Annals of Botany 107: 1427– 1431, 2011

doi:10.1093/aob/mcr122, available online at www.aob.oxfordjournals.org

PREFACE: PART OF A SPECIAL ISSUE ON EVOLUTION AND DEVELOPMENT

The evolution of flower development: current understanding and
future challenges
Annette Becker 1, Karine Alix 2 and Catherine Damerval 3,*
1
University of Bremen, Evolutionary Developmental Genetics Group, Leobener Str., UFT, 28359 Bremen, Germany,
2
AgroParisTech and 3CNRS – UMR 0320/8120 Génétique Végétale INRA/Univ. Paris-Sud/CNRS/AgroParisTech, Ferme du
Moulon, F-91190 Gif-sur-Yvette, France
* For correspondence. E-mail damerval@moulon.inra.fr

One of the most fascinating questions in evolutionary biology
is understanding how novelties such as new organs or novel
body plans arise. Answering this question is all the more chal-
lenging as obvious predecessors cannot always be identified in
the incomplete fossil record. Evolutionary developmental
(evo-devo) studies address this issue by examining how devel-
opmental mechanisms have evolved over time. To undertake
such studies, rigorous assessment of trait homology (i.e. inher-
ited from a common ancestral trait) is necessary, and this can
now be conducted in a robust phylogenetic framework thanks
to the remarkable recent progress in molecular systematics
(e.g. APG III, 2009; Moore et al., 2010). Close examination
of the sequence of developmental events underlying homolo-
gous traits, and the genes regulating developmental changes,
is critical to our understanding of the present state and evol-
ution of biodiversity. Indeed, the emergence of novel body
plans or organs very often coincides with the rise of a
wealth of new species, suggesting that evo-devo concepts
can revolutionize our understanding of macro-evolutionary
events. The flower is doubtlessly the most beautiful example
of an evolutionary innovation that is believed to have been a
major contributor to the diversification of angiosperms.
Flowering plants nowadays dominate terrestrial ecosystems
and, as a major food source, are of outstanding importance
for mankind. Floral structure is generally conserved with
four main organ types (sepals, petals, stamens and carpel);
however, the variation on this theme is breathtaking. The
types of variation include abortion of organs, radial versus
bilateral symmetry, whorled or spiral phyllotaxis, dramatic
variations in the colour, arrangement, number or size of
floral organs, or even evolution of extra floral organs, such
as, for example, in the genus Aquilegia. In recognition of the
recent advances in our understanding of the mechanisms
involved in the evolution of floral phenotypes, this issue
gathers together eleven articles contributing to the field of
‘flower evo-devo’, which represent diverse approaches
ranging from morphological and developmental comparative
studies, to phylogenetic analyses of important developmental
regulators, and gene function analysis in non-model plants.
Beyond their remarkable appearance and diversity that
enchant our eyes (Fig. 1), flowers function as the angiosperm
reproductive system. The amazing morphological diversity
results from the interplay of selection and developmental con-
straints; however, evaluating the relative importance of these
two evolutionary forces is not straightforward. Traits that
# The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
have evolved several times independently provide interesting
frameworks for addressing this issue. For instance, bilateral
symmetry appears to be an adaptive trait that has probably
evolved jointly with specialized pollinators, increasing precision
in pollen deposition on the pollinator’s body and thus resulting
in better cross-pollination efficiency (e.g. Citerne et al., 2010).
Symmetry characteristics involved in flower–pollinator inter-
actions are often clade-specific but with conserved general
trends (e.g. bilaterally symmetrical flowers exist in Orchid-
aceae and Fabaceae but with different architectures: Fig. 1C,
H). Bilateral floral symmetry probably emerged repeatedly as
a result of selection for increased reproductive efficiency,
and involved the evolutionary tinkering of inherited genetic
networks (Jacob, 1977). The molecular network controlling
flower symmetry is beginning to be characterized in distantly
related taxa of core eudicots, revealing both shared and differ-
ent factors (Costa et al., 2005; Wang et al., 2008). Similarly,
selfing has evolved multiple times from outbreeding, with
associated changes in several floral traits. In this Special
Issue, Sicard and Lenhard (2011) examine the selfing syn-
drome, with a specific focus on sex allocation to male vs.
female function and flower morphology. The molecular
bases of these traits are still largely unknown, but this
system appears promising for examining the importance of
genetic constraints in evolution, especially in the early stages
of the transition to selfing when selection associated with out-
breeding is expected to be relieved.
Homeotic mutants in model organisms have been crucial for
the discovery of genes controlling key steps in developmental
processes. The evolutionary potential of homeotic mutants is
still strongly debated. Goldschmidt (1940) was the first to
propose the concept of ‘hopeful monsters’, which has been
strongly challenged by the tenants of the Synthetic Theory
of evolution. It seems, however, that discrete phenotypical
differences between species cannot always be explained by
the accumulation of small changes and that, in at least some
cases, evolution may have proceeded in a saltationist rather
than a gradualist way (Rudall and Bateman, 2003; Theißen,
2009). Gould underlined that mutations in key developmental
genes could result in drastic phenotypical changes in adult
forms without conflicting with the Darwinian theory, and
that the evolutionary potential of such phenotypes could not
be simply dismissed (Gould, 1980). In plants, few mutants
of floral phenotype are known (e.g. the ‘peloria’ flower in
Linaria; Gustafsson, 1979): in this issue, Wang et al. (2011,
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1428 Becker et al. — The evolution of flower development

F I G . 1. Floral diversity among angiosperms. (A) Aconitum napellus. (B) Akebia quinata. (C) Lotus corniculatus. (D) Lamprocapnos spectabilis. (E) Doronicum sp.
(F) Gentiana acaulis. (G) Papaver somniferum. (H) Ophrys scolopax. (I) Cleome spinosa. (J) Leptospermum scoparium. (K) Callistemon citrinus. (L) Eschscholzia
californica. (M) Brassica oleracea. (N) Aquilegia alpina. (O) Heracleum spondylium. (P) Lilium martagon. Images: C. Damerval (A– H, N– P); A. Becker (I–L);
K. Alix (M).

who also review other cases) describe a double-flowered
mutant of periwinkle, and underline the need for fitness
studies in natural habitats to evaluate the evolutionary potential
of such anomalous phenotypes. Ronse de Craene et al. (2011)
address the question of the evolutionary role of carpeloidy, by
comparing the hermaphrodite flowers of Carica papaya and
the superman1 mutant of Arabidopsis thaliana, which both
display stamen-to-carpel conversions. They are able to show
that the developmental mechanisms differ in the two species
and suggest that the way the conversion takes place in arabi-
dopsis may be reminiscent of early events in the evolution
of bisexuality in plants. This comparative developmental
study highlights the importance of in-depth knowledge of
how organs are formed in order to formulate relevant evol-
utionary hypotheses. In connection with this topic, a review
by Peter Endress (2011) is devoted to the development and
evolution of angiosperm ovules. These organs can be traced
back to the origin of seed plants, being shared by angiosperms
and gymnosperms. Angiosperm ovules have evolved specific
traits, some of which may be related to their inclusion in the
carpels. The review points towards the diversity and morpho-
logical trends of ovules in major angiosperm clades, providing
evo-devo researchers with a new framework to investigate the
molecular bases of ovule evolution.
More than 20 years ago A. thaliana was established as a
convenient plant system to study the molecular mechanisms
of diverse physiological and developmental processes. The
molecular genetics of flower development has been a major
research focus from very early on, and yielded a wealth of
information about the regulation of floral organ identity, and
floral meristem identity, maintenance and termination.
Studies on A. thaliana in combination with Antirrhinum
majus, for which large collections of mutants have been avail-
able for a long time, have allowed the identification of a
limited number of transcription factor families such as the
MADS, TCP, NAM/CUC and YABBY families that have
played crucial roles in floral morphogenesis in core eudicots.
Orthologs and/or homologs of the A. thaliana and A. majus
 Becker et al. — The evolution of flower development
genes have been identified in other angiosperm species as
being related to specific traits, and have been characterized
in terms of sequence conservation and expression patterns.
This so-called candidate-gene approach has turned out to be
very insightful, suggesting that many genes have functions
that are conserved among higher eudicots, and sometimes
between them and other lineages of angiosperms, in accord-
ance with the monophyly of angiosperms (Soltis et al., 2008;
APG III, 2009). An emblematic gene family for flower devel-
opment is the MIKC-type MADS-box transcription factor
family: indeed, most genes involved in the control of floral
organ identity in arabidopsis and antirrhinum are MADS-box
genes (Coen and Meyerowitz, 1991; Causier et al., 2010).
Studies of MADS-box gene expression in key species for
floral diversity suggest that their role in floral organ identity
specification is widely conserved among angiosperms (Kim
et al., 2005). Additionally, MADS-box genes have been
shown to play roles in a variety of developmental processes
in plants, such as floral meristem specification, regulation of
flowering time, embryo and fruit development, and are
involved in nodulation during symbiosis with nitrogen-fixing
bacteria (Zucchero et al., 2001; Seo et al., 2009; Vrebalov
et al., 2009; Zheng et al., 2009, Kaufmann et al., 2010).
Considering the reproductive phase, SOC1 is a major flowering
pathway integrator in arabidopsis (Moon et al., 2003); in this
Special Issue, Ruokolainen et al. (2011) characterize three
homologs of SOC1 in Gerbera hybrida, and describe the con-
tribution of a paralog of SOC1 to the floral and inflorescence
phenotype in this species. Indeed, the candidate-gene approach
is currently the only way to tackle unusual variation in pheno-
typic traits. For example, Clianthus maximus is a Fabaceae
species with an unusual order of floral organ differentiation
that produces inflorescences all year round, all of which
abort except during a limited time in the autumn. Song et al.
(2011) address the molecular bases of these unusual traits by
characterizing MADS-box genes of the ABC model of floral
organ identity and the homolog of Leafy.
The characterization of candidate-genes in a growing
number of species affords the possibility to reconstruct the
evolutionary history of gene families. In many cases, such
studies point to the frequency of independent gene dupli-
cations and losses. This must be considered in the context of
whole-genome duplication (WGD), a major process of the
evolutionary history of angiosperms (Van de Peer et al.,
2009), which has opened the way for the emergence of
novel functions and/or patterns of expression by neo- or sub-
functionalization of duplicated genes. Several papers in this
Special Issue underline the importance of these phenomena.
Vialette-Guiraud et al. (2011) focus on the evolutionary
origin of the NAC gene family (NAM, ATAF1/2 and CUC3)
in seed plants. Members of this large transcription factor
family are essential for the formation of organ boundaries in
plants. The members of the NAM subfamily are regulated by
micro-RNAs (miRNAs), while CUC3 subfamily members
are not. Intriguingly, Vialette-Guiraud et al. demonstrate
that separate NAC and CUC3 lineages already exist in the
three earliest diverging angiosperm lineages (Amborellales,
Nympheales, Austrobaileyales: ANA-grade) but a common
ortholog of both groups, possessing a miRNA regulation
site, was present in gymnosperms. The most recent common
1429
ancestor of angiosperms and gymnosperms thus most likely
contained a NAC gene expressed under the control of small,
non-coding RNAs. Members of the TCP transcription factor
gene family have crucial roles in the regulation of cell div-
ision, controlling organ size and bilateral symmetry in
several plant species (Martin-Trillo and Cubas, 2009). This
family has been studied for a long time in eudicots, where it
has been shown to undergo repeated duplication events (e.g.
Citerne et al., 2003; Howarth and Donoghue, 2006;
Damerval et al., 2007; Zhang et al., 2010). Here, Howarth
et al. (2011) compare expression patterns of orthologs of
specific TCP genes in radially and bilaterally symmetrical
members of the Dipsacales, and find meaningful associations
between gene duplication, changes in expression patterns,
and flower symmetry and shape. Mondragón-Palomino and
Trontin (2011) establish a phylogenetic framework for the
TCP family in monocots, and suggest that expansion of
these genes in grasses originates from two rounds of WGD.
Genetic redundancy as a by-product of small-scale or genome-
wide duplication is a mechanism that should ensure robustness
of the gene networks underlying developmental processes,
while neo- or sub-functionalization would contribute to ‘evol-
vability’ of these networks. Evolutionary possibilities offered
by multiple duplicates is then reviewed by Geuten et al.
(2011) in the case of B-class genes, whose role in petal and
stamen identity appears conserved in a large group of angios-
perm species. Through mathematical modelling, they tackle
the role of diversification in activation mechanisms and
protein – protein interactions on downstream gene regulation.
As a means to decipher the molecular origin of evolutionary
novelties, the candidate-gene approach suffers from several
limitations. The first one is that experimental designs in non-
model plants often lack the ability to specifically down-
regulate genes in order to test functional hypotheses, because
transformation protocols are available for a few species only,
and are mostly time-consuming and laborious (often involving
tissue culture steps). Recently, however, this limitation has
partly been relaxed by using VIGS (virus-induced gene silen-
cing), which employs the plant’s innate defence system against
viruses not only to silence the viral genome but also to target
genes of interest. As most plants are susceptible to viruses and
many virus genomes can be converted into vectors suitable for
VIGS, this valuable technique has been successfully applied to
elucidate the role of floral homeotic genes in Nicotiana
tabacum and basal eudicots such as Papaver somniferum,
Eschscholzia californica, Thalictrum sp, and Aquilegia sp
(Drea et al., 2007; Gould and Kramer, 2007; Wege et al.,
2007; Becker and Lange, 2010; Di Stilio et al., 2010;
Yellina et al., 2010). In this Special Issue, Hands et al.
(2011) report the functional analysis of two differentially
spliced Papaver somniferum AGAMOUS orthologs, and
demonstrate that beyond an expected redundant function in
specifying carpel and stamen identity, one of the splicing pro-
ducts has unique roles in septum, ovule and stigma develop-
ment. This finding is especially important as it is one of the
rare cases where a functional significance can be attributed
to alternative splicing.
A second limitation to the candidate-gene approach is that
the ‘classical’ model species A. thaliana and A. majus are
members of the highly derived clade of core eudicots, and
1430 Becker et al. — The evolution of flower development
their genetic repertoire has most likely changed tremendously
since the lineage split from the remaining angiosperms. In
addition, the genome of A. thaliana is rather reduced in size
and might not be a suitable representative for most angio-
sperms. Thus, the regulation of flower development in plants
distant from arabidopsis might involve genes that are not
merely orthologs to A. thaliana genes, and/or the regulatory
networks may be different. Flower evo-devo thus needs to
move towards a less ‘arabidocentric’ view, even more so
when taking into consideration recent studies that show that
significant functional differences exist between orthologs of
transcriptional regulators. One example for such a phenom-
enon is the arabidopsis YABBY gene CRABS CLAW (CRC),
which is required for carpel and nectary development. Its
rice ortholog DROOPING LEAF (DL) is required for leaf
midrib formation and carpel organ identity specification and
floral meristem termination. The basal eudicot Eschscholzia
californica’s ortholog EcCRC is also required for floral meris-
tem termination and carpel development but it is not involved
in carpel organ identity and leaf development (Alvarez and
Smyth, 1999; Yamaguchi et al., 2004; Orashakova et al.,
2009).
Alternative approaches to study regulation of floral develop-
ment in non-model plant species could be the establishment of
collections of mutants. This would allow screening for novel
mutants and subsequent identification of the mutant locus
and the characterization of novel genes. Another option is
the generation of organ-specific transcriptome databases for
phylogenetically relevant species, followed by large-scale
VIGS analysis to transiently knock-down genes and screen
for developmentally impaired phenotypes. These
candidate-gene-free approaches would allow assumption-free
analysis of development in a large phylogenetic context, and
should lead to the discovery of novel components of regulatory
networks.
The large number of sequences deposited in publicly avail-
able databases, derived from sequencing projects and individ-
ual gene-identification approaches, has already yielded a
wealth of sequence information even for genes that are
usually under-represented in transcriptomes, such as transcrip-
tion factors regulating development that have generally low
transcript abundance (Boavida et al., 2011). Such information
is available for species that are interesting for their particular
phylogenetic position, for example the Floral Genome
Project (FGP) has provided floral transcriptome sequences
for members of the important ANA-grade that diverged very
early in angiosperm evolution. With the advent of
next-generation-sequencing techniques at a more affordable
price, transcriptome – but also genome – sequencing projects
will become feasible for an even wider range of species in the
near future. These genomic data will enable reconstructions of
more detailed gene phylogenies, allowing analyses of gene
birth and death rates, molecular clocks and evolutionary
forces acting on developmental regulators. The resulting infor-
mation will be highly valuable, for example in assessing the
contribution of homeotic mutants to morphological innovation
and speciation, or in choosing genes for comparative func-
tional analyses, which then will help in understanding ances-
tral gene functions. Additionally, it will be possible to
elaborate new tools to investigate in depth important
evolutionary questions, such as the relative importance of
selection and developmental constraints, and the evolution of
modularity and its role in robustness of genetic networks.
The possibility to model gene networks and their morphologi-
cal outcomes, and to simulate perturbation in network func-
tioning as a result of genetic mutation or environmental
cues, should be illuminating in this respect.
ACK N OW L E DG E M E N T S
We thank Dr Hélène Citerne for fruitful discussions on flower
evo-devo, and for critical reading of an earlier draft of this
manuscript.
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