Tell me who your sister is and I’ll tell who you are

by Aalt-Jan van Dijk
Wageningen University, The Netherlands

After spending time with family during the Christmas holidays, it became again clear to me how much we learn about ourselves by watching our relatives. This involves both similarities and striking differences. Although at a completely different time-scale, a similar principle holds when analyzing plant species and their genomes: depending on the goal of the analysis, a judicious choice of species to-be-compared-with can be extremely helpful. In particular, it can be very useful to focus on a “sister species”, the closest relative of the group of species of interest. As I’ll describe using two examples, this is of clear relevance for flowering research.

A few months ago, one example of such sister lineage genome analysis was presented with the Tarenaya hassleriana genome (Figure 1; Cheng et al. 2013). Tarenaya hassleriana belongs to the Cleomaceae, which is the phylogenetic sister family to the Brassicaceae, including Arabidopsis thaliana and Brassica crops. One finding of notice in the comparison involved MADS-box transcription factors, which have various roles in flower development. The fate of these flowering regulators after a genome triplication that occurred independently in T. hassleriana and in Brassica, was analyzed. In general, after a genome multiplication many of the new gene copies get lost. However, a striking difference was observed between Brassica and Tarenaya: Brassica retained twice as much floral MADS genes as Tarenaya. Although further analysis clearly would be warranted, morphological diversity in Brassica was speculated to be related with this difference.
More recently, a second example was reported in the final 2013 issue of Science, with the publication of the Amborella trichopoda genome sequence (Amborella Genome Project, 2013). Amborella is a shrub endemic to New Caledonia in the southwest Pacific Ocean. It has previously been indicated that it is the single sister species to all other flowering plants (Figure 2). In addition to analysis of structural aspects of genome evolution (which I will not discuss here), the Amborella genome enabled analysis of how flowering-relevant gene functions developed during flower evolution.

Figure 2. (Left) Amborella trichopoda, sister to all flowering plants. (Right) Simplified land plant phylogeny

Figure 2. (Left) Amborella trichopoda, sister to all flowering plants.(Right) Simplified land plant phylogeny

By comparing the Amborella genome to other available plant genomes, the ancestral gene content at key nodes in land plant phylogeny could be reconstructed. Roughly 25% of 5,210 gene families were specific to flowering plants and not found in non-flowering plants. This suggests that a diverse collection of novel gene functions was likely associated with the origin of flowering plants. Gene Ontology (GO) annotations related to reproduction were indeed overrepresented in this set of gene families. However, GO terms related to homeostasis and related to response to environmental cues, including herbivory, were even stronger enriched in these flowering-specific gene families. The latter was rationalized in the paper by referring to the importance of plant-herbivore coevolution in the diversification of flowering plants. As a side note, it is good to realize that there are many uncertainties associated with GO term analysis, including the fact that for many genes there is no experimental evidence for their function (Kourmpetis et al. 2011; Rhee and Mutwil). The remaining 75% of the 5,210 gene families were found in the common ancestor of all seed-bearing plants, both flowering and non-flowering. This suggested that flowering plants co-opted many pre-existing genes to the business of making flowers. One specific example discussed in the paper is again for the MADS-box genes. The data supports the hypothesis that duplication and diversification of floral MADS-box genes likely occurred before the origin of flowering plants, despite MADS-box genes being tightly associated with the origin of the flower. Apparently, as with us humans, what makes plants unique in comparison even with close relatives is not only which genetic components are present, but also the way in which these components are utilized!

Amborella Genome Project .2013. The Amborella genome and the evolution of flowering plants. Science 342(6165):1241089.

Cheng S, van den Bergh E, Zeng P, Zhong X, Xu J, Liu X, Hofberger J, de Bruijn S, Bhide AS, Kuelahoglu C, et al. 2013. The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers. Plant Cell 25(8):2813-30.

Kourmpetis Y, van Dijk ADJ, van Ham RCHJ, ter Braak CJF. 2011. Genome-wide computational function prediction of Arabidopsis proteins by integration of multiple data sources. Plant Physiol. 155(1):271-81.

Rhee S. and Mutwil M. Towards revealing the functions of all genes in plants. Trends Plant Science. 10.1016/j.tplants.2013.10.006.

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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. l.ronsedecraene@rbge.ac.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.

Bello MA, Rudall PJ, González F, and Fernández-Alonso JL. 2004. Floral morphology and development in Aragoa (Plantaginaceae) and related members of the order Lamiales. International Journal of Plant Science 165: 723-738.

Busch A and Zachgo S. 2007. Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proceedings of the National Academy of Science USA 104, 16714-16719.

Citerne H, Jabbour F, Nadot S, and Damerval C. 2010. The evolution of floral symmetry. In: J.C. Kader and M. Delseny (eds.), Advances in Botanical Research. London: Elsevier, pp. 85-137.

Citerne HL, Pennington RT, and  Cronk QCB. 2006. An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proceedings of the National Academy of Science USA 103: 12017-12020.

Cubas P, Vincent C, and Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.

Donoghue MJ, Ree RH and Baum DA. 1998. Phylogeny and the evolution of flower symmetry in the Asteridae. Trends in Plant Science 3: 311-317.

Endress PK 1998. Antirrhinum and Asteridae – evolutionary changes of floral symmetry. Society for Experimental Biology. Symposium Series 51: 133-140.

Endress PK 1999. Symmetry in flowers. Diversity and evolution. International Journal of Plant Science 160 [6 Suppl]: S3-S23.

Howarth DG and  Donoghue MJ. 2005. Duplications in cyc-like genes from Dipsacales correlate with floral form. International Journal of Plant Science 166: 357-370.

Howarth DG. Martins T, Chimney E, and Donoghue MJ. 2011. Diversification of CYCLOIDEA expression in the evolution of bilateral flower symmetry in Caprifoliaceae and Lonicera (Dipsacales). Annals of Botany 107: 1521-1532.

Jabbour F, Nadot S, Damerval C. 2009. Evolution of floral symmetry: a state of the art. C. R. Biologies 332: 219–231

Luo D, Carpenter R, Vincent C, Copsey L, and Coen E. 1996. Origin of floral asymmetry in Antirrhinum. Nature 383: 794-799.

Luo D, Carpenter R, Copsey L, Vincent C, Clark J, and Coen E. 1999. Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.

Preston JC, Martinez CC, and Hileman LC. 2011. Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome. Proceedings of the National Academy of Science USA 108: 2343-2348.

Ronse De Craene LP. 2010. Floral diagrams. An aid to understanding flower morphology and evolution. Cambridge, Cambridge University Press.

Soltis DE, Soltis PS, Endress PK, and Chase MW. 2005. Phylogeny and evolution of angiosperms. Sinauer, Mass., USA.

Tucker, S. C. 1999. Evolutionary lability of symmetry in early floral development. International Journal of Plant Science 160, 6 Supplement: S25-S39.

Vogel, S. 1990. History of the Malpighiaceae in the light of pollination ecology. Memoirs of the New York Botanical Garden 55: 130-142.

Zhang W, Kramer EM, and C.C. Davis. 2010. Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proceedings of the National Academy of Science USA 107: 6388-6393.

Zhang W, Steinmann VW, Nikolov L, Kramer EM, and Davis CC. 2013. Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors. Frontiers in Plant Science 4: doi: 10.3389/fpls.2013.00302.

Zhou X-R, Wang Y-Z, Smith JF, and Chen R. 2008. Altered expression patterns of TCP and MYB genes relating to the floral developmental transition from initial zygomorphy to actinomorphy in Bournea (Gesneriaceae). New Phytologist 178: 532-543.

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Adaptative walk or random walk?

by Martin Lascoux
Department of Ecology and Genetics, EBC, Uppsala University, Uppsala University, Sweden

The search for the genetic factors controlling phenological traits in Arabidopsis thaliana, in particular flowering time, started in a candid and optimistic mood, with the rapid identification of FRI and FLC as two of the main culprits. Further studies, however, have consistently led to a far more complex picture, with more genes involved and sometimes either FRI, FLC, or both missing. Given what is today known about the genetic basis of complex traits this is perhaps hardly surprising. The new emerging picture is also a consequence of a shift in the type of experiments that are carried out. There are three main differences between recent studies and earlier ones. First, in contrast to early studies that used a single individual per population, recent studies often incorporate local genetic variation. Second, phenology tends today to be measured under more natural conditions. Finally, earlier studies were based on unstructured worldwide samples while more recent studies have considered different geographical scales. In a recent and very interesting study, Brachi and collaborators focus on the latter. Using a hierarchical sampling of French Arabidopsis thaliana populations together with a worldwide sample, they investigated the association of phenology with environmental ecological variables, on the one hand, and variation at 135 SNPs, on the other hand, at different geographical scales. Three main conclusions emerge, none of which is particularly reassuring with regards to our ability to one day reach a generic understanding of the control of phenology in Arabidopsis. First, history matters and it matters a lot: most of phenological variation can simply be explained by neutral genetic variation. It is worth pointing out that, in this respect, A. thaliana might be a particularly difficult species. Other species might not have been disturbed to the same extent. Second, local selective agents such as edaphic conditions or interspecific competition, play an important role in shaping adaptive variation. Third, different genes control phenology in different places and at different geographical scale. I would tend to be a bit more pessimistic than the authors and think that all this would seem to seriously complicate the reconstruction of “the adaptive walks that natural populations follow towards local phenotypic optima”. Hopefully I am wrong and they are right.

Brachi B, Villoutreix R, Faure N, Hautekèete N, Piquot Y, Pauwels M, Roby D, Cuguen J, Bergelson J, Roux F. (2013) Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana. Mol Ecol 22: 4222-4240

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The mechanics of symmetry

by Beverley Glover
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK. bjg26@cam.ac.uk

Flowers come in many different shapes and sizes, but their symmetry is usually described in a binary fashion. Some flowers are bilaterally symmetrical, also known as zygomorphic or monosymmetric (for example, sweet peas). These flowers have a clear top (dorsal side) and bottom (ventral side), and it is only possible to draw a single line of symmetry through them. The alternative state is to be radially symmetrical, also known as actinomorphic or polysymmetric (for example, poppies). It is possible to draw many different lines of symmetry through an actinomorphic flower.

Ophrys speculum has a highly zygomorphic flower, with inner tepals and both whorls of reproductive organs affected

Fig.1. Ophrys speculum has a highly zygomorphic flower, with inner tepals and both whorls of reproductive organs affected

Although we generally think of flowers as having only one of two options when it comes to their symmetry, in fact the overall form of a flower can arise from differential development of organs in one or more whorls of the floral meristem. Many orchids, for example, show extreme bilateral symmetry, with the inner tepals clearly zygomorphic, and the stamens and carpels fused into a single gynostemium, itself often dorsally positioned (Fig 1). The flower of snapdragon (Antirrhinum majus) is the classic genetic model in which zygomorphy has been studied, and its symmetry is based on expansion of the dorsal petals relative to the lateral and ventral ones but abortion of the dorsal stamen (Fig 2).
Fig 2. Antirrhinum majus is the classic genetic model for studies of zygomorphy. The petals and stamens are affected in this species

Fig 2. Antirrhinum majus is the classic genetic model for studies of zygomorphy. The petals and stamens are affected in this species

In contrast the flowers of a number of species of Solanum show zygomorphy only in the stamen whorl, with differential development of anthers to fill feeding or pollinating roles in their interaction with pollen-collecting bees (De Luca and Vallejo-Marin, 2013). These variations in symmetry can be most dramatic in the Asteraceae (the daisy family), where in different species or varieties different combinations of actinomorphic, slightly zygomorphic and strongly zygomorphic florets combine in a condensed inflorescence to produce a flower head (capitulum) that appears fully radially symmetrical (Fig 3; Chapman et al. 2012).
The presence of many subtly different forms of zygomorphy suggests a developmental mechanism that is flexible in both its spatial position within the flower and the strength with which it acts. We have known for over 15 years that the zygomorphy of the Antirrhinum
Fig 3. Daisies, such as this Gorteria diffusa, produce an apparently radially symmetrical capitulum (flower head) by combining central actinomorphic disk florets with an outer ring of highly zygomorphic ray florets

Fig 3. Daisies, such as this Gorteria diffusa, produce an apparently radially symmetrical capitulum (flower head) by combining central actinomorphic disk florets with an outer ring of highly zygomorphic ray florets

flower is dependent on the actions of both dorsalising factors (the partially redundant TCP transcription factors CYCLOIDEA (CYC) and DICHOTOMA (DICH)) and ventralising factors (the MYB transcription factor DIVARICATA (DIV)) (Luo et al. 1996; Almeida et al. 1997). In 2005 Corley et al. used a combination of genetic and molecular approaches to define a further MYB protein, RADIALIS (RAD), as a target of CYC/DICH and the antagonist to the ventralising signals provided by DIV, which is transcribed in all regions of the floral meristem. A model in which RAD and DIV competed to bind promoter regions of downstream ventral-specific genes was the simplest explanation, with DIV outcompeted by RAD in the dorsal parts of the flower as RAD is activated by CYC/DICH in this region.
Recent work by Raimundo et al. (2013) has dissected the molecular interaction between DIV and RAD in more detail, and has shown that the mechanism of symmetry determination is a little more complicated than initially supposed. The authors determined the optimal DNA binding site of the DIV protein, and found that RAD did not bind the same motif. Moreover, RAD did not displace DIV from a DIV-DNA complex, and RAD and DIV proteins did not interact in a yeast 2 hybrid assay. Having effectively disproven the earlier model, the authors then reasoned that RAD and DIV might interact through a third protein. Using RAD as bait in a yeast 2 hybrid screen they identified a pair of novel MYB proteins, which they termed DRIF1 and DRIF2. Tests with DRIF1 showed that it also bound to DIV, and that the DIV-DRIF1-DNA complex was disrupted by the addition of RAD, which competed with DIV not for the DNA but for the DRIF1 protein. Analysis of the subcellular localisation of these proteins revealed that RAD is present in both cytoplasm and nucleus, while DIV is found in the nucleus only. DRIF1 was found to be nuclear localised in the presence of DIV, but cytoplasmically localised in the presence of RAD. In combination these data show that the antagonism between dorsal and ventral activities that occurs when RAD and DIV are both present in the dorsal part of the floral meristem is due to the ability of RAD to sequester the DRIF proteins in the cytoplasm, preventing their interaction with DIV and consequently preventing the DIV protein from activating transcription when bound to DNA.
This mechanism is not unique to floral symmetry. The sequestration of key components of transcriptional complexes in the cytoplasm is a common theme in many aspects of both plant and animal development, including in the processes (such as the floral transition) that occur in response to light signals. It is a system that is both robust and flexible, and has the potential to be adapted to suit a variety of specific requirements. It is perhaps fitting, given that complexity of zygomorphic flowers in their many forms, that the control of floral symmetry operates through a similarly complex molecular interaction.

Almeida J, Rocheta M & Galego L 1997. Genetic control of flower shape in Antirrhinum majus. Development 1244, 1387-1392.
Chapman MA, Tang S, Draeger D, Nambeesan S, Shaffer H, Barb J, Knapp S & Burke J. 2012. Genetic analysis of floral symmetry in Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae. PLoS Genetics 8, (3), e1002628.
Corley S, Carpenter R, Copsey L & Coen E. 2005. Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. PNAS 102, 5068-5073.
De Luca PA & Vallejo-Marín M. 2013. What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16, 429-435.
Luo D, Carpenter R, Vincent C, Copsey L & Coen E. 1996. Origin of floral asymmetry in Antirrhinum. Nature 383, 794-799.
Raimundo J, Sobral R, Bailey P, Azevedo H, Galego L, Almeida J, Coen E & Costa M. 2013. A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in Antirrhinum flower asymmetry. The Plant Journal 75, 527-538.

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Forecasting flowering phenology

Aalt-Jan van Dijk
Plant Research International, Wageningen University

A prominent example of the role computational predictions play in everyday life is that of the weather forecast – will the weather allow your outdoor activities, and how about the weather during holidays? A similar situation is faced by plants in their decision when to start flowering: they should take information from the environment into account, in other words, they should forecast the weather. From a scientific point of view, there is a second layer of “forecasting” related to flowering: how do changes in the climate influence the choices made by plants? On-going interest in assessing the impact of global warming is clear – note that in a couple of days (end of September) the next Intergovernmental Panel on Climate Change (IPCC) Assessment Report is due.
Recently, a novel approach towards forecasting the influence of temperature on flowering was published (Satake et al. 2013). Before discussing this paper, I will briefly describe a bit of context. A popular approach to model the influence of the environment on flowering has been to use information about e.g. average temperatures and/or the number of days with temperature above a certain level, to find thresholds after which flowering would start. In the last few years, molecular and mechanistic aspects have been introduced to such approaches. In one example, mutants impaired in different signalling pathways in Arabidopsis thaliana were grown in field experiments (Wilczek et al. 2009). A variant of the above mentioned modelling approach was used, in which the accumulation of appropriately scaled “photothermal units” describes the progression of plants towards the initiation of reproductive growth. In this variant, individual scaling factors were linked to the activities of specific genes. In this way, each genotype accumulated photothermal units on the basis of day lengths and temperature averages in each experimental planting, modified according to the environmental sensitivity of the line. A second example presented a two-year census of the expression of a temperature-dependent flowering-time gene, AhgFLC, in a natural population of perennial Arabidopsis halleri (Aikawa et al. 2010). This revealed that the regulatory system in which this gene is involved, extracts seasonal cues as if it memorizes temperatures over the past six weeks.

Flowering forecast

Flowering forecast – information about the weather (left-hand arrow) is taken into account in a computational model of a gene regulatory network (bottom panel); this in turn predicts flowering time (right-hand arrow).FLC and FT indicate the two genes modelled by Satake et al.; red arrow indicates repression activity.

Now, a follow-up on this work forecasts flowering phenology under the influence of temperature changes, again for Arabidopsis halleri (Satake et al. 2013). This time, not only the influence of the environment was included, but also a mechanistic model of a gene regulatory network that influences flowering time. The parameters describing the interactions in this network were fitted to data obtained in controlled experiments in the lab. Importantly, this was done separately for different natural populations. The resulting sets of parameters capture differences in how these populations respond to temperature change, as mediated by the gene regulatory network. Subsequently, these models were tested by predicting how these populations would respond to temperature conditions measured in the field, where the models show a convincing ability to predict flowering. One striking so far untested prediction of the model is that it forecasts that under climate warming, the shift in the return time to vegetative growth is greater than that in floral initiation. This would correspond to a significant reduction of the flowering period and ultimately to losing the opportunity to flower at all.
From a computational point of view, it is interesting that the parameters of the gene regulatory network model presented by Satake et al. capture information about responses to the environment, and how these responses differ between natural populations. This extends recent efforts towards modelling flowering time gene regulatory networks, such as (Dong et al. 2012 and Jaeger et al. 2013). Nevertheless, genetic information is not yet explicitly present in the Satake et al. model, in the sense that no connection is made to causal variants in the genome that presumably are present in the different natural populations. Hence, for a novel population of interest, this approach is not directly able to predict its behaviour based on genetic information. I expect that we will see in the near future modelling approaches that use such knowledge on which genetic changes underlie differences between populations. One recent example of an underlying causal variant for Arabidopsis thaliana is given by (Méndez-Vigo et al. 2013) and such information could in principle be incorporated as influencing the parameters in the model. That being said, this work provides an important step towards describing how plants deal with the weather forecast!

Satake A, Kawagoe T, Saburi Y, Chiba Y, Sakurai G, Kudoh H. 2013. Forecasting flowering phenology under climate warming by modelling the regulatory dynamics of flowering-time genes. Nat Commun 4:2303.

Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G, Welch SM, Schmitt J. 2009. Effects of genetic perturbation on seasonal life history plasticity. Science 323(5916):930-4.

Aikawa S, Kobayashi MJ, Satake A, Shimizu KK, Kudoh H. 2010. Robust control of theseasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proceedings of the National Academy of Sciences 107(25):11632-7.

Dong Z, Danilevskaya O, Abadie T, Messina C, Coles N, Cooper M. 2012. A gene regulatory network model for floral transition of the shoot apex in maize and its dynamic modelling. PLoS One 7(8):e43450.

Jaeger KE, Pullen N, Lamzin S, Morris RJ, Wigge PA. 2013. Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis. Plant Cell 25(3):820-33.

[6] Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C. 2013. The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet 9(1):e1003289.

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The scents of summer

Amy L. Parachnowitsch Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com Summer is always a busy time—especially for those who do their research outside. As the chill of the mornings harkens the coming of fall and the fruits of this year’s research are harvested, I find myself sitting at my desk once again and reflecting on what has passed this season. Both my research and my focus have been drawn more and more to the world of floral scent. Many papers have peaked my interest in the last few months and I think it is an exciting time to be studying floral scent. Hopefully we’ll be able to share a few of our own discoveries soon but here’s a brief overview of some of the recent papers on floral scent.

Rafflesia cantleyi (Rafflesiaceae) a parasitic plant with oviposition site mimicry

Rafflesia cantleyi (Rafflesiaceae) a parasitic plant with oviposition site mimicry. Image by Suk-Ling Wee (University Kebangsaan Malaysia)

Most recently, Jurgens et al have published an analysis of oviposition site mimicking flowers. These flowers include carrion, rotting plant and feces mimics, which often have particular structures that can physically resemble the model as well as scents that can boarder on the repulsive to humans. Jürgens et al show that, in general, these oviposition mimics have converged on producing similar scents (mainly sulfur compounds) and these scents are divergent from other pollination systems. The hypothesis that scent is a key trait in oviposition site mimicry is not new. However, the authors were able to show the generality of these patterns by taking a phylogenic approach that included a wide range of species across many plant families. Their work is certainly a step forward in our understanding of this special pollination system. It will be interesting to see whether the general approach could be used to understand scent in other pollination systems as well. Some system specific papers are also pushing our understanding of floral volatiles forward. Friberg et al have found incredible scent diversity in the Lithophragma-Greya moth system. First used as a stepping point to understanding how geography may influence co-evolution, this system looks like it may also provide some clues to the evolution of floral scents. The diversity of scent found throughout the range and among closely related species is truly remarkable. It will be very interesting to see whether there is a functional role and/or evolutionary significance to the variation. Two other papers explore the issue of local adaptation of floral scents in more detail. Breitkopf et al found scent differentiation and pollinator preferences suggesting local adaptation of orchids to contrasting pollinators. However, there was no genetic differentiation to support divergence at genome level. In a contrasting paper, Chartier et al found no local adaptation in scents of two Arum species, despite pollinator differences. When transplanted, both species trapped the local fauna, likely due to the similarity of their scents. And to remind us that not everything is general in pollination biology, a paper by Maia et al describes the scents involved in a scarab beetle-pollinated plant, Taccarum ulei (Araceae). They find two unusual scents make up the majority of the floral volatiles and are attractive to the beetles.

Image by Amy L. Parachnowitsch

Image by Amy L. Parachnowitsch


For those reflecting back before the summer and looking for a broad perspective on floral volatiles, three recent reviews provide a diversity of viewpoints on the subject. Dudareva et al overviews the biosynthesis, function and engineering of floral scent. This is a good summary of floral volatile biosynthesis and function with a focus on agricultural systems. In particular they outline some of the coming challenges of applying knowledge of the function of floral scent to crops. Taking a more evolutionary approach, Schiestl and Johnson discuss the role of pollinators in shaping floral scent evolution in the broader context of floral signals as a whole. They argue that by understanding pollinators we can better understand how flowers have evolved to exploit them. They also provide compelling examples of how considering floral signals from the pollinators view can provide further understanding of floral convergence. To complete the trio, Farré-Armengol et al address the potential conflict of attracting mutualists but deterring antagonists with floral scent. Furthermore, they take a very broad approach and compare olfactory and visual cues, discuss the functions of patterns of scent emission, as well as how global change may effect floral volatiles. All of the reviews point out what we know and where data are lacking. Thus, taken together these three reviews are a good way to assess where the field is and where it might be going. So indeed, it is an exciting time to be studying floral scents. Now, time to reflect on our own system and the results from the summer.

Breitkopf H, Schlüter PM, Xu S, Schiestl FP, Cozzolino S and Scopece G. 2013. Pollinator shifts between Ophrys sphegodes populations: might adaptation to different pollinators drive population divergence? Journal of Evolutionary Biology:n/a-n/a.

Chartier M, Pélozuelo L, Buatois B, Bessière J-M and Gibernau M. 2013. Geographical variations of odour and pollinators, and test for local adaptation by reciprocal transplant of two European Arum species. Functional Ecology DOI: 10.1111/1365-2435.12122

Dudareva N, Klempien A, Muhlemann JK and I Kaplan. 2013. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytologist 198:16-32.

Farré-Armengol G, Filella I, Llusia J and Peñuelas J. 2013. Floral volatile organic compounds: Between attraction and deterrence of visitors under global change. Perspectives in Plant Ecology, Evolution and Systematics 15:56-67.

Friberg M, Schwind C, Raguso RA and Thompson JN. 2013. Extreme divergence in floral scent among woodland star species (Lithophragma spp.) pollinated by floral parasites. Annals of Botany 111:539-550.

Jürgens A, Wee SL, Shuttleworth A and Johnson SD. 2013. Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms. Ecology Letters.

Maia ACD, Gibernau M, Dötterl S, Navarro DM dAF, Seifert K, Müller T and Schlindwein C. 2013. The floral scent of Taccarum ulei (Araceae): Attraction of scarab beetle pollinators to an unusual aliphatic acyloin. Phytochemistry 93:71-78.

Schiestl FP and Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology Evolution 28:307-315.

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Sugar regulates flowering

Soraya Pelaz
Institució Catalana de Recerca i Estudis Avançats (ICREA) and Centre for Research in Agricultural Genomics (CRAG), 08193 Barcelona, Spain. soraya.pelaz@cragenomica.es

It has been said for a long time and repeated as a mantra that plants do not flower even under inductive conditions until they get enough reserves for flowering. Such statement has finally been supported with experimental data. Wahl et al. (2013) have shown how the trehalose-6-phosphate (T6P) pathway controls flowering by regulating the levels of FLOWERING LOCUS T (FT), a known florigen that responds to inductive day-length conditions, and by interacting with the recently described age pathway, regulating the levels of the microRNA156 (miR156). Flowering is controlled by many different genetic pathways that respond to the environment such as light or temperature, and to endogenous conditions like hormone levels or age (Fornara et al. 2010; Wellmer et al. 2010). Now a metabolic pathway has been added to these known genetic pathways. T6P has been proposed to relay information about carbohydrate availability acting as a central hub in carbon signalling (Lunn et al. 2006). Accordingly, null alleles of TREHALOSE PHOSPHATE SYNTHASE 1 (TPS1), encoding the enzyme that catalyzes the formation of T6P, cause embryo lethality (Eastmond et al. 2002). Low expression of TPS1 results in T6P reduction and in a late-flowering phenotype, whereas activation of TPS1 in the shoot apical meristem (SAM) promotes extremely early flowering.

Flowering is induced through the activation of a few genes called floral pathway integrators where all genetic pathways converge; among them FT and SOC1 play central roles (Fornara et al. 2010; Wellmer et al. 2010). Environmental conditions are sensed in the leaves and some mobile signals such as the FT protein or the hormones gibberellins move to the SAM, where flowers are produced, to induce flowering (Bernier 1988; Fornara et al. 2010; Wellmer et al. 2010). Wahl and collaborators (2013) have shown that most of the late flowering phenotype of plants with reduced levels of TPS1 was due to low FT levels, as constitutive expression of FT almost completely suppressed the late flowering of TPS1-downregulated plants. The fact that plants with reduced levels of T6P also flowered late under non inductive day-length conditions prompted the researchers to study other affected pathways. The age pathway has been proposed to function directly at the SAM and to repress precocious flowering. miR156 targets a set of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes, which promote flowering through the activation of the floral pathway integrators. The miR156 is highly expressed early in development and decays as the plant ages, allowing the activation of floral inducers (Yamaguchi et al. 2009; Wang et al. 2009; Wu et al. 2009). This ensures flowering in the event of non inductive environmental conditions. It is still unknown what regulates miR156 expression, but Wahl and collaborators (2013) show that T6P somehow controls miR156 levels as reduction on the biosynthetic T6P enzyme results in an early increase of miR156 levels, although these still gradually declined along development.

Taken together, T6P signalling acts both in leaves and in the SAM and integrates environmental (day length) and physiological (carbohydrate levels) signals together with the age pathway to promote flowering.

References

Bernier G. 1988. The control of floral evocation and morphogenesis. Annual Review of Plant Physiology and Plant Molecular Biology 39:177-219.

Eastmond PJ, Van Dijken AJH, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JDG, Smeekens SC and Graham IA. 2002. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. The Plant Journal 29: 225-235.

Fornara F, de Montaigu A. and Coupland G. 2010. SnapShot: Control of flowering in Arabidopsis. Cell 141, 550: 550 e1-2.

Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible W-R, Carillo P, Hajirezaei M-R and Stitt M. 2006. Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of Storch synthesis in Arabidopsis thaliana. Biochem J. 397: 139-148

Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M and Schmid M. 2013. Regulation of flowering by trehalose-6-phospate signaling in Arabidopsis thaliana. Science 339: 704-707.

Wang J-W, Czech B and Weigel D. 2009. miR156-Regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4): 738-749.

Wellmer F and Riechmann JL. 2010. Gene networks controlling the initiation of flower development. Trends in Genetics 26: 519-27.

Wu G, Park MY, Conway SR, Wang J-W, Weigel D and Poethig RS. 2009. The sequential sction of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750-759.

Yamaguchi A, Wu M-F, Yang L, Wu G, Poethig RS and Wagner D. 2009. The MicroRNA-Regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Developmental Cell 17: 268-278.

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Toxic nectar to improve pollinator fidelity?

Amy L. Parachnowitsch
Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

Maybe because so many of us rely and enjoy caffeine (I’m sipping a large cup of tea as I write this), a recent Science paper on flowers dosing their nectar with caffeine has made quite an impact in popular media. You can find accounts of the paper at New York Times, National Geographic, ScienceNews and pretty much any news source you care to read. The blog world also is a buzz (excuse the pun) with this paper. Everything from science blogs such as Scientific American, Discover, Addiction to food/barista sites (Home-Barista, Foodbeast, Champagnewhisky) are talking about this research.

What makes this particular article so interesting to so many? On the surface, this story touches upon things which people are generally intrigued about: drugs and improving memory. It doesn’t hurt that the drug involved, caffeine, is one people are familiar with and most have directly experienced. There are plenty of good descriptions of this research (including the original article and its summary), and I suggest taking the time to read the full story. In short, Geraldine Wright and coauthors discovered that bees could remember floral cues (scent) better if the reward they received contained caffeine via the caffeine’s action of stimulating the bees’ brain cells. Moreover, plants that produce caffeine in their nectar seem to do this at a level that is active but not so high that bees will reject the nectar because of the bitter taste.

Beyond our interest in drugs and memory, I think what makes these kinds of stories resonate so strongly with non-scientists is that plants are often viewed as static things that we (or other animals) exploit. Rarely do people consider that plants might actually be exploiting us (or other animals), although Mikael Pollan popularized this concept in his best seller The Botany of Desire. Of course, those studying plants have no difficulty seeing that plants do behave, and that evolutionarily, they have been selected to exploit animals in all kinds of ways.

Image courtesy of Geraldine Wright

Bee on citrus flower. Image courtesy of Geraldine Wright

As a pollination biologist and evolutionary ecologist, I’m interested in these findings because the work adds to our understanding of the co-evolutionary interactions between flowers and their pollinators. By improving memory of pollinators these plants may increase pollinator fidelity, suggesting that an important function of ‘toxic nectar’ may be to manipulate pollinators. However, secondary compounds in nectar are common (e.g. toxic nectar), and much work remains to understand the ecological and evolutionary roles of these different components of floral reward. I am excited to see research programmes such as those of this group (and others) proceed because their work hints at the growing trend of approaching floral phenotypes in a holistic way. In this study, caffeine found in the floral nectar enhanced bees memory of floral scent. Thus, to appreciate the role of reward (nectar), secondary compounds found in the reward (caffeine) and scent, it was necessary to study all of these components together. The more we integrate different aspects of floral phenotypes into research programmes, the better we will be able to understand the amazing floral diversity we see.

References

Adler LS. (2000), The ecological significance of toxic nectar. Oikos, 91: 409–420. doi: 10.1034/j.1600-0706.2000.910301.x

Chittka L and Peng F. Caffeine Boosts Bees’ Memories. Sciences. 2013. Vol. 339 no. 6124 pp. 1157-1159. DOI: 10.1126/science.1234411

Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC. Caffeine in Floral Nectar Enhances a Pollinator’s Memory of Reward. Science. 2013. Vol. 339 no. 6124 pp. 1202-1204.

Pollan M. The Botany of Desire (2001). Random House, hardcover: ISBN 0-375-50129-0, 2002 paperback: ISBN 0-375-76039-3

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How flowers excel in their hospitality: the evolution of papillate conical cells in petals is linked with accommodating the right visitors

Louis Ronse De Craene
Royal Botanic Garden Edinburgh, Edinburgh EH3 5LR, Scotland, UK. l.ronsedecraene@rbge.ac.uk

Most flowers rely on animal pollinators for the transfer of their genes. As a result, flowers have developed different strategies to attract and reward pollinators, including variable shapes, specific scent, colour, and nectar production.

Petals are the main visual attractant for floral visitors and have evolved repeatedly in the angiosperms (Ronse De Craene and Brockington 2013). Petals can be generally distinguished from sepals by their bright colour, but also by the development of a specific cell type. These cells, called papillate conical cells, are generally concentrated mainly on the ventral side of the petal. Conical cells have been considered as a distinctive trait for petals that are found in the majority of angiosperms and several authors consider the conical cells as a defining marker for petal identity (Irish 2009).

SEM of conical cells, Solanum. Courtesy of B. Glovers.

SEM image of the ventral petal surface of Solanum sp. (Solanaceae) showing the conical epidermal cells. Courtesy of B. Glovers.

As such they are used as evidence for explaining homeotic conversions between petals and other organs. The petal epidermal micromorphology is increasingly investigated as a marker of petal identity (e.g. Logacheva et al. 2008, Ojeda et al. 2009, Landis et al. 2012).

The genetic basis for conical cells is complex. Conical cells in Antirrhinum and Petunia are regulated by MIXTA and MIXTA-like genes (Noda et al. 1994, Baumann et al. 2007), which have also been linked to hair formation. In petals, MIXTA is expressed when the cells do not divide, and so they differentiate as conical cells. However, in leaves of transgenic plants ectopically expressing MIXTA the cells divide and produce trichomes (Glower et al. 1988). In the bilaterally symmetric flowers of Lotus japonicus (Leguminosae), homologues of CYCLOIDEA are responsible for the differentiation of the dorsal petal and the activation of MIXTA genes linked with the development of papillate conical cells (Feng et al. 2006, Wang et al. 2010). However, in Arabidopsis it is not known which genes are responsible for the conical cell formation (Glover and Martin 2002).

In a recent review Whitney et al. (2011) explained that conical cells are important in changing the optical properties of the petals, as well as their wettability, temperature and the production of scent. The most important attributes, however, are optical and mechanical, in advertising the flower and in providing a foothold for visitors (Kay et al. 1981, Whitney et al. 2009, Alcorn et al. 2012). Bees are known to grasp the petals, especially in vertical bilaterally symmetrical flowers, and this is the main function of the conical cells, next to light absorption. Birds, on the other hand, do not need a foothold, as they can hover in front of the flower (the case of hummingbirds), or visit the flower from a neighbouring perch (most honeycreepers and sunbirds) (Proctor et al. 1996). Thomson and Wilson (2008) reviewed the mechanisms leading to a shift between bee and hummingbird pollination in closely related species, such as Mimulus and Penstemon. However, they did not consider the presence or absence of conical cells. Attributes of bird pollination are different, and one could be the absence of conical cells.

Aphelandra scabra: bird pollinated flower. Courtesy of  L Ronse de Craene

Aphelandra scabra: bird pollinated flower. Courtesy of L Ronse de Craene

Indeed, Ojeda et al. (2012) investigated the presence of conical cells on petals of Macaronesian Lotus (Leguminosae), using established knowledge of the phylogenetic relationships in the genus. They demonstrated that conical cells are lost when flowers shift from bee pollination to bird pollination. While most bee-pollinated Lotus species are characterized by abundant conical cells, especially on the standard petal and to a lesser extent on the wings, bird-pollinated species, such as L. berthelotii have the papillate cells replaced by tabular rugose cells. The authors also found a higher concentration of trichomes on the standard and wing petals and suggested that a shift to bird pollination was accompanied by a shift in petal identity. The known gene expression in Lotus japonicus shows the requirement of LjCYC2 for standard petal development and the differentiation of conical cells, while LjCYC3 appears to regulate the development of wings and tabular rugose cells (Feng et al 2006. 2006, Weng et al. 2011). In bird pollinated Lotus LjCYC3 would have a more expanded expression at the expense of LjCYC2. The driving force in this change must be the pollinator preferences.

The example of Lotus shows the flexibility of flowers to adapt to different pollinators. The transition functions as a means to exclude one kind of visitor to the advantage of another. That conical cells have a major function as providing a foothold for visitors comes from observations in other groups of plants. It is not only the bird pollination syndrome that leads to a loss of conical cells. Case studies in Solanaceae have shown that conical cells are variously present in the genera Solanum and Nicotiana (Glover pers. comm.). An important factor for loss of conical cells besides bird pollination could be a shift to buzz-pollination. The mechanism of buzz-pollination implies that pollen is released from the anthers by the vibration of wings of visiting insects.

Ramonda myconi(Gesneriaceae): buzz-pollinated flower with exposed anthers and reflexed petals. Courtesy of L Ronse de Craene

Ramonda myconi (Gesneriaceae): buzz-pollinated flower with exposed anthers and reflexed petals. Courtesy of L Ronse de Craene

In buzz-pollinated flowers petals are usually reflexed and visitors either hover below the flower or grasp the anthers to shake out the pollen (Proctor et al. 1996). In a broader study of Leguminosae, Ojeda et al. (2009) also found that conical cells are not distributed evenly among different subfamilies. While Faboideae generally have conical cells, these are not always present in Caesalpinoids, and are generally absent in Mimosoids. Flowers of Mimosoids have their flowers grouped in heads and the main attractant are long showy stamens (so-called brush flowers: Ronse De Craene 2010). As a result the smaller petals lack the conical papillate cells.

These observations indicate that conical cells are very specifically correlated with specific pollination systems as suggested by Kay et al. (1981) and that shifts in pollinators could lead to their disappearance. A current project at RBGE is investigating the evolution of conical cells in the Gesneriaceae, a large mainly tropical family that has evolved different modes of pollination. The understanding of the phylogeny of this large family (e.g. Möller et al. 2009) and known pollination mechanisms (e.g. Harisson et al. 1999) is important to postulate evolutionary changes and the drivers for change in the floral morphology.

Flowers have a tremendous ability to adapt to changes in requirements from visitors and – in a striking analogy with the human world – are truly experts in changing the accommodation and shifting the menu on offer to full satisfaction of the customer.

References

Alcorn, K., Whitney, H. and B.J. Glover. 2012. Flower movement increases pollinator preference for flowers with better grip. Functional Ecology 26: 941-947.

Bauman, K., Perez-Rodriguez, M., Bradley, D., Venail, J., Bailey, P., Hailing, J. et al. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701.

Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Ca, Z., Wang, Y. et al. 2006. Control of petal shape and flower zygomorphy in Lotus japonicus. Proceedings of the National Academy of Science USA 103: 4970-4975.

Glover, B.J., and C. Martin. 2002. Evolution of adaptive petal cell morphology. In Q.C.B. Cronk, R.M. Bateman, and J.A. Hawkins, eds., Developmental Genetics and Plant Evolution. Taylor & Francis, London, 160-172.

Glover, B.J., Perez-Rodriguez, M., and C. Martin. 1998. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125: 3497-3508.

Harrison, C.J., Möller, M., and Q.C.B. Cronk. 1999. Evolution and development of floral diversity in Streptocarpus and Saintpaulia. Annals of Botany 84: 49-60.

Irish, V. 2009. Evolution of petal indentity. Journal of Experimental Botany 60: 2517-2527.

Kay, Q.O.N., Daoud, H.S., and C.H. Stirton. 1981. Pigment distribution, light reflection and cell structure in petals. Botanical Journal of the Linnean Society 83: 57-84.

Landis, J.B., Barnett, L.L., and L.C. Hileman. 2012.  Evolution of petaloid sepals independent of shifts in B-class MADS box gene expression. Development Genes and Evolution 222: 19-28.

Logacheva, M.D., Fesenko, I.V., Fesenko A.N., and A.A. Penin. 2008. Genetic and morphological analysis of floral homeotic mutants tepal-like bract and fagopyrum apetala of Fagopyrum esculentum. Botany 86: 367-375.

Möller, M., et al. 2009. A preliminary phylogeny of the ‘Didymocarpoid Gesneriaceae’ based on three molecular datasets: incongruence with available tribal classifications. American Journal of Botany 96: 989-1010.

Noda, K.I., Glover, B.J., Linstead, P., and C. Martin. 1994. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369: 661-664.

Ojeda, I., Francisco-Ortega, J., and Q.C.B. Cronk. 2009. Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Annals of Botany 104: 1099-1110

Ojeda, I. Santos-Guerra, A., Caujapé-Castells, J., Jaén-Molina, R., Marrero, A., and Q.C.B. Cronk. 2012. Comparative micromorphology of petals in macaronesian Lotus (Leguminosae) reveals a loss of papillose conical cells during the evolution of bird pollination. International Journal of Plant Sciences 173: 365-374.

Proctor, M., Yeo, P., and A. Lack. 1996. The Natural History of pollination. Timber Press, Portland, Oregon.

Ronse De Craene, L.P. 2010. Floral diagrams. An aid to understanding flower morphology and evolution. Cambridge, Cambridge University Press.

Ronse De Craene, L.P., and S. Brockington. 2013. Origin and evolution of petals in the angiosperms. Plant Ecology and Evolution 146: in press.

Thomson, J.D., and P. Wilson. 2008. Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. International Journal of Plant science 169: 23-38.

Wang, J. Wang, Y., and D. Luo. 2010. LjCYC gees constitnte floral dorsoventral asymmetry in Lotus japonicus. Journal of Integrative Plant Biology 52: 959-970.

Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., Luo, D., and J. Yang. 2011. Petal development in Lotus japonicus. Journal of Integrative Plant Biology 53: 770-782.

Whitney, H., Chittka, L. Bruce, T., and B.J. Glover. 2009. Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Current Biology 19: 948-953.

Whitney, H.M., Bennett, K.M.V., Dorling, M., Sandbach, L., Prince, D., Chittka, L., and B.J. Glover. 2011. Why do so many petals have conical epidermal cells?  Annals of Botany 10: 609-616.

Thanks to Beverley Glover for helpful suggestions to improve the text.

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Does a petunia of any other name smell as sweet? Unraveling the complexity of floral scents
Amy L. Parachnowitsch

Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

As the perfume industry and anyone who has ever dabbed on scent before a date are keenly aware, smells can help attract mates. Flowers use such volatile blends, which we, in turn, often use in our perfumes, to attract the pollinators that do their mating for them. However, much like other floral characters (Strauss and Whittall 2006), there is a growing appreciation that agents other than pollinators may drive the function and evolution of floral scents.

Diabrotica undecimpunctata on Petunia x hybrida

Diabrotica undecimpunctata on Petunia x hybrida

In Ecology Letters, Kessler et al. (2012) examine the possibility that some components of volatile blends might function to deter herbivores, rather than attract pollinators. The problem many plants may face with advertising floral rewards to pollinators with scent or really any showy trait, is that plants might inadvertently attract herbivores (e.g. Theis and Adler 2011). Thus, floral traits may represent a compromise between attracting mutualistic and antagonistic visitors. The conflict in scent production might be particularly important for night flowering plants that cannot rely on visual cues to attract pollinators. Kessler et al’s study builds on previous work that has shown volatiles can function to reduce herbivory (e.g. Kessler et al. 2008, Junker and Blüthgen 2010, Galen et al. 2011). Here, the authors take advantage of genetically transformed night flowering petunia (Petunia x hybrida) that were gene-silenced at different points in the shikimate and phenylpropaniod scent pathways. Using five different lines, they were able expose plants with different floral scent blends to herbivory and compare their performance. What makes their approach particularly powerful is that the genetically transformed plants were exposed to field conditions to assess the ecological impacts of the blends. Kessler et al. focused on florivore interactions because florivores are particularly likely to be sensitive to floral scents (florivores eat flowers), and are likely to exert selection on floral traits due to their more direct impact on fitness than leaf herbivores (McCall and Irwin 2006).

The authors found three petunia floral scents that were important in plant-florivore interactions. Methyl benzoate, an important attractant of petunia pollinators, was a host location cue for generalist florivores. Therefore, methyl benzoate production is likely under conflicting selection by mutualists and antagonists – a hypothesis that could be tested in wild populations of native petunias. Unfortunately, this study did not examine pollinator behaviour, so it is unknown whether pollinators would also avoid lines with reduced methyl benzoate. For two other compounds, isoeugenol and benzyl benzoate, increased emission acted as feeding deterrents for generalist florivores. In an elegant manipulation, the authors paired field and feeding trial results with a volatile-addition experiment. Adding the feeding deterrents to the volatile headspace of lines that lacked these compounds rescued the deterrent effect on florivores, confirming the function of these volatiles. Again, pollinator response is unknown. However, this set of experiments was able to definitively determine the functional role of these three compounds in generalist florivore interactions. These plants are not native to the habitat where they were tested, it is thus possible that interactions in the native range and for native plants could differ from what was observed here.
Nonetheless, these results suggest that complex floral volatile blends are likely the result of selection by multiple agents and function to both attract pollinators and repel herbivores.

It is an exciting time to be studying floral scents. As analyses of these traits becomes more accessible, we are gaining a more holistic understanding of floral scents and their role in plant-insect interactions (e.g. Schiestl 2010). A complete picture of the role of scent in floral diversity will come from studying floral phenotypes in an integrated fashion as well as studying the multiple agents that exert selection on floral traits. Combining mechanistic studies such as the example discussed here with studies of naturally occurring plant phenotypes (e.g. Galen et al. 2011, Parachnowitsch et al. 2012) will strengthen our understanding of function and evolution of scent in flowers.

References

Galen, C., R. Kaczorowski, S. L. Todd, J. Geib, and R. A. Raguso. 2011. Dosage dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. American Naturalist 177:258-272.

Junker, R. R. and N. Blüthgen. 2010. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany 105:777-782.

Kessler, D., C. Diezel, D. G. Clark, T. A. Colquhoun, and I. T. Baldwin. 2012. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecology Letters.

Kessler, D., K. Gase, and I. T. Baldwin. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200-1202.

McCall, A. C. and R. E. Irwin. 2006. Florivory: The intersection of pollination and herbivory. Ecology Letters 9:1351-1365.

Parachnowitsch, A. L., R. A. Raguso, and A. Kessler. 2012. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytologist 195:667-675.

Schiestl, F. P. 2010. The evolution of floral scent and insect chemical communication. Ecology Letters 13:643-656.

Strauss, S. Y. and J. B. Whittall. 2006. Non-pollinator agents of selection on floral traits. In: LD Harder and SC H. Barrett, editors. Ecology and Evolution of Flowers. Oxford University Press, Oxford, UK. pp. 120–138.

Theis, N. and L. S. Adler. 2011. Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93:430-435.

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