson S, Tranby T, Krizek BA. 2005. AINTEGUMENTAlike (AIL) genes are expressed in young tissues and may specify
meristematic or division-competent states. Plant Molecular Biology
57, 613–628.
Olson-Manning C, Wagner MR, Mitchell-Olds T. 2012. Adaptive
evolution: evaluating empirical support for theoretical predictions.
Nature Reviews Genetics 13.
Parachnowitsch AL, Caruso CM. 2008. Predispersal seed
herbivores, not pollinators, exert selection on floral traits via female
fitness. Ecology 89, 1802–1810.
Parachnowitsch AL, Kessler A. 2010. Pollinators exert natural
selection on flower size and floral display in Penstemon digitalis. New
Phytologist 188, 393–402.
Powell AE, Lenhard M. 2012. Control of organ size in plants.
Current Biology 22, R360–R367.
Rea AC, Liu P, Nasrallah JB. 2010. A transgenic self-incompatible
Arabidopsis thaliana model for evolutionary and mechanistic studies
of crucifer self-incompatibility. Journal of Experimental Botany 61,
1897–1906.
Roeder AHK, Chickarmane V, Cunha A, Obara B, Manjunath
BS, Meyerowitz EM. 2010. Variability in the control of cell division
underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS
Biology 8, e1000367.
Sandring S, Ågren J. 2009. Pollinator-mediated selection on floral
display and flowering time in the perennial herb Arabidopsis lyrata.
Evolution 63, 1292–1300.
Sargent R, Goodwillie C, Kalisz S, Ree R. 2007. Phylogenetic
evidence for a flower size and number trade-off. American Journal of
Botany 94, 2059–2062.
Schemske DW, Ågren J. 1995. Deceit pollination and selection on
female flower size in Begonia involucrata: An experimental approach.
Evolution 49, 207–214.
Schiestl FP, Schluter PM. 2009. Floral isolation, specialized
pollination, and pollinator behavior in orchids. Annual Review of
Entomology 54, 425–446.
Sicard A, Lenhard M. 2011. The selfing syndrome: a model
for studying the genetic and evolutionary basis of morphological
adaptation in plants. Annals of Botany 107, 1433–1443.
Siriwardana NS, Lamb RS. 2012. The poetry of reproduction: the
role of LEAFY in Arabidopsis thaliana flower formation. International
Journal of Developmental Biology 56, 207–221.
Spigler RB, Lewers KS, Ashman TL. 2011. Genetic architecture
of sexual dimorphism in a subdioecious plant with a proto-sex
chromosome. Evolution 65, 1114–1126.
Stanton ML, Preston RE. 1988. Ecological consequences and
phenotypic correlates of petal size variation in wild radish, Raphanus
sativus (Brassicaceae). American Journal of Botany 75, 528–539.
Sugimoto-Shirasu K, Roberts K. 2003. “Big it up”:
endoreduplication and cell-size control in plants. Current Opinions in
Plant Biology 6, 544–553.
Szecsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C,
Bendahmane M. 2006. BIGPETALp, a bHLH transcription factor is
involved in the control of Arabidopsis petal size. The EMBO Journal
25, 3912–3920.
Tang C, Toomajian C, Sherman-Broyles S, Plagnol V, Guo
Y-L, Hu TT, Clark RM, Nasrallah JB, Weigel D, Nordborg M.
2007. The evolution of selfing in Arabidopsis thaliana. Science 317,
1070–1072.
Tantikanjana T, Nasrallah JB. 2012. Non-cell-autonomous
regulation of crucifer self-incompatibility by Auxin Response Factor
ARF3. Proceedings of the National Academy of Sciences USA 109,
19468–19473.
Tantikanjana T, Rizvi N, Nasrallah ME, Nasrallah JB. 2009. A dual
role for the S-locus receptor kinase in self-incompatibility and pistil
development revealed by an Arabidopsis rdr6 mutation. The Plant Cell
21, 2642–2654.
Varaud E, Brioudes F, Szecsi J, Leroux J, Brown S, PerrotRechenmann C, Bendahmane M. 2011. AUXIN RESPONSE
FACTOR8 regulates Arabidopsis petal growth by interacting with the
bHLH transcription factor BIGPETALp. The Plant Cell 23, 973–983.
Venail J, Dell’Olivo A, Kuhlemeier C. 2010. Speciation genes in
the genus Petunia. Philosophical Transactions of the Royal Society B
Biological Sciences 365, 461–468.
Verdonk JC, Shibuya K, Loucas HM, Colquhoun TA, Underwood
BA, Clark DG. 2008. Flower-specific expression of the Agrobacterium
tumefaciens isopentenyltransferase gene results in radial expansion
of floral organs in Petunia hybrida. Plant Biotechnology Journal 6,
694–701.
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM.
1992. LEAFY controls floral meristem identity in Arabidopsis. Cell 69,
843–859.
Weiss J, Delgado-Benarroch L, Egea-Cortines M. 2005. Genetic
control of floral size and proportions. Int. J. Dev. Biol . 49, 513–525.
Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P,
Farmer EE, Nath U, Weigel D. 2008. Control of jasmonate biosynthesis
and senescence by miR3189 targets. PLoS Biology 6, e230.
Williams JL, Conner JK. 2001. Sources of phenotypic variation
in floral traits in wild radish, Raphanus raphanistrum (Brassicaceae).
American Journal of Botany 88, 1577–1581.
Scoville AG, Lee YW, Willis JH, Kelly JK. 2011. Explaining the
heritability of an ecologically significant trait in terms of individual
quantitative trait loci. Biology Letters 7, 896–898.
Winter CM, Austin RS, Blanvillain-Baufume S, Raeback MA,
Monniaux M, Wu M-F, Sang Y, Yamaguchi N, Parker JE, Parcy
F, Jensen ST, Hongzhe L, Wagner D. 2011. LEAFY target genes
Control of flower size | 1437
reveal floral regulatory logic, cis motifs, and a link to biotic stimulus
response. Cell 20, 430–443.
Xu R, Li Y. 2012. The Mediator complex subunit 8 regulates organ
size in Arabidopsis thaliana. Plant Signaling and Behavior 7, 182–183.
Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH.
2008. Mimulus is an emerging model system for the integration of
ecological and genomic studies. Heredity 100, 220–230.
Zenoni S, Reale L, Tornielli GB, Lanfaloni L, Porceddu A, Ferrarini
A, Moretti C, Zamboni A, Speghini A, Ferranti F, Pezzotti M.
2004. Downregulation of the Petunia hybrida α-expansin gene PhEXP1
reduces the amount of crystalline cellulose in cell walls and leads to
phenotypic changes in petal limbs. The Plant Cell 16, 295–308.
Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli
A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F. 2012.
Molecular basis for the specification of floral organs by APETALA3 and
PISTILLATA. Proceedings of the National Academy of Sciences USA
109, 13452–13457.
Xu R, Li Y. 2011. Control of final organ size by Mediator complex
subunit 25 in Arabidopsis thaliana. Development 138, 4545–4554.
Zenoni S, Fasoli M, Tornielli GB, Dal Santo S, Sanson A,
de Groot P, Sordo S, Citterio S, Monti F, Pezzotti M. 2011.
Overexpression of PhEXPA1 increases cell size, modifies cell wall
polymer composition and affects the timing of axillary meristem
development in Petunia hybrida. New Phytologist 191, 662–677.