List of clades in which radial symmetry is conserved in all or most of its descendents.
Flower Symmetry is a key evolutionary innovation in some lineages of angiosperms. The flowers of the primitive angiosperm plants were radially symmetrical actinomorphic. Later bilaterally symmetrical zygomorphic flowers independently evolved in several clades of angiosperms. This transition of trait is associated with an adaptation to specialized methods of pollination. Zygomorphic flowers allow more specific plant insect interaction. So, the transition from radial symmetry to bilateral symmetry facilitates reproductive isolation which in turn might have led to diversification or rapid speciation of some lineages in angiosperms. Phylogenetic analyses in lineages of angiosperms revealed that few clades have shown that there have been reversals, that is, there is transition from bilateral symmetry to radial symmetry. When such studies are correlated with genetic studies, it is revealed that CYC (TCP family) transcription factors are responsible for the transition of this floral trait. Phylogenetic analyses, genetic studies and Evo-Devo analyses can answer important questions such as what other transition in floral symmetry is found in angiosperms? Is there a pattern of floral symmetry transition in different lineages? Do these transitions act as key innovation for the clades in which they have evolved?
- floral symmetry
Flower is a significant novelty for evolutionary success in angiosperms. It primarily comprises four whorls—sepals, petals, stamens, and carpels. The shape of the flower changes because of change in the shape or morphology of any of these whorls. This gives rise to different shape and symmetry of flowers. The change in symmetry can occur in any of the whorl; however, it is widely studied in petals . Floral symmetry is an important trait as it impacts the visual appearance of a flower. Hence, it’s been a fascination for human eye. Pollinators are usually attracted to flowers due to its diverse forms of colors but also due to the symmetry it possesses, thereby contributing to the plant pollination syndrome [2, 3, 4]. Broadly there are the two types of floral symmetry, radial symmetry also known as polysymmetry or actinomorphy and bilateral symmetry also known as monosymmetry or zygomorphy. Flowers with radial symmetry have more than two planes of symmetry and are called as actinomorphic. Flowers with bilateral symmetry have single plane of symmetry and are called as zygomorphic [5, 6, 7]. There is another rare form of symmetry in flowers that is known as asymmetry . This refers to morphologies where there is no pane of symmetry (Figure 1).
These categories have been studied at various different levels such as the molecular aspects of these transitions and how the pollinators perceive them [5, 6]. There have been transitions from actinomorphy to zygomorphy many times during the diversification of angiosperms, and these transitions are more common in species-rich lineages such as Fabaceae, Lamiales, and Orchidaceae. However, reversals from zygomorphy to actinomorphy are also reported [9, 10, 11, 12].
We in this chapter focus on the different genetic studies, which have been conducted to understand the molecular basis of the variation in floral symmetry and what do we get to know when these studies are correlated with phylogenetic studies. These studies have provided insights into how and when these transitions in floral symmetry evolve.
2. Diversity of floral symmetry in angiosperm flowers
Apart from the flower symmetry categories mentioned above, there are many other forms of flower symmetry such partial zygomorphy and few others. There are different degrees of symmetry. In the year 1925, based on the aspects of symmetry as used in crystallography, new terms were introduced. Of those rotational symmetry, mirror symmetry and spiral symmetry are to name a few .
Later correlation studies between floral symmetry and pollination biology were conducted. These studies focused on how pollinators perceived flowers. With these studies, three-dimensional aspects were added to the floral symmetry terminology [10, 14, 15]. After around 75 years, an elaborated and modified classification was proposed, which was also based on visual perception of flowers by the pollinators [2, 3]. These terminally only applied to very discreet flower forms and only in mature flowers .
However, there are variable degrees of floral symmetry at different developmental stages. This variation can also be seen in different lineages, or there might be convergent evolution of this state in two different and closely unrelated clades. Endress  considered these two aspects, that is, developmental changes and phylogenetic changes, and identified three forms of monosymmetry and three forms of asymmetry.
First form of monosymmetry is found in taxa with elaborated monosymmetric flowers, for example, Lamiales, Asterales, and Leguminosae. The second is taxa in which monosymmetry arises, but predominantly the group is polysymmetric, e.g.,
3. The genetic basis of flower symmetry
The genetics of a flower is regulated by specific transcription factors (TFs) . TFs such as MADS (First alphabet of MCM1 in yeast, AGAMOUS in Arabidopsis, DEFICIENS in snapdragon, and SERUM RESPONSE FACTOR in human)-box are widely studied for various developmental pathways from root development to fruit development. One important role is determination of organ development in flower. ABCDE model and its modifications are based on the different functions of
Floral development is also controlled by other set of TFs Known as
Recent studies show that
3.1 Developmental genetics of floral symmetry in dicots
The molecular basis of floral symmetry was first studied in
Another member of clade lamiales
More complex mechanism takes place in Asteraceae. Here the inflorescence is complex and is known as capitulum. For example, in
3.2 Developmental genetics of floral symmetry in monocots
Little is known about floral symmetry in monocots. Orchidaceae family supports the DDR (DDR stands for DIV, RAD, and DIV-and-RAD-Interacting Factor DRIF) regulatory module . Recent study revealed that
4. Other putative genes
Other putative genes are such as
5. Phylogenetic pattern in floral symmetry
Floral symmetry patterns are best understood in phylogeny context. These studies help in understanding how often the transition from radial symmetry to bilateral symmetry has occurred and vice versa. It also gives insight on what lineages these transitions have taken place and when those transitions occurred on geological timescale.
We now have clear understanding about the major lineages of angiosperms. Recent studies focus on mapping various morphological traits on these robust phylogenetic analyses. In relation to floral symmetry, recent studies have constructed it as a character and different forms (radial symmetry, bilateral symmetry, asymmetry, etc.) on phylogenies . Such robust studies have answered the abovementioned questions.
Studies revealed that the ancestral flower of angiosperms was radially symmetrical . Floral symmetry character reconstruction on ordinal phylogeny also revealed the same scenario and showed that the transition to bilateral symmetry is widespread on angiosperm phylogeny. Parsimony reconstruction on family phylogeny revealed that there are at least 70 such transitions from radial to bilateral symmetry in angiosperms including 23 in monocots and 46 in eudicots .
Later studies focused on detailed phylogeny of smaller clades. Character reconstruction of floral symmetry in Lamiales at family level revealed one transition from radial to bilateral symmetry and one vice versa . Multiple transitions from radial to bilateral symmetry were observed in Brassicaceae, Ranunculaceae, and Solanaceae [52, 53, 54].
Bilateral symmetry has evolved at least 130 times independently in different clades, and there were at least 70 reversals . Based upon these transitions, four basic groups have been observed. These are: first, there are clades where radial symmetry is conserved (Table 1). Second, clades wherein bilateral symmetry has evolved independently (Table 2). Third, clades wherein bilateral symmetry arises as single early event (Table 3), and fourth group includes clades that show reversal to radial symmetry (Table 4). Basal angiosperms have radial symmetry with exceptions such as in
|Group 1||Amborrellales, Pandanales, Arecales, Dasypogonaceae, ceratophyllales, Trochodendrales, Buxales, Gunnerales, Dileniales, Vitales, Celastrales, Oxalidales, Fagales, Crossosomatales Picramniales, Heurteales, Malvales, Berberidopssidales, Cornales, Nymphaellales, Austrabaileyales, Chaloranthales, Canellales, Magnoliales, Petrosaviales, Aquifoliales, Escalloniales, Bruniales, Paracryphiales, Garryales, Icacinaceae, Metteniusaceae, Oncothecaceae, Vahliaceae|
|Group 2||Piperales, Laurales, Acorales, Alismatales, Dioscoreales, Liliales, Asparagales, Poales, Commelinales, ranunculales, Proteales, Sabiales, Saxifragales, Zygophyllales, Malphighiales, Fabales, Rosales, Cucurbitales, Geraniales, Myrtales, Sapindales, Brassicales, Santalales, Caryophyllales, Ericales. Apiales, Dipsacales, Asterals, Boraginaceae, Gentianales, Solanales|
|Group 3||Zingiberales, Lalmiales Acorales, Fabales, Dispacales|
|Group 2||Orchidaceae, Fabaceae, Malpighiaceae,Capparaceae, Cleomaceae, Brassicaceae, Caprifoliaceae and Aster-aceae|
6. Floral symmetry on geological timescale
First fossil remains of flowers with inserted flower parts are found to be from early Cretaceous period (Barremian-Aptian period) around 125 million years ago (Ma.). This fossil represents the flowers of the ancestors of early Nympheales [56, 57]. The first fossil of a flower, which is pentamerous, was reported from late Cretaceous period (Cenomanian period) around 100 Ma. This fossil remains has both petals and sepals. It is considered as a representative of ancient ancestor of Eudicots .
Clearly, the above fossil records show that there was a transition from closed floral structure to an open floral structure. The flower evolved from closed noncyclic structures to more open and cyclic forms. This transition took place in Mid-Cretaceous period. It is during this period that many floral traits evolve. Many of these traits are key innovations. This floral trait evolution coincides with the major diversification period of angiosperms [59, 60].
The first transition from radial symmetry to bilateral symmetry can be traced to the first radiation in angiosperms. These flower remains are reported from Turonian fossils from late Cretaceous, which is around 100 Ma. These flower fossils have staminodal nectaries making the radial flower partially bilateral. These flowers fossils are the first report of zygomorphic flower form, although these forms were not exactly bilaterally symmetrical. These fossils represented the precursors or ancestors of zygomorphic flowers [59, 61].
First complete zygomorphic flowers are recorded from Paleogene (Paleocene-Eocene period) around 55 Ma . This is the time period where a second major diversification of angiosperms took place. So, we have seen that both the radiation events of angiosperms diversification coincide with the evolution of floral traits including floral symmetry . Thus, floral symmetry transition is clearly the key innovation, which might have played crucial role in radiation of angiosperms. Of course, there might be other factors too that played their part. One such factor is evolution of pollinators.
Interestingly, the evolution of those floral traits that lead to diversification of angiosperms in the above-said events coincides with the advent of specialized pollinators. Also, the evolution of bilateral symmetry in some plant lineages cooccurs with the time period when there was a rise of some bee families. Thus, in some lineages the Coevolution of insect pollinators with the floral symmetry holds true [2, 5]. Although there are other abiotic and biotic factors that are needed to be taking into account such as climatic conditions and various architectural components of flower.
Great deal of progress is being made on study of floral symmetry evolution in dicots. The
Most of the species-rich lineages have bilateral symmetry. Based on this observation, many hypothesize that bilateral symmetry is related to increased specificity to pollinators, thereby increasing the chances of reproductive isolation. This holds true for many taxa, but not all lineages of angiosperms follow the same pattern.
Evolution is a highly complex phenomenon, and diversification of species is dependent on various factors and not just one single trait. Therefore, it is necessary to take holistic approach and to combine other factors such as developmental stages, floral mechanics, etc., with the phylogenetic framework to get a detailed answers about floral symmetry.
The authors acknowledge the DST Project Grant (file no. ECR/2017/000563) for financial support during conceptualization and manuscript preparation.
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