At the swing of a pendulum: reversals from monosymmetry to radial symmetry are a frequent phenomenon in angiosperms

by Louis Ronse De Craene
Royal Botanic Garden Edinburgh, Edinburgh EH3 5LR, Scotland, UK.

Monosymmetric flower: Westringia fruticosa (Lamiaceae). Note the 3:2 pattern of the corolla and sequential stamen maturation.

Fig 1. Early monosymmetric flower: Westringia fruticosa (Lamiaceae). Note the 3:2 pattern of the corolla and sequential stamen maturation.

Changes in floral symmetry are an important evolutionary process in flowers. In general four forms of symmetry are recognized in flowers (Endress 1999, Citerne et al. 2010): flowers are either polysymmetric (actinomorphic, with more than one mirror-images if divided in half – very much like slicing a cake), bisymmetric (with two mirror images), or monosymmetric (zygomorphic, with a single mirror image, often called bilateral symmetry: Fig. 1); The final form is asymmetry, which is fairly rare in angiosperms. I also refer to the previous post by Beverley Glover on The mechanisms of symmetry. Monosymmetry is the most frequent flower shape besides polysymmetric flowers. The condition has evolved independently in all major groups of angiosperms, especially in rosids and asterids (Jabbour et al. 2009). Monosymmetry is generally associated with insect (especially bee) pollination, necessitating a landing platform for visitors. Interestingly, genera or even families that are mainly polysymmetric rarely have monosymmetric species, and if they occur, monosymmetry is usually a late-developmental event in the flower (Fig. 2). On the other hand, genera or families that are mainly monosymmetric will have an early onset of monosymmetry in the development, affecting the shape and number of organs being developed (Fig. 1) (Endress 1999, Ronse De Craene 2010). Developmentally, the onset of monosymmetry is regulated by several factors, such as the initiation sequence and subsequent growth of organs, as well as external parameters, such as the orientation of the flower and the opposing pressure of subtending bracts and inflorescence axis (e.g. Endress 1999, Tucker 1999).

Late monosymmetric flower: Iberis sempervirens (Brassicaceae)

Fig. 2. Late monosymmetric flower: Iberis sempervirens (Brassicaceae)

It is clear that monosymmetry evolved at an early stage in some groups of plants and represents a major evolutionary change. What is interesting is that a reversal has frequently arisen from monosymmetry to polysymmetry.
Most Lamiales are monosymmetric, with a constant pattern of three anterior and two posterior petals (Donoghue et al. 1998, Endress 1999, Ronse De Craene 2010). The posterior stamen is generally reduced or lost, and this corresponds typically to the flower of Antirrhinum (Plantaginaceae). Although most Lamiales have monosymmetric flowers, there are several independent derivations of polysymmetry (Soltis et al. 2005).
Reversals to actinomorphic flowers are strongly correlated with the degree of reduction of the posterior side of the flower. In Gesneriaceae the posterior staminode is well developed and reversals to actinomorphic flowers are relatively straightforward, as in Ramonda (Endress 1998; Fig. 3). Actinomorphic flowers in Lamiales are frequently tetramerous (e.g. Plantago, Buddleja).

Fig. 3. Ramonda myconi(Gesneriaceae): the return of a polysymmetric flower in a monosymmetric family

Fig. 3. Ramonda myconi (Gesneriaceae): the return of a polysymmetric flower in a monosymmetric family

A mechanical explanation is linked with a strong polarity between the anterior side and the posterior side of the flower. The posterior side is strongly compressed and this is accompanied by the progressive loss of the staminode and possibly posterior sepal. At the same time the two posterior petals can fuse into a single petal, leading to a tetramerous flower (Endress 1999, Bello et al. 2004).

The mechanical explanation is linked to a genetic cause. As shown for Antirrhinum, monosymmetry is regulated by the antagonistic expression of the TCP transcription factors CYCLOIDEA (CYC) and DICHOTOMA (DICH) against the MYB transcripton factor DIVARICATA (DIV) (Luo et al. 1996). CYC is responsible for the dorsal identity of the corolla and androecium in monosymmetric flowers, while DIV acts on the ventral identity. In a number of case-studies of mutants of Antirrhinum, monosymmetric flowers become polysymmetric either by expansion of DIV at the expense of CYC (Luo et al. 1996), by methylation of CYC, effectively neutralizing its activity (e.g. peloria of Linaria: Cubas et al. 1996), or by expansion of CYC at the expense of DIV, creating fully dorsalized flowers (Luo et al. 1999). This is accompanied by an increase in merism to hexamery. The genetic pathways described for Antirrhinum appear to be conserved in diverse groups of angiosperms outside Lamiales that have been investigated for homologues of CYC (CYCLOIDEA-like genes), with an increased complexity by repeated duplication events (Howarth and Donoghue 2005, Citerne et al. 2010, Preston et al. 2011).
Changes in symmetry can thus be explained in two ways:
-as a loss-of-function event (downgrading of CYC) leading to a reversal to actinomorphy (Luo et al. 1996). Preston et al. (2011) suggested that radially symmetrical flowers of Plantago evolved through loss of CYC-like genes, although they did not explain how tetramery came about;
-as a gain-of-function event (expansion of CYC) leading to actinomorphy (Donoghue et al. 1998). In Gesneriaceae, a reversal to actinomorphy is either an expansion (e.g. Tengia: Peng et al. 2010) or a downgrading of CYC (e.g. Bournea: Zhou et al. 2008). Both processes may result in similar floral morphology.
A similar scenario of dorsal or ventral expansion has been shown to be reproduced in other core eudicots outside Lamiales, such as Lonicera in the Dipsacales (Howarth et al. 2011), or Cadia in Leguminosae (Citerne et al. 2006). Most of these examples relate to families or orders that are highly monosymmetric.

Fig. 4.Bunchosia sp. (Malpighiaceae): example of Neotropical polysymmetric flower. Note the equal paddle-shaped petals. Photo Kyle Dexter

Fig. 4. Neotropical polysymmetric flower: Bunchosia sp. (Malpighiaceae). Note the equal paddle-shaped petals. Photo Kyle Dexter

However, it is interesting to see that a similar process occurs in groups of plants with little or no monosymmetry, emphasizing the universality of CYC expression in the angiosperms. In an interesting paper Zhang et al. (2013) described this for Malpighiaceae, a member of the mainly polysymmetric order Malpighiales. Malpighiaceae is a medium-sized tropical family occurring in the New and Old World. Flowers are typically pentamerous with paddle-shaped petals and are either polysymmetric (Fig. 4) or weakly to strongly monosymmetric (Figs. 5, 6). As monosymmetry is a late-developmental event, all floral organs are present in flowers (even as some may be staminodial) and zygomorphy is often reflected in a small difference in length of one petal (banner*). Zygomorphic flowers tend to be found as a specialization associated with Neotropical bees foraging for oil produced on external glands of the sepals (Figs 5, 6; Vogel 1990).

Fig. 5. Berysonima chrysophylla (Malpighiaceae): example of Neotropical monosymmetric flowers catering for oil-collecting bees. Note the paired glands on the outside of the calyx on the younger flowers at the top. Photo Toby Pennington

Fig. 5. Berysonima chrysophylla (Malpighiaceae): Neotropical monosymmetric flowers catering for oil-collecting bees. Note the paired glands on the outside of the calyx on the younger flowers at the top. Photo Toby Pennington

Zhang et al. (2013) demonstrated that zygomorphy in Malpighiaceae is linked with a duplication of the CYC2 lineage in CYC2A and CYC 2B, which may influence monosymmetry in different degrees (cf. Zhang et al. 2010). Interestingly, with the loss of oil bee specialisations there was a reversal to actinomorphy in four independent cases. Zhang et al. (2013) demonstrated that this reversal was always accompanied by changes in the CYC2 expression. A derived actinomorphy is in some cases accompanied by the expansion the CYC2A expression to the anterior petals, in a similar way as Cadia in Leguminosae (Citerne et al. 2006). In the other cases actinomorphy is attained by loss of CYC2B expression. These results indicate that CYC expression appears to be more widespread in actinomorphic flowers than originally thought.

Fig. 6. Stigmaphyllon sp. (Malpighiaceae): detail of monosymmetric flower with two longer petals. Photo Tiina Sarkinen

Fig. 6. Stigmaphyllon sp. (Malpighiaceae): detail of monosymmetric flower with two longer petals. Photo Tiina Sarkinen

Research of Howarth and Donoghue (2005) and Howarth et al. (2011) suggests that CYC is expressed in all petals of basal Dipsacales, even actinomorphic morphs, such as Viburnum, and that monosymmetry is related to a restriction of CYC to the dorsal side of the flower. Zhang et al. (2013) also suggested that Arabidopsis may not be the best representative for actinomorphic flowers, in that CYC expression has been lost in this model genus (see Busch and Zachgo 2007). As CYC2 is expressed in Elatinaceae, the sister family to Malpighiaceae, it can be assumed that this is also the case for basal Malphighiaceae. However, the reconstruction of the ancestral condition is equivocal and it remains uncertain whether a broad expression of CYC2 or an absence of it is ancestral in the family (Zhang et al. 2013).

In conclusion, evolution of symmetry appears to be an exciting research topic. There is a need to better understand the effects of CYC on other parameters than the petals, such as floral merism, stamen reductions, and the polarization of the shape of the flower. The close correlation between the expression of CYC2 and floral morphology as seen for Malpighiaceae reflects a highly conserved genetic developmental program. However, patterns of change of symmetry are totally unpredictable, as a reflection of the twists of evolution. The pendulum keeps swinging…

*Monosymmetry in Malpighiaceae is not running along a median line, but is oblique, as one of the two posterior petals is longest but becomes displaced along the median line by a torsion of the pedicel (Ronse De Craene 2010). In other cases two petals are longer (Fig. 6).

Thanks to Toby Pennington, Kyle Dexter and Tiina Sarkinen for providing photographs of Malpighiaceae.

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One Response to At the swing of a pendulum: reversals from monosymmetry to radial symmetry are a frequent phenomenon in angiosperms

  1. jeffollerton says:

    Really interesting posting, Louis, thanks. Can I make a point about your title: “reversals from monosymmetry to radial symmetry” implies that radial symmetry is an ancestral condition and monosymmetry is more derived, which is still trotted out as the standard model of angiosperm flower evolution in some text books. However as you acknowledge in your piece, monosymmetry evolved early in the angiosperms and should not necessarily be considered a more derived trait in clades without understanding how that clade has evolved. I think a better title would have been “transitions from monosymmetry to radial symmetry”.



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