Morphogenesis of Flowers-Our Evolving View - Plant Cell
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The Plant Cell, Vol. 17, 330–341, February 2005, www.plantcell.org ª 2005 American Society of Plant Biologists
HISTORICAL PERSPECTIVE ESSAY
Morphogenesis of Flowers—Our Evolving View
In this essay, the time course of our un- about plant sexual reproduction. The clos- and classification. An Italian physician,
derstanding of the structure and function of est they got was to realize that there are Andrea Cesalpino (1519–1603), proposed
flowers will first be outlined from prehistoric two forms of date palm and that fruit set the first natural system of plant classifica-
times to the mid-twentieth century. Infor- could be promoted if dust of a flowering tion (i.e., one in which plants are grouped
mation is taken mostly from Sachs (1875), shoot of a sterile tree was shaken over the by their degree of relationship) using their
Arber (1950), and especially Morton (1981). flowering shoots of potentially fertile trees. fructification properties. These included the
More recent studies on the genetic basis The first historical records of attempts to position of the abscising floral organs on
of flower development will then be re- comprehend the general properties of the seed case (i.e., whether the ovary is
viewed, focusing on floral organs rather plants are the writings of the Greek philo- superior with the outer organs at its base or
than ovules, seeds, or fruits. Finally, major sopher Theophrastus (;370–285 BCE). The inferior [organs at its apex]), the number of
gaps in our present understanding and father of botanical science, Theophrastus seeds in a fruit, and the number of cavities
possible future advances will be discussed. was a colleague of Aristotle, whom he (locules) per fruit. Joachim Jung (1587–
succeeded as leader of the Lyceum. Theo- 1657), a professor of Natural Sciences in
phrastus considered plants to be made up Hamburg, clarified the distinction between
EARLY IDEAS ABOUT FLORAL of persistent parts (roots, stems, branches, petals and the organs that surround the
STRUCTURE AND FUNCTION and twigs) and ephemeral parts (leaves, flower (which Jung called the perianthium
flowers, fruits, including seeds, and the and which includes what we now call floral
Until ;12,000 years ago, humankind sur-
stalks of these organs). In his view, flowers bracts as well as sepals). He also noted
vived by exploiting wild plants and animals
were basically defined by the petals, al- that stamens are often divisible into a ped-
for food and shelter. Since then, domesti-
though they did include stamens and the iculus (filament) and a capitulus (head or
cation of many species led to major popu-
styles of carpels. Sepals were considered anther).
lation increases, urbanization, and the
small leaves, and the ovary seemed to be The invention of the microscope allowed
availability of time for creative pursuits.
viewed not as a floral part but as the future two major contributions to plant anatomy
These changes have been associated with
fruit case. Thus, the flower represented only soon after. Italian Marcello Malpighi (1628–
the rise of mechanical invention, literacy,
those organs that abscised from the de- 1694) and Englishman Nehemiah Grew
and ultimately modern civilization.
veloping fruit. Sexual reproduction was not (1641–1712) observed not only plant mor-
The domestication of plants required
understood or distinguished from vegeta- phology, but they linked mature structures
knowledge of how to cultivate them suc-
tive reproduction. The role of stamens, the with their development for the first time.
cessfully. However, the initial choice of
fertilization of ovules, and the universal They recognized the generality of proper-
species and the improvement of strains
occurrence of seeds as a stage in the life ties of different floral organs across spe-
were rather haphazard and empirical pro-
cycle were not comprehended. cies. For example, they observed that what
cesses. Improvement mostly relied on early
For the next 1800 years, interest in the we now call perianth organs (sepals and
farmers selecting seeds from the best
study of plants was mostly limited to their
performing plants of the current crop to petals) are usually essentially leaf like and
role in medicine, with descriptions of useful
grow in the next season. Occasionally, rare that stamens, almost universal compo-
species being reproduced down the gen-
genetic variants or hybrids would arise that nents of flowers, always released dust
erations in compendia called herbals. In
were seized on as offering major benefits in from their upper regions. The Englishman
Oriental cultures, plant descriptions were
quality and yield. For example, domesti- John Ray (1623–1705) subsequently named
particularly accurate, and they also in-
cated maize differs from its wild Mexican this dust pollen and also distinguished
cluded species of aesthetic attraction
ancestor teosinte by several major genetic between the calyx (now called sepals) and
such as peonies, lilies, and chrysanthe-
variants that result in reduced branching the internal corolla made up of showy
mums in addition to medicinal plants.
and larger, nonshattering ears (Doebley, ‘‘petals,’’ a name he popularized and which
2004). Also, the domestication of bread came into common use. Thus, the compo-
wheat in the Middle East included the nents of the flower were now defined
EUROPEAN AWAKENING: ANALYTICAL
selection of two sequential interspecies almost as in current usage except that the
AND EXPERIMENTAL APPROACHES
hybrids that apparently arose after sponta- ovary was still not recognized as a floral
neous hybridization events between culti- In Europe from the sixteenth century on, component, only the style.
vated and weedy species (Feldman et al., attempts were renewed to understand the Surprising as it now seems, it wasn’t until
1995). Ancient civilizations did not know basic principles of plant structure, function, the end of the seventeenth century that theFebruary 2005 331
HISTORICAL PERSPECTIVE ESSAY
role of pollen in fertilization was established corded until 1878 by Eduard Strasburger of shared properties, in his case involving six
and that sexual reproduction was con- Bonn (1844–1912). More generally, it was parts: the calyx, corolla, stamens, pistil,
firmed in plants. Rudolph Jacob Camera- Hofmeister who established in 1851 that pericarp, and seeds. But his innovation was
rius (1665–1721), director of the Botanic alternating generations involving sexual re- to provide just one word to specify each
Garden in Tübingen, Germany, observed production (now called the sporophyte- plant type within a genus, rather than
that most flowers had stamens positioned gametophyte cycle) was a property common a wordy descriptive phrase. This word is
close to the style that topped the future to bryophytes, ferns, lycopods, and gymno- now known as the species name, and his
seed case. He proposed that such flowers sperms as well as angiosperms. This was binomial system of nomenclature is fol-
were hermaphrodite and that pollen re- a major unifying theory that linked all land lowed to this day.
leased from the anthers landed on the style plants and was dependent on the key finding
and ensured that seeds subsequently de- that ferns contained cells obviously equiva- DEVELOPMENT OF IDEAS ABOUT
veloped. He concluded that petals were not lent to the male and female gametes of FLOWER MORPHOLOGY
involved because many flowers lack petals animals (motile sperm and sessile eggs). AND MORPHOGENESIS
but set seeds (e.g., vines and cereals), and Interestingly, the chromosomal basis of this
also some garden plant variants had extra alternation of generations was not deduced The study of plant development was not
petals at the expense of stamens (double until the end of the nineteenth century, neglected. In 1790, the German poet
flowers), and even though these may have another major contribution by Strasburger. Johann Wolfgang von Goethe (1749–
styles, fruit was not usually set. Camerarius Returning to the eighteenth century, 1832) published an influential extended
then performed experiments to test the role Swedish botanist Carolus Linnaeus (Carl essay entitled ‘‘Versuch die Metamorphose
of pollen. He used plant species in which von Linné, 1708–1778) had a major in- der Pflanzen zu erklären’’ (An attempt to
flowers of two types occurred: male (sta- fluence on plant science. Linnaeus’ use of interpret the metamorphosis of plants) in
mens only) and female (styles only). These floral and fruit properties as the basis of 1790. The idea of metamorphosis had been
were present either on separate plants classification of plants helped emphasize proposed much earlier by Cesalpino and
(dioecious, including the mulberry Morus these structural features, although floral refined by Linnaeus. In Linnaeus’ words
and dog’s mercury Mercurialis) or on the function was not involved. His hierarchical ‘‘the flower [can be regarded] as the interior
same plant (monoecious, castor oil plant scheme was based firstly on stamen portions of the plant which emerge from the
Ricinus and maize Zea). By preventing any number and arrangement within the flower bursting rind; the calyx as a thicker portion
pollen from landing on styles in each case, (Figure 1). He proposed 24 primary groups of the shoot; the corolla as an inner and
in 1694, he confirmed the necessary role of that he called classes, with the first 10 thinner rind; the stamens as the interior
pollen in fruit and seed set. Again, it is corresponding to plants with 1, 2, and so fibers of the wood, and the pistil as the pith
surprising in hindsight how long it took for on up to 10 free stamens per flower all of of the plant’’ (Sachs, 1875). Based on his
this conclusion to be extended to under- the same length and the next 10 also observations of variations in normal plant
standing the role of insects in transfer of including other stamen properties, such growth and on abnormalities that some-
pollen between anthers and styles (the as different lengths and degrees of fusion times occur, Goethe (1790) provided an
1760s by Joseph Gottlieb Koelreuter to each other and to other floral organs. alternative view of metamorphosis: ‘‘The
[1733–1806] in Karlsruhe) and the adapta- The last four groups included monoecious, same organ which on the stem expands
tion of many flowers to insect-driven cross- dioecious, mixed dioecious-hermaphrodite, itself as a leaf, and assumes a great variety
pollination rather than self-fertilization (in and apparently flowerless plants. Within the of forms, then contracts in a calyx—
1793 by Christian Konrad Sprengel [1750– first 13 classes, Linnaeus then defined expands again in the corolla—contracts in
1816] in Berlin). subgroups (orders) based on the number the reproductive organs—and for the last
The mechanics of fertilization were not of styles per flower, and in the other classes time expands in the fruit.’’ Goethe named
fully defined until even later. In 1833, British he used fruit characters. As this scheme the generalized organ ‘‘Blatt,’’ and thought
botanist Robert Brown (1773–1858) con- was based on stamens and styles/fruits, of it as a generalized plant organ rather
firmed that pollen tubes emerge from pollen Linnaeus called it the ‘‘sexual system.’’ He than as a leaf, leaves being just one of
grains and grow down the style, and he did not claim that this was a natural scheme, the forms it could adopt. This simple and
showed for the first time that a pollen tube although related plants often clearly grouped attractive proposal has influenced the
enters the micropyle of an ovule immediately together, but its simplicity and ease of use thinking of plant scientists until the present
before the embryo starts to develop. But it meant that it was widely followed until day (see below).
wasn’t until the 1840s that Wilhelm Friedrich displaced by more natural schemes. In line with this scheme, sepals and
Hofmeister (1824–1877), working in Linnaeus’ second contribution, after petals are obviously similar in form to
Hamburg, showed that the embryo was classification, was the invention of the leaves, but stamens and carpels are less
derived from the egg cell within the embryo binomial system of nomenclature. Within so. In this regard, Robert Brown indepen-
sac, and the actual process of nuclear fusion his orders, he followed earlier authors in dently obtained evidence that pointed to all
of the sperm and egg nuclei was not re- grouping plants into named genera with floral organs sharing leaf-like properties.332 The Plant Cell
HISTORICAL PERSPECTIVE ESSAY
For carpels, his interpretation was that the
units of multilocular gynoecia can be
thought of as leaf-like carpels joined along
their edges. For both carpels and stamens,
he proposed that the reproductive tissues
(ovules and pollen) arose along the edges
of the foliar-like organ. This interpretation of
the gynoecium and its relationship to later
developing fruit and seeds provided the
basis for our modern view of the flower as
including the ovary as well as the styles
(and stigmas), rather than the former being
looked on solely as the future fruit. In pas-
sing, in 1827, Brown clarified the difference
between the naked seeds produced by
conifers and cycads and the single-seeded
indehiscent fruits that include a pericarp
derived from the ovary (such as those that
occur in grasses and daisies), leading to
the establishment of the fundamental dif-
ference between gymnosperms and angio-
sperms.
A new developmental approach to the
natural classification of plants was intro-
duced in 1813 by the Swiss botanist
Augustin-Pyrame de Candolle (1778–
1841). de Candolle highlighted the sym-
metry of flowers, the number and relative
placement of organs set up early in de-
velopment, as being of key importance in
classification. Furthermore, he identified
three processes by which this symmetry
could apparently be modified later in
development: organ abortion, organ mod-
ification, and organ adherence, modifica-
tions that should be taken into account
when grouping species with the same
overall symmetry. Such similarities and
differences were apparent in the increas-
ingly accurate and detailed descriptions of
early flower development highlighted by
Jean-Baptiste Payer’s (1818–1860) mas-
terpiece ‘‘Traité d’Organogénie Comparée
de la Fleur’’ (Treatise on the comparative
organogenesis of flowers) published in
Figure 1. The Basis of Linnaeus’ Sexual System for the Classification of Flowering Plants.
Paris in 1857.
Linnaeus defined 24 classes based on the number of stamens per flower (A to N), their variable length During the nineteenth century, details of
(O to P), their degree of fusion (Q to U), and the presence of some flowers without stamens (V to Y) and the cellular basis of plant development
of plants apparently without flowers (Z). He then subdivided classes into orders mostly based on the were described. The universal presence of
number of styles (carpels) in each flower. Each order was then again divided into genera based on six
one nucleus in each cell had been estab-
other floral and fruit characteristics. Finally, similar plants within a genus were given a single Latin
lished by Robert Brown, and the cell as the
descriptor, now know as the species name. The genus and species names are the binomial system we
use today. (Watercolor by Georg Dionysius Ehret drawn in 1736. Original held in the Natural History
unit of all plant tissues generalized by
Museum, London, UK, and reproduced with permission.) Matthias Jakob Schleiden (1804–1881) of
Jena in 1839. The fact that cells only ariseFebruary 2005 333
HISTORICAL PERSPECTIVE ESSAY
from preexisting cells by a process of flower (gestalt), and third, the later elabo- with spiral phyllotaxy, sepals and petals
binary separation was established in plants ration of specialized characteristics (style). often not distinguished, stamens with
by the Swiss botanist Karl Wilhelm von The blueprint is relatively stable in evolu- short filaments, and free carpels lacking
Nägeli (1817–1891) in Munich in 1846, well tionary terms, growth patterns that define styles and sealed by secretion (Endress,
before the same conclusion was reached the overall size and shape of the flower less 2001a).
by Virchow in animals (1859). The chromo- so, and elaborations such as pollinator-
somal events that underlie cell division specific colors and perfumes are relatively
GENES, GENES, GENES
awaited Eduard Strasburger’s contribution fluid.
at the end of the nineteenth century. The origin of flowers has been the sub- For many years, it had been clear that the
ject of much speculation for the last 100 development of flowers must be under
THE TWENTIETH years (Arber, 1937; Cronquist, 1988; Doyle, genetic control. Mutants that disrupt the
CENTURY—MERISTEMS, 1994), although resolution is still not in normal processes were well known. From
COMPARATIVE MORPHOLOGY, sight. Two alternative schemes were pro- the early 1980s, new technology allowed
AND EVOLUTION posed early: the euanthial theory, in which the responsible genes to be cloned, their
flowers arose de novo, and the pseudan- molecular nature to be deduced, their
The first half of the last century saw prog- thial theory, in which they arose through the expression patterns to be mapped, con-
ress in our understanding of the properties combination of originally separate female sequences of their loss or gain of function
of meristems (Wardlaw, 1965; Steeves and and male inflorescence shoots. The main to be assessed, and their interactions with
Sussex, 1989). The structure of shoot apical difficulty in distinguishing between these (in other genes, including related genes, to be
meristems and flower meristems was de- their many versions) is the lack of obviously determined. Access to the molecular and
fined, and their functional partition into stem ancestral fossils or of closely related extant cellular functions of flower developmental
cells in the central zone, and organogenic groups. A recent euanthial scheme, the genes was available at last (Lohmann and
cells in the peripheral zone, deduced. The anthophyte hypothesis, proposed that the Weigel, 2002; Leyser and Day, 2003; Jack,
origin and maintenance of epidermal (L1) flower-like structures of living Gnetophytes 2004).
and subepidermal (L2) cell layers was also and fossils, including the Bennettitales and
followed through the use of genetically the true flowers of Angiosperms, are Organ Identity Genes
marked lineages. In addition, some un- evolutionarily related (Doyle, 1994). How-
derstanding of the basis of the phyllotactic ever, this particular scheme is now dis- One question investigated in detail was how
pattern of leaf initiation was obtained by credited because molecular phylogenetic the individual developmental path followed
manipulating the developing meristem, al- study has revealed that the Gnetophytes by a newly arising organ—either sepal,
though these studies were not extended to are most closely related to conifers among petal, stamen, or carpel—was determined.
flowers. the Gymnosperms and are not the sister The answers came from the study of
Study of the comparative development group of the Angiosperms, and so their mutants. Plant biologists have long been
of flowers reached its zenith later in the reproductive structures are presumably fascinated with the abnormal, the mon-
twentieth century. The invention of the similar to flowers by convergent evolution strous, and the defective (Meyerowitz et al.,
scanning electron microscope in 1952 (Crepet, 2000). The evolutionary origin of 1989). Goethe (1790) had drawn attention to
allowed simple and detailed examination each type of floral organ also was not observations of what he called abnormal
of early developmental events. These stud- resolved (Arber, 1937; Cronquist, 1988; metamorphosis. This refers to the situation
ies provided new characters, such as the Endress, 1994). where the organs that are normally formed
order of initiation of floral organs, to help On the other hand, firm deductions about on a plant in a time series (cotyledons,
distinguish between closely related spe- the directions of floral evolution within the leaves, bracts, sepals, petals, stamens, and
cies. More generally, such comparative angiosperms have recently become possi- styles) ‘‘are sometimes transformed, so that
studies provided insights into the relative ble. Accurate phylogenies of most orders they assume—either wholly or in some
rates and possible directions of evolution of and many families have been assembled lesser degree—the form of the nearest in
floral form. For example, Endress (1994) from multiple data sets: morphology, the the series.’’ Bateson (1894) invented a
highlights three aspects of flower structure sequences of translated genes from nuclei, new name for abnormal metamorphosis,
with different underlying rates of evolution- plastids and mitochondria, and the se- homeosis, arguing that ‘‘the essential
ary change. He calls these organization, quences of nuclear rRNA genes (Soltis et phenomenon is not that there has been
construction, and mode. Essentially, these al., 1999; Angiosperm Phylogeny Group, a change, but that something has been
correspond with, first, the floral blueprint 2003). These definite lineages have, for changed into the likeness of something
(bauplan) that defines the number and example, allowed the structure of ances- else.’’ Homeotic changes were recognized
position of organs (including their degree tral flowers to be deduced as probably as providing clues about the normal organ-
of fusion with each other), second, the being small and primarily bisexual, with ogenetic process (Meyerowitz et al., 1989),
basic three-dimensional structure of the few to moderate numbers of organs often although some have erroneously argued334 The Plant Cell HISTORICAL PERSPECTIVE ESSAY that they represent atavistic reversions to 2, and 3, is redundantly involved in defining shoots with inflorescence-like properties. more primitive forms. the petal, stamen, and carpel domain of The FLORICAULA gene of Antirrhinum It was argued that the normal function of the flower primordium in Arabidopsis (Pelaz (Coen et al., 1990) and LEAFY, its ortholog such homeotic mutant genes was to define et al., 2000). SEPALLATA function, some- from Arabidopsis (Weigel et al., 1992), the identity of the organ. Their cloning and times called E function, is sufficient to encode transcription factors that impose characterization would test this idea. Such transform leaves into petal-like structures a floral identity on primordia that arise from an approach had proved spectacularly suc- in combination with A and B function and the flank of shoot apical meristems after their cessful in insects in gaining an understand- into stamen-like organs with B and C floral induction. Floral meristem identity is ing of how body segment identity is function (Honma and Goto, 2001). This also promoted by a MADS box transcription determined through the action of homeobox was soon nicely integrated with the finding factor gene in these species, the orthologs genes (Bender et al., 1983). For plants, two that MADS polypeptides associate as SQUAMOSA and APETALA1 in Antirrhinum model species were mainly involved, the multimers (Egea-Cortines et al., 1999), and Arabidopsis, respectively. Interestingly, mouse ear cress Arabidopsis thaliana and when pairs of known ABC MADS pro- in other species, the functions of all these the snapdragon Antirrhinum majus. For teins were shown to also associate with genes do not always include specification of Arabidopsis, its convenient genetics SEPALLATA proteins (Honma and Goto, flower meristem identity. In passing, study of (Koornneef et al., 1983) and small genome 2001). LEAFY gene function in Arabidopsis has allowed genes to be cloned based on their Of the proposed organ identity functions, revealed the basis of the unusual flower map position. For Antirrhinum, active trans- A function has not been confidently defined initiation property of this species—flowers posable elements had already been cloned, beyond Arabidopsis. The main MADS gene arise naked from the flank of the inflores- and this, coupled with a large series of associated with A function, APETALA1, has cence meristem. In many species (including characterized flower mutants (Stubbe, an earlier flower meristem identity function Antirrhinum), they arise from the axil of a leaf- 1966), was the basis of cloning of genes that is present in many other species, but like bract generated by the meristem. It with unstable, transposon-induced mutants. a role in sepal and petal identity specifica- seems this potential remains in Arabidopsis, Based on single and multiple mutant tion elsewhere is not apparent. The other but bract development is normally inhibited phenotypes, it had already been proposed known A function gene from Arabidopsis, by LEAFY function. that organ identity genes ‘‘allow cells to APETALA2, is a member of a different A later role of these genes is to establish determine their place in the developing family of plant-specific transcription factors the expression of floral organ identity genes, flower,’’ and that they acted combinatori- (Jofuku et al., 1994). Its ortholog from at least in Arabidopsis (Lohmann and ally by ‘‘setting up or responding to Antirrhinum occurs as recently duplicated Weigel, 2002; Jack, 2004). For example, concentric, overlapping fields within the genes, LIPLESS1 and 2, and these do not expression of B function genes is lost in flower primordium’’ (Bowman et al., 1989). repress expression of C function genes, leafy apetala1 double mutants, and expres- When homeotic genes were cloned, these although they do influence sepal and petal sion of the C function gene AGAMOUS is predictions were borne out. The first to development to some extent (Keck et al., directly activated by LEAFY. be cloned was the DEFICIENS gene of 2003). APETALA2 is expressed throughout In flower meristems, the maintenance of Antirrhinum (Sommer et al., 1990), soon the flower, even in the stamen and carpel the central stem cell zone is at first regulated followed by the AGAMOUS gene of regions where C function inhibits its action. by the same genes that maintain the shoot Arabidopsis (Yanofsky et al., 1990). In Recently, it has been discovered that apical meristem (Leyser and Day, 2003). In each case, the genes encoded transcrip- APETALA2 function is regulated posttras- Arabidopsis, this apparently involves a self- tion factors related to several already criptionally by a specific microRNA sustaining feedback loop. The homeobox known in humans and yeast and together miR172, with evidence that this includes transcription factor WUSCHEL promotes were called the MADS family. The action of inhibition of translation (Aukerman and stem cell properties immediately above the organ identity genes in Arabidopsis and Sakai, 2003; Chen, 2004). Thus, it seems organizing center where it is expressed. Antirrhinum was soon summarized in the that C function is inhibiting APETALA2 A The size of this center is constrained by ABC model (Coen and Meyerowitz, 1991), function through its sharing of a common CLAVATA signaling proteins. WUSCHEL now well known. It can be summarized as expression domain in the flower primor- promotes production of the CLAVATA3 follows: A function defines sepals, A1B dium with this microRNA. How this domain ligand in the overlying stem cells, and this petals, B1C stamens, and C carpels, with is jointly defined is not yet known. ligand then moves downward and sideways A and C antagonizing each other’s func- and likely interacts with the CLAVATA1 re- tion. Subsequent studies have modified Flower Meristem Genes ceptor. This receptor is present in a wider and refined the ABC model and extended zone than WUSCHEL, and it apparently it to many other species (Lohmann and Just as floral organs have a genetically de- prevents CLAVATA3 from moving further Weigel, 2002; Jack, 2004). fined fate, so do floral meristems. Genes in and inhibiting WUSCHEL expression. A An important recent discovery was that involved here were first identified from constant number of stem cells is thus another set of MADS genes, SEPALLATA1, mutants in which flowers were replaced by maintained. However, unlike shoots, flower
February 2005 335
HISTORICAL PERSPECTIVE ESSAY
meristems eventually terminate growth Organ Polarity Genes radial symmetry (with two, three, four, five,
(they are determinate). The C function or more axes of symmetry) and those with
gene AGAMOUS is involved here with Another aspect of spatial divergence in- bilateral symmetry (with only one axis, so-
another function in addition to its role in volves specification of the polarity of in- called mirror image flowers) (Figure 2A).
organ identity. It also suppresses the dividual organs. Genes that control which Biologically, the latter are associated with
transcription of WUSCHEL, thus terminat- side of an organ is which (i.e., whether insect and vertebrate pollination where
ing cell proliferation in the central zone adaxial or abaxial) were discovered in floral bilateral visual cues direct the pollinator to
(Lenhard et al., 2001; Lohmann et al., 2001). organs and leaves, and the same functions a reward within the flower. Bilaterality in
seem to apply in each case. Generally, flowers seems to be the derived form,
flattened organs arising from the flanks of having arisen independently in many line-
Organ Boundary Genes both shoot and flower meristems are now ages, especially advanced ones (Donoghue
The genetic mechanisms by which organ called lateral organs, although I suggest et al., 1998; Endress, 2001b). The sym-
spacing is set up and maintained constitute that an Anglicized version of the term Blatt metry difference is apparently genetically
a different category of genetic function in the sense that Goethe used it (see above) controlled, as botanists interested in de-
within the flower, and our understanding of is more appropriate. Genes from three formed flowers had noticed a special cat-
this area is also growing. Genes involved in families of transcription factors are in- egory called ‘‘peloric,’’ in which large radial
organ spacing can be conveniently divided volved. Two, first discovered through floral flowers sometimes occurred in species
into two categories: those that regulate mutants of Arabidopsis, were the YABBY that are normally bilateral. The cloning of
boundaries between whorls of different family (Sawa et al., 1999; Siegfried et al., two related genes associated with peloric
organs and those that keep organs of the 1999) and the KANADI family (Eshed et al., mutant phenotypes in the bilateral model
same type separate within whorls. In the 2001). These are expressed in outer (abax- species Antirrhinum revealed how bilater-
former category, the SUPERMAN (SUP) ial) regions of newly growing primordia. ality may be imposed (Luo et al., 1995,
gene of Arabidopsis was characterized Conversely, the third family, comprising the 1999). These genes, CYCLOIDEA and
early, and its function is best understood type III HD-Zip transcription factors PHA- DICHOTOMA, encode transcription factors
(Sakai et al., 1995, 2000). In sup mutants, BULOSA, PHAVOLUTA, and REVOLUTA, of the TCP class that apparently act to
additional stamens develop at the expense is expressed in the inner (adaxial) domain suppress growth in the upper (adaxial) part
of carpels. Cloning of the gene revealed that (McConnell et al., 2001). It seems that of the developing flower primordium. This
it encodes a C2H2 zinc finger transcription the functions of the adaxial-promoting creates an abaxial–adaxial polarity that
factor and that the gene is expressed early PHABULOSA-like family and the abaxial- results in diversity in the form that floral
in the third whorl where stamens sub- promoting KANADI family members are organs, especially petals and stamens,
sequently arise, and later only in the region mutually antagonistic, based on comple- adopt in upper and lower parts of the
adjacent to the fourth whorl. Genetic and mentary phenotypes following either their flower. Without the function of the two
molecular evidence indicates that the SUP loss or gain of function. The YABBY family genes, all petals and all stamens are very
protein inhibits proliferation of cells at the seems to be involved in sideways out- similar in each case.
inner boundary of the third whorl. growth of organs following earlier estab-
The paradigm for genes that control lishment of their polarity by members of the
WHAT DON’T WE KNOW?
organ boundaries within whorls is the other two families. Again, it has recently
CUP-SHAPED COTYLEDON (CUC) family been found that regulation of the three
PHABULOSA-like genes includes a post- How Is the Floral Ground
of genes of Arabidopsis, first identified in Plan Established?
Petunia as the NO APICAL MERISTEM transcriptional step, this time by microRNA
gene (Souer et al., 1996). cuc mutants are miR165/166 (e.g., Emery et al., 2003). Despite much progress, we still don’t un-
characterized by lateral fusion of radially Lateral organs (blatts) also have polarity in derstand how spatial information is gener-
adjacent organs, including sepals and sta- a second dimension, lateral/medial, and this ated to set up the blueprint (bauplan) of the
mens (Aida et al., 1997). At least three CUC is influenced by another gene, the PRESSED flower (Figure 2). The number of organs of
genes, all members of the multimember FLOWER homeodomain gene of Arabi- each type is highly conserved. For instance,
NAC family of transcription factors, are dopsis (Matsumoto and Okada, 2001). most monocots have trimerous flowers,
generally expressed in boundaries be- PRESSED FLOWER is expressed specifi- whereas many eudicots are tetramerous or
tween organs, where they also may act cally in lateral domains of leaves, sepals, pentamerous (Figure 2A) (Cronquist, 1988;
individually to suppress intercalary growth. petals, and stamens and, at least in the Endress, 1994; Judd et al., 2002). Loss of
Recently, it has been shown that the sepals, seems to promote lateral growth. function of the bZIP transcription factor
boundary-specific location of CUC1 and Genes Controlling Bilateral Symmetry gene PERIANTHIA often makes Arabidopsis
CUC2 function is regulated posttranscrip- flowers pentamerous (with five sepals,
tionally by microRNA miR164 (Laufs et al., It has long been recognized that flowers petals, and stamens), although how this
2004; Mallory et al., 2004). occur in two basic designs, those with occurs is not clear (Chuang et al., 1999).336 The Plant Cell
HISTORICAL PERSPECTIVE ESSAY
Loss of function of CLAVATA genes also
leads to extra organs, but this seems to be
a consequence of an increase in size of the
flower meristem (Clark et al., 1993).
Recently, the spacing and timing of leaf
primordium initiation has been shown to be
regulated by auxin and cytokinin gradients
(Reinhardt et al., 2003; Guilini et al., 2004),
and similar processes may well be involved
for floral organs. Certainly, disruption of
auxin transport results in major upsets to
floral organ number (Okada et al., 1991).
However, the situation in flowers is much
more complex than in the vegetative shoot:
with up to four different organ types arising
in defined succession, either in a whorled
or spiral phyllotaxy (Figure 2B); with the
new primordia arising either opposite or
alternate to organs that have already arisen
(Figure 2C); with whole whorls sometimes
reiterated, and in some cases two organs
arising in place of one (dédoublement), or
vice versa (Figure 2D) (Endress, 1992). It is
challenging to believe that such complexity
could be set up as a self-organizing
system, but at least we have a simpler
precedent in the shoot apical meristem.
Other aspects of the floral ground plan
are also conserved. These include whether
(D) Duplication of organs may occur by the
reiteration of a whorl (as in poppies) or by two
organs arising in place of one or vice versa
(dédoublement, as in Lepidium [Brassicaceae]).
(E) Organs may either be free or show different
patterns of fusion with each other. Those within
a whorl may be coherent in a tube (e.g., the
corolla of Antirrhinum). Different types of organ
may be adherent (e.g., the stamens and corolla of
Antirrhinum). These forms are usually congenital.
Post-genital fusions occur after organs have
formed (e.g., anthers in the daisy family, Aster-
aceae).
(F) The place of attachment of the perianth
organs and stamens varies. They may be
attached to the receptacle near the base of the
Figure 2. Variations in Floral Structure.
ovary (hypogynous) or at the top of the ovary
(A) The symmetry of flowers is defined by the number of similar axes that can be drawn through its plan. (epigynous). They are sometimes attached on the
Radially symmetric flowers (also called regular or actinomorphic) have two or more axes and include rim of a floral tube (perigynous), which itself may
many monocots (3), Arabidopsis (2, derived from 4), tomato, and Petunia (5). Bilaterally symmetric be basal or apical to the ovary. The ovary is either
flowers (also called irregular, zygomorphic, or mirror-imaged) have only one and include Antirrhinum superior if the other organs (or a floral tube) are
and the pea family (Papilionaceae). attached to its base or inferior if they are attached
(B) Phyllotaxy of organs may be spiral (especially in the basal angiosperms) or whorled. to its apex. The floral tube is sometimes called
(C) Organs may arise alternate with, or opposite to, those in the adjacent whorl. a hypanthium.February 2005 337
HISTORICAL PERSPECTIVE ESSAY
organs are attached to each other in tempts are now being made to define Irish, 2003). The resolution of these meth-
a pattern that is either connate (cohesion complete cell lineages within develop- ods can be greatly improved by confining
within a whorl) or adnate (adhesion be- ing Arabidopsis flowers (Reddy et al., the comparison to short time intervals
tween whorls) (Figure 2E). In evolutionary 2004) and the allometry of growth in through using a conditionally expressed
terms, lack of fusion seems to be ancestral developing Antirrhinum petals (Rolland- version of the gene (William et al., 2004) or
(Endress, 2001a). Modifications to this Lagan et al., 2003), with the ultimate by assessing expression in limited amounts
pattern can be envisioned as arising from aim of understanding their regulatory of tissue achievable by laser capture
differential changes in growth. For exam- basis. microdissection (Meyers et al., 2004).
ple, fusion of organs within a whorl, such as Most flowers are hermaphrodite, but The context of action of transcription
fused petals within the corolla, mostly a derived form of floral architecture is factors is also now being better under-
seems to result from intercalary growth found in unisexual flowers of dioecious stood. It is clear that the condition of the
between initially distinguishable primordia. and monoecious species. It seems that in chromatin in which target genes are em-
Such fusion is congenital, compared with many unisexual flowers, the male and bedded is important (e.g., histone modifi-
post-genital fusions between already female organ primordia arise, but those of cation status and DNA methylation and the
formed structures that presumably occur one sex or other stop growing early in maintenance of these states) (Goodrich
by different mechanisms (Raven and development. Despite some clues from and Tweedie, 2002; Reyes et al., 2002).
Weyers, 2001). mutants of monoecious maize, the nature These may lead to stable epigenetic
Another aspect of the ground plan of of the molecular switch that generates changes within extensive and long-lived
phylogenetic importance is the site of unisexual flowers is still not known in any cell lineages, such as those that occur in
insertion of the outer organs relative to species (Tanurdzic and Banks, 2004). On plants. Also, the combinatorial presence of
the ovary (Cronquist, 1988; Judd et al., the other hand, the molecular basis of other transcription factors, and coactivator
2002). They may be either attached close self-incompatibility not associated with or corepressor proteins, helps generate
to its base (hypogyny, with the ovary physical differences between plants is diversity of outcomes based on a limited
superior) or to its apex (epigyny, with the relatively well understood (Kachroo et al., number of factors and targets. In yeast,
ovary inferior) (Figure 2F). In some cases, 2002; Franklin-Tong and Franklin, 2003). global approaches to identifying all pos-
the peripheral organs all arise at the top of Surprisingly, this does not yet extend to sible interactions between proteins (the
a floral tube (perigyny). Perigyny can the molecular genetic basis of heterostyly, interactome) have been performed (Uetz
occur with the tube attached either at a form of genetically controlled self- et al., 2000), and similar mapping of plant
the base or the apex of the ovary, incompatibility associated with reciprocal proteins is possible in yeast and in plant
although intermediate attachment also differences in stamen and style length cells (Immink et al., 2002). Genetic ap-
occurs. Differential early growth can ac- (Barrett et al., 2000). proaches are also possible. For example,
count for these different patterns (Soltis et mutant screens to identify enhancers of A
al., 2003). Compared with the hypogynous Transcription Factors—What Are Their and C organ identity function have un-
ancestral condition (Endress, 2001a), ad- Regulators, Interactors, and Targets? covered the AGAMOUS corepressor pro-
ditional growth of the flower primordium teins LEUNIG and SEUSS (Franks et al.,
outside the ovary could result in epigyny if It is apparent that most flower development 2002) and a gene (HUA ENHANCER1)
it remains coherent (apparently fused) with genes known to date encode transcription involved in processing microRNA 172 that
the ovary. If such growth is not attached, factors, but the function of a transcription targets APETALA2 mRNA for inactivation
or if it continues above the ovary, then factor is to regulate the expression of other (Chen, 2004). It is interesting that a relatively
perigyny would result. To me, arguments genes, and until we know what these genes large number of transcription factor genes
about whether such growth represents are, we won’t know exactly how the involved in plant morphogenesis are sus-
receptacle tissue or floral organ tissue transcription factor regulates morphogen- ceptible to microRNA regulation. Within
seem semantic because the receptacle is esis. Very few direct downstream target flowers, these include members of the
defined by its location rather than being genes are known so far (Jack, 2004). We do APETALA2, CUC, and PHABULOSA fam-
a specific tissue type (Raven and Weyers, know that LEAFY directly activates APE- ilies. It may be that this form of mRNA
2001). TALA3 and AGAMOUS expression and degradation or blockage occurs rapidly,
Understanding how the complex topo- that AGAMOUS activates SPOROCYTE- avoiding any effect of long-lived transcripts
graphical interplay between growth pro- LESS, but there are few other examples. in fast changing cellular environments
motion and suppression is set up and This may soon change, however, as geno- (Rhoades et al., 2002).
maintained within the flower primordium mic approaches are adopted. Targets may Although not transcription factors, roles
is a big challenge, although roles for hor- be identified by comparing expression in flower development are known for at
mones and other unknown morphogens, patterns of all genes in plants that differ least one of the 700 or so F-box genes
microRNAs, and growth-suppressing by only one specific transcription factor found in the Arabidopsis genome,
boundary genes can be predicted. At- function (e.g., Schmid et al., 2003; Zik and UNUSUAL FLORAL ORGANS, and its338 The Plant Cell
HISTORICAL PERSPECTIVE ESSAY
Antirrhinum ortholog FIMBRIATA (Lohmann transcription factor proteins are capable of established to extend knowledge of de-
and Weigel, 2002; Jack, 2004). F-box limited movement between cell layers. Also, velopmental genes known from model
proteins target specific proteins for degra- the small CLAVATA3 peptide, a ligand for species more broadly across a selection
dation via the proteasome. It seems likely the CLAVATA1 receptor-like kinase, is mo- of angiosperms (Soltis et al., 2002). The aim
that many additional F-box proteins will bile within the central zone of the shoot and is to identify cDNAs of orthologous genes
be uncovered when the targets of flower flower meristem (Lenhard and Laux, 2003). and to map their expression patterns as an
development transcription factors are We also know that those RNAs involved in indication of their function. This will help
defined. Perhaps extensive redundancy, RNA silencing are capable of acting at test the generality of function of already
or vital pleiotropic actions earlier in de- a distance within a plant, although how far known genes, although genes not yet
velopment, have kept them hidden so far microRNAs move needs to be examined, identified, or those that do not function in
during mutant screens of flower develop- especially those that target developmentally the model species, are unapproachable by
ment. regulated transcripts. A role for lipid-like this strategy (Baum et al., 2002). Baum et
One outcome of all this knowledge about molecules, including sterols, is not estab- al. (2002) argue that a more informative
developmental cascades of transcription lished, although they are implicated by the approach would be to develop a wider
factor action will be the ability to model presence of putative sterol binding sites range of model species in which function is
flower development so that gaps will be in, for example, the PHABULOSA-family of examined in depth. Already, functional and
revealed and predictions made about un- transcription factors (McConnell et al., genomic information is accumulating in
known outcomes. Indeed, such model 2001). Tantalizingly, these sites are also other model species, with rice (Shimamoto
building using known organ identity genes targets of microRNA binding (Emery et al., and Kyozuka, 2002) and maize (Lawrence
of Arabidopsis has already begun 2003). Also, among the hormones, auxin is et al., 2004) providing divergent monocot
(Espinosa-Soto et al., 2004). known to move in specific directions asso- information that is intrinsically important as
ciated with early developmental decisions well as allowing comparisons with data
How Is Spatial and Dimensional (e.g., Reinhardt et al., 2003). Overall, it is from the established core eudicots. Baum
Information Signaled? an open question how far these scattered et al. (2002) also argue that hypotheses
observations will be generalized and about function will be readily testable in
Perhaps the largest gap in our present whether unknown signaling mechanisms, species closely related to established
understanding is how morphogenetic sig- especially any that sense internal physical models. For example, comparative study
nals are generated, transmitted, perceived, forces, await discovery. of the role of the LEAFY transcription factor
and acted on in the developing flower (Golz in controlling the generation of single
and Hudson, 2002). We know such signals How Do Flowers Evolve? rosette flowers in two different relatives of
exist because, for example, floral organs Arabidopsis has indicated that it has
retain fixed relative locations and orienta- Evolution involves genetic change. We are occurred by parallelism, with the same
tions within the flower meristem (e.g., Griffith already approaching an understanding of morphological outcome resulting from in-
et al., 1999). Within organs, feedback must the underlying genetic basis for rapidly dependent modifications to LEAFY gene
somehow be signaled so that the organ evolving aspects of the flower. Genes function (Yoon and Baum, 2004).
adopts the appropriate size and shape. This controlling traits such as the pollination Generally, our understanding of the
is apparently not related to cell number be- syndrome can be identified in segregating mechanisms of evolution of morphology
cause size and cell number can be un- populations from crosses between differ- (evo-devo) is at an exciting stage. In
coupled (Foard and Haber, 1961; Hemerly ent interfertile species (i.e., quantitative trait flowering plants, the rapid explosion in
et al., 1995). Whether or not physical forces mapping). Recent successful examples of diversity that followed their origin in the
are involved (Green, 1999) has not been this approach are the mapping of loci early Cretaceous (;130 million years ago)
established, although they alone cannot be corresponding to 12 floral traits, mostly may be linked to modularity within their
responsible. It seems likely that morpho- involving petal color and shape, in the new structure, the flower (Carroll, 2001).
gens, by triggering specific actions in a monkey flower (Mimulus) (Bradshaw et al., Synergies resulting from interactions be-
concentration-dependent manner, are cen- 1998), and of petal color, corolla and tween floral organ modules with different
tral to developmental processes. stamen length, nectar production, and functions may have promoted the relatively
The nature of intercellular signaling mol- fragrance in Petunia (Stuurman et al., fast rate of evolution because floral struc-
ecules, and their pathways of movement, 2004). Eventually, the molecular function ture is itself strongly associated with re-
are beginning to be established, both of these genes may be identified through productive success. The origin of these
between adjacent cells (either by direct a candidate gene approach using the modules is still an open question, however,
secretion or through plasmodesmata) and growing knowledge base in model species. and the discovery of new fossils of the
between organs (through the epidermis, The basis of evolution of more conserved immediate ancestors of angiosperms
cortex, or phloem) (Haywood et al., 2002; properties of the flower is less accessible. would be a major advance (Crepet, 2000;
Wu et al., 2002). We know that several Recently a floral genome project was Stuessy, 2004).February 2005 339
HISTORICAL PERSPECTIVE ESSAY
Just as modular structures have prolifer- ACKNOWLEDGMENTS Bowman, J.L., Smyth, D.R., and Meyerowitz,
ated, so have the controlling genes. There E.M. (1989). Genes directing flower develop-
I thank past and present students and col- ment in Arabidopsis. Plant Cell 1, 37–52.
are more than 1500 transcription factor
leagues at Monash University for stimulating Bradshaw, H.D., Jr., Otto, K.G., Frewen, B.E.,
genes in Arabidopsis (Riechmann, 2002),
discussions and interactions, Cris Kuhlemeier for McKay, J.K., and Schemske, D.W. (1998).
many occurring in large families. Duplication access to information before publication, and Quantitative trait loci affecting differences
of a transcription factor gene immediately the Australian Research Council for long-term in floral morphology between two species
opens the possibility of divergence in func- research support. of monkeyflower (Mimulus). Genetics 149,
tion as either gene can maintain the existing 367–382.
function. Two routes are available: changes Carroll, S.B. (2001). Chance and necessity: The
in the translated sequence that may alter David R. Smyth evolution of morphological complexity and
target genes and influence interacting pro- School of Biological Sciences diversity. Science 409, 1102–1109.
teins or changes to the regulatory sequences Monash University Chen, X. (2004). A microRNA as a translational
that may result in transference of function Melbourne, Victoria 3800 repressor of APETALA2 in Arabidopsis flower
in developmental time or space. For exam- development. Science 303, 2022–2025.
Australia
Chuang, C.-F., Running, M.P., Williams,
ple, recent evidence reveals that the B david.smyth@sci.monash.edu.au
R.W., and Meyerowitz, E.M. (1999). The
function gene APETALA3 duplicated and
PERIANTHIA gene encodes a bZIP protein
the C-terminal end diversified in ancestors of
involved in the determination of floral organ
core eudicots such that B function now number in Arabidopsis thaliana. Genes Dev.
controls the identity of petals as well as 13, 334–344.
stamens (Lamb and Irish, 2003). Clark, S.E., Running, M.P., and Meyerowitz,
Extending phylogenetic assays of known E.M. (1993). CLAVATA1, a regulator of meri-
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