Carpels Advanced article

David R Smyth, Monash University, Melbourne, Australia Article Contents

. Introduction
Carpels are the female reproductive organs within a flower that enclose the ovules, . Genes and Carpel/Ovule Development
protecting them and screening out inappropriate pollen. They arose, probably from leaf- . Evolution of Carpels
like organs, long after the origin of ovules. Genes controlling key steps in carpel and ovule . Pollination
development are being discovered.
doi: 10.1002/9780470015902.a002067.pub2

Introduction
In seed plants, which evolved around 360 million years ago, Genes that regulate the identity of each floral organ type,
male and female gametes arise within specialized structures including the carpel, are now well known. They function
formed by the mature diploid plant. The female structure is alone or in combination to switch the developmental pro-
the ovule, the organ that bears the egg. A specific cell within gramme of newly arising organ primordia into the pathway
the ovule undergoes meiosis early in ovule development. appropriate to their position within the flower. In the model
One of the resulting haploid products then undergoes cell laboratory species Arabidopsis thaliana, carpel identity func-
divisions to form the gametophyte. In turn, one of these tion is controlled by the gene AGAMOUS. The gene encodes
cells becomes the egg. In the more primitive seed plants,
including gymnosperms, the ovule may be embedded in a
leaf-like megasporophyll, but the egg is exposed at the
surface so that pollen, the male gametophyte, can gain
ready access to it. Following fertilization, the ovule serves
to house the developing diploid embryo and encases it in a
seed coat for dispersal. See also: Gametophyte and
sporophyte; Gymnosperms; Plant embryogenesis (zygotic
and somatic); Plant reproduction; Seeds
Around 130 million years ago, a group of seed plants
arose in which the formerly naked ovules became enclosed
in a specialized structure, the carpel. Carpels are usually
made up of three components – the ovary (the chamber in
which ovules arise), the stigma (specialized surface tissue
for the reception of pollen) and a style (providing a trans-
mitting tract for growth of the pollen tube between the Figure 1 Structure of carpels of the model laboratory species Arabidopsis
stigma and the ovary) (Figure 1). All the carpels in one thaliana. (a) Scanning electron micrograph of a mature flower with several
sepals, petals and stamens removed to reveal the central female
flower, whether single or multiple, free or fused, are col-
reproductive organ (medial view). This is made up of two congenitally
lectively called the gynoecium. After fertilization, the fused carpels (left and right) that are together called the gynoecium. The
ovary component of carpels usually undergoes further three components of the gynoecium are an upper stigma with papillae on
growth and modification to generate the fruit that encloses which pollen grains germinate, a short style with internal transmitting tract
the developing seeds. The presence of carpels defines the tissues through which the pollen tubes grow and a large, two chambered
ovary. Each chamber represents one carpel, and the two chambers are
angiosperms, or flowering plants, a group that has been
separated by a septum, which also carries transmitting tract tissues. (b) Side
spectacularly successful with approximately 250 000 spe- (lateral) view of a gynoecium of Arabidopsis with part of the ovary wall
cies now living. Not only does the carpel protect the ovules dissected away. This reveals the internal ovules within one of the two
during their development, it also provides a barrier chambers (corresponding to one of the two carpels). Each ovule has a short
through which only appropriate pollen tubes can grow to stalk (funiculus, f), an internal nucellus that carries the embryo sac
(including the female gamete) and two sheaths of tissue (integuments, i)
achieve fertilization, features likely to have contributed to
surrounding the entrance to the ovule (micropyle). In this species, the
this explosive success. See also: Angiosperms; Fruit integuments are turned upwards (anatropous). Pollen grains have
germinated on the stigma, and pollen tubes (t) have grown down the style
Genes and Carpel/Ovule Development and septum, and several can be seen in the chamber (top right). (c) Cleared
gynoecium of Arabidopsis in which the pollen tubes have been selectively
stained with the fluorochrome aniline blue. Their path of travel from the
Carpel genes stigma, down the transmitting tract, and to micropyles of individual ovules,
can be observed. (a) and (c) Reproduced from Alvarez and Smyth (2002)
The structure of the mature carpel is the result of the finely with permission of The University of Chicago Press and (b), courtesy of John
tuned action of many genes. Alvarez.

ENCYCLOPEDIA OF LIFE SCIENCES & 2006, John Wiley & Sons, Ltd. www.els.net 1
 Carpels

a transcription factor of the MADS family and its primary Many other carpel genes are known, although they
function is to regulate the expression of other, mostly uni- mostly have pleiotropic mutant effects in other parts of the
dentified, genes. The genetic mechanism by which carpel developing plant. This suggests that they do not play a
identity is established is highly conserved in flowering plants, specific role in defining carpel-specific processes. Even so,
as orthologues of AGAMOUS with similar roles have been one interesting pleiotropic gene that seems to control as-
reported in many other species. See also: Arabidopsis: pects of both proximal–distal and abaxial–adaxial polarity
Flower development and patterning; Arabidopsis thaliana as within the developing Arabidopsis gynoecium is ETTIN
an experimental organism; Plant genetics and development; (Nemhauser et al., 2000). This gene is related to those that
Regulatory genes in plant development: MADS bind to elements in the promoters of auxin-activated genes,
However, AGAMOUS function is not alone in initiating and it may thus provide a link between the action of this
the Arabidopsis carpel development programme. When the hormone and carpel growth processes. See also: Plant
functions of the closest MADS relatives of the AGAMOUS growth factors and receptors
gene were examined, it was found that duplicated SHAT-
TERPROOF genes were also involved in defining carpel
identity (Table 1) (Pinyopich et al., 2003). Constitutive ex- Ovule genes
pression of these genes could fully restore the carpel de-
velopmental programme when AGAMOUS function was A series of genes controlling the development of ovules has
lost. On the other hand, when SHATTERPROOF func- also been discovered. Ovule identity seems to be under
tion was lost, carpels develop normally because AGA- simple genetic control. In Petunia hybrida, the FLORAL
MOUS function is still present. The mutant phenotype of BINDING PROTEIN 11 gene is expressed specifically in
the SHATTERPROOF genes revealed itself later during ovules but, when it is expressed ectopically in all tissues,
fruit development when the loss of their role in defining the ectopic ovules arise on the surface of sepals and petals. This
dehiscence zone became apparent. indicates that the MADS protein encoded by this gene may
When individual components of the Arabidopsis gy- normally specify ovule identity within newly developing
noecium were investigated using genetic dissection meth- primordia within the gynoecium (Colombo et al., 1995). In
ods, it was revealed that AGAMOUS function specifies Arabidopsis, the orthologue of this gene is SEEDSTICK,
only the identity of the wall of the ovary (the valve) and and this, too, establishes ovule identity (Table 1) (Pinyopich
outgrowth of the style. Two other transcription factor et al., 2003). Interestingly, all close MADS relatives of
genes, CRABS CLAW and SPATULA, have been de- SEEDSTICK, including AGAMOUS, apparently deter-
scribed whose regulatory functions are required to bring mine ovule identity, although their other functions (i.e.
about the full carpel development programme (Alvarez target genes) are mostly not shared (Table 1). See also: Plant
and Smyth, 1999). CRABS CLAW function is required to organ primordia; Plant cell differentiation
ensure lateral and vertical growth of the carpels, and Other, later-acting genes are also known that are in-
SPATULA function is needed for appropriate develop- volved in growth of the ovule primordium, development of
ment of tissues arising from the edges of the carpels, es- the ovule coat (integuments), growth of the stalk (fun-
pecially the transmitting tract. Among other regionally iculus) and development of the female gametophyte within
acting genes uncovered so far, STYLISH1 and 2 appar- the nucellus (Skinner et al., 2004) (Figure 1). It is interesting
ently act redundantly to promote growth of the style and that several of these genes may have been involved in
stigmatic regions (Kuusk et al., 2002), and KNUCKLES, modifications to ovule development that occurred during
encoding a zinc-finger transcription factor, acts to support angiosperm evolution. The ovules of gymnosperms and
development of the basal region of the ovary (Payne et al., other extinct seed plants typically have only one coat or
2004). See also: Regulatory genes in plant development: integument (unitegmic) and the body of the ovule sits
MADS erect on the stalk (orthotropous). On the other hand, most

Table 1 The roles of four closely related MADS transcription factor genes in controlling carpel, ovule and fruit development in
Arabidopsis
Flower deter-
Gene Carpel identity Stamen identity minacy Ovule identity Fruit dehiscence Seed abscission
AGAMOUS + + + + 2 2
SHATTER- + 2 2 + + 2
PROOF1 & 2
SEEDSTICK 2 2 2 + 2 +
Source: see Pinyopich et al. (2003).

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 Carpels

angiosperm ovules have double coats (bitegmic), and the

body of the ovule is turned back along the stalk (an-
atropous). Mutants with loss of function phenotypes that
are now unitegmic, or orthotropous, may have occurred in
genes involved in defining the more advanced forms.

Evolution of Carpels
There has been much speculation about how the me-
gasporophyll formed an enclosed chamber during angio-
sperm evolution. Comparative developmental studies of
the single free carpels within basal families suggest that
they are derived from leaf-like organs that bear ovules
along each edge (Endress and Igersheim, 2000). If these
folded inwards (towards the stem) so that the edges either
touched or lay flat alongside each other, structures resem-
bling an ovary would result. Further, the development of Figure 2 Carpel structure in the most primitive angiosperm, Amborella
trichopoda. Flowers of this New Caledonian woody shrub have several free
hairs and/or secretions at the point of touching would fa- urn-shaped carpels, each with a single ovule. In this diagram of a
cilitate the development of a transmitting tract that faci- longitudinal section of one carpel, the large cap of stigmatic cells, the
litates the growth of pollen tubes to the internal ovules. It is narrow canal through which pollen tubes grow (the transmitting tract) and
now a series of short steps to generate the typical structure the single, penduluous (orthotropous) ovule within the ovary are visible.
of the enclosed carpel. The infolded edges could fuse post- Both the canal and the chamber around the ovule are filled with secretion.
The floral axis is on the left. For further details see Endress and Igersheim
genitally. Alternatively, a similar outcome is achieved if the (2000).
edges are fused congenitally from the base. Either way, a
cup-shaped structure (ascidium) is produced. The upper of the carpel evolution pathway outlined above. See also:
region could become elongated into a style, and the hairs Molecular phylogeny reconstruction; Amborellales
and secretions might become localized towards the apex
and evolve into stigmatic tissue. The canal within the style
(part of the transmitting tract) may also be filled by similar
hairs or secretions, or it may be fully sealed by congenital Pollination
fusion of ingrowing cells. See also: Flowering plants,
evolution; Morphological evolution: epigenetic mecha- Carpels play an important role in ensuring that only pollen
nisms; Selection: units and level of the appropriate type fertilizes the egg (Weterings and
Such a speculative scheme (among others) accounts for Russell, 2004). Pollen grains first make contact with the
the evolution of single, free carpels. Aggregation into fused carpel through the stigma (Figure 1b). Here they hydrate and
multicarpellate gynoecia, such as those that occur in about germinate. A tube emerges from a pore in their wall and
80% of all flowering plants, and embedding of the ovary penetrates the stigma, growing between stigmatic cells or
within the floral receptacle to form the inferior ovary seen within the middle lamella of one such cell, or even within the
in many higher angiosperms are apparently additional re- cell itself. The pollen tube then moves into the transmitting
finements based on the single carpel unit. tract that underlies the stigma, following this defined path
Recently, molecular phylogenetic studies have revealed within the style and ovary. In many cases, the transmitting
that the most basal extant angiosperm is the relict woody tract is solid and made up from cells that have secreted an
shrub Amborella trichopoda (Qiu et al., 1999). This is the extracellular matrix of carbohydrates, glycoproteins and
only member of the family Amborellaceae, and is confined other proteins that provide nutrition for the elongating
to the island of New Caledonia in the South Pacific. Carpels pollen tube. In other cases, the tract is a hollow tube but the
in this species are urn-shaped and capped with a broad, cells lining it provide secretions thought to offer the same
stigmatic surface (Endress and Igersheim, 2000; Figure 2). specialized support. As the pollen tube continues to grow, it
They have an unfused transmitting tract canal that is filled eventually reaches the vicinity of the ovule. Here, a re-
with secretion, as is the chamber that contains the one pen- markable series of events occurs as it leaves the transmitting
dulous, straight (orthotropous) ovule. Each flower has sev- tract and grows specifically towards the ovule’s opening
eral unfused carpels arranged in a spiral. Thus, the structure (micropyle). It contacts the two specialized cells, often pro-
of carpels in this primitive species, and indeed in the next truding into the micropyle (the synergids), penetrates one of
most basal families including water lilies and a small group them and releases its two haploid sperm cells. Typically, one
including star anise and the Australian tropical climber of these then fuses with the neighbouring egg, and another
Austrobaileya, is consistent by it representing an early stage with two polar nuclei of the central cell to generate the

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nutritive endosperm. See also: Plant reproduction; Stamen apparatus (synergids and egg cell) naturally protrudes
and pollen development; Pollen: structure, development from the micropyle (Higashiyama et al., 2001). Isolated
and function; Gametogenesis ovules can attract pollen tubes only if at least one of the
synergids remains active (individual egg apparatus cells
can be inactivated by laser ablation). Also, pollen tubes are
Pollen recognition attracted only if they have already grown through a style,
i.e. they are ‘potentiated’. The chemical basis of these
Just how carpel tissues are able to recognize specific pollen
events is not yet known.
grains has been investigated and some answers are avail-
In maize, however, there is now good evidence that a
able. In a range of different families, genetically controlled
specific short distance signal that attracts pollen tubes to
systems of self incompatibility have evolved. In species
the female gametophytic tissue is a small peptide (Márton
with ‘wet’ stigmas in the nightshade family (Solanaceae),
et al., 2005). The Egg Apparatus1 gene, encoding a 94
for example, pollen that shares its haploid (gametophytic)
amino acid peptide, is active only in the two synergids and
genotype with the stylar cells through which it is growing is
egg cell. Importantly, while downregulation of the gene in
recognized, and its growth is chemically disrupted. On the
maternal tissue using RNA interference did not disrupt the
other hand, in some species with ‘dry’ stigmas in the mus-
movement of pollen tubes into the micropyle, they no
tard family (Brassicaceae), it is only those pollen grains
longer sought out the synergids. The Egg Apparatus1 gene
whose outer coat does not share its paternal (sporophytic)
was not found in fully sequenced genomes outside of the
genotype with the stigma cells on which it falls that will
grasses, further suggesting that the peptide may play a role
hydrate and germinate.
in restricting inter-species fertilization. See also: Positional
The molecular nature of the self versus nonself recogni-
information in plant development; Sperm–egg interac-
tion process has now been established in the Solanaceae and
tions: sperm–egg binding in mammals
the Brassicaceae. In each case it is a ‘lock and key’ event. In
the former, gametophytic system, the style produces degra-
dative S-RNAase molecules (Kao and Tsukamoto, 2004). References
The pollen tube expresses a specific F-box protein that pre-
sumably recognizes and targets for removal of all S-RNA- Alvarez J and Smyth DR (1999) CRABS CLAW and SPATULA, two
Arabidopsis genes that control carpel development in parallel with
ase molecules ‘except’ for the one encoded by the same S
AGAMOUS. Development 126: 2377–2386.
‘allele’. In this way, the style inactivates the pollen of the Alvarez J and Smyth DR (2002) CRABS CLAW and SPATULA genes
same genotype by means of those S-RNAase molecules that regulate growth and pattern formation during gynoecium develop-
have not been eliminated. In the latter, sporophytic system, ment in Arabidopsis thaliana. International Journal of Plant Sciences
the stigma carries specific receptor protein kinases that are 163: 17–41.
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all pollen grains from each plant (Nasrallah, 2002). In this MADS box gene FBP11 determines ovule identity. Plant Cell 7:
1859–1868.
case, however, the active recognition is between molecules
Endress PK and Igersheim A (2000) Gynoecium structure and evolution
generated by the ‘same’ S ‘allele’. The recognition leads to a in basal angiosperms. International Journal of Plant Sciences 161
blocking of pollen tube penetration of the style. The con- (suppl.): S211–S233.
sequence is that any pollen grain of that species that is not Higashiyama T, Yabe S and Sasaki N et al. (2001) Pollen tube attraction
recognized as ‘self’ can grow. See also: Ribonucleases; Self- by the synergid cell. Science 293: 1480–1483.
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One process that still requires explanation is how the path Márton ML, Cordts S, Broadhvest J and Dresselhaus T (2005) Micro-
pylar pollen tube guidance by Egg Apparatus 1 of maize. Science 307:
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(Weterings and Russell, 2004). Chemical signalling proc- Nasrallah JB (2002) Recognition and rejection of self in plant repro-
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In mutants of Arabidopsis, guidance to the ovule is lost TIN in Arabidopsis gynoecium morphogenesis. Development 127:
when two genes are in mutant form, and one of these genes, 3877–3888.
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up a GABA concentration gradient towards the ovule Payne T, Johnson SD and Koltunow AM (2004) KNUCKLES (KNU)
(Palanivelu et al., 2003). encodes a C2H2 zinc-finger protein that regulates development of
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Smyth DR (2005) Morphogenesis of flowers – our evolving view. Plant
Bowman JL, Baum SF, Eshed Y, Putterill J and Alvarez J (1999) Cell 17: 330–341.
Molecular genetics of gynoecium development in Arabidopsis. Current
Topics in Developmental Biology 45: 155–205.