Review
Tansley insight Symmetry matters Author for correspondence: Lars Østergaard Tel: +44 1603 450572 Email: [email protected]
Laila Moubayidin and Lars Østergaard Department of Crop Genetics, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK
Received: 14 February 2015 Accepted: 26 March 2015
Contents Summary
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I.
Introduction
II. III.
Conclusions
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Acknowledgements
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Bilateral and radial symmetries
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References
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Symmetry breaking
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IV. Symmetry transitions
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Summary New Phytologist (2015) 207: 985–990 doi: 10.1111/nph.13526
Key words: Arabidopsis gynoecium, bilateral symmetry, plant development, radial symmetry, symmetry breaking, symmetry transition.
The development of multicellular organisms depends on correct establishment of symmetry both at the whole-body scale and within individual tissues and organs. Setting up planes of symmetry must rely on communication between cells that are located at a distance from each other within the organism, presumably via mobile morphogenic signals. Although symmetry in nature has fascinated scientists for centuries, it is only now that molecular data to unravel mechanisms of symmetry establishment are beginning to emerge. As an example we describe the genetic and hormonal interactions leading to an unusual bilateral-to-radial symmetry transition of an organ in order to promote reproduction.
I. Introduction The word ‘symmetry’ was coined in Greece to describe the harmonic arrangement of parts that have same measures and proportions. It is therefore no surprise that such a geometric feature has been extensively used in scientific disciplines, such as mathematics, chemistry and biology, as well as in arts and architecture, through human history since then. In addition to being extensively associated with beauty and harmony, symmetry is a functional necessity in biology as it also provides fitness advantages to organisms. For example, a symmetric wingspan is a prerequisite for birds to fly, and humans would find it hard not to be walking in circles if one leg was shorter than the other. On a smaller scale, various types of symmetry can also be observed at the level of single organs and cells, promoting their functions and determining developmental advantages. The number of duplicated body parts or shapes that make an organism/organ symmetric determine the type of symmetry the body has got, for example, bilateral or radial symmetry (Fig. 1a,b). Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
However, symmetry type is not always fixed for life: it can be either broken or changed from one type to another through an organism’s lifespan (Fig. 1c,d) (Lowe & Wray, 1997; Palmer, 2004; Li & Bowerman, 2010; Moubayidin & Østergaard, 2014). The latter can be the case when an apex of a primordium changes its symmetry through development, resulting in different symmetries from base to tip. Transitions where a whole radially symmetric individual is converted into a bilaterally symmetric one are relatively common, for example, during embryogenesis of both animals and plants (Lau et al., 2012; Campos-Ortega & Hartenstein, 2013), whereas transitions from bilateral to radial symmetry are more rarely observed. The Arabidopsis thaliana female reproductive organ, the gynoecium, is so far the only molecularly documented example of a developing structure that reprograms its development over time to achieve a bilateral-to-radial symmetry transition (Fig. 2a,b) (Moubayidin & Østergaard, 2014). In this review we provide examples of symmetries found in nature within organisms, organs and cells, as well as examples of symmetry breaking and transitions. New Phytologist (2015) 207: 985–990 985 www.newphytologist.com
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(a) Bilateral symmetry
(b) Radial symmetry
(c) Symmetry breaking
(d) Symmetry transition
Fig. 1 Shadow representations of symmetry formation found in nature. (a) Butterfly with bilateral symmetry along the body axis, and (b) star fish with five-fold radial symmetry. Axes of symmetry in (a) and (b) are indicated by pink lines. The image in (c) shows a male fiddler crab with differentiallysized claws (brown) as an example of symmetry breaking, whereas the style (brown) of the Arabidopsis gynoecium (d) undergoes a transition in symmetry.
II. Bilateral and radial symmetries In bilateral symmetry only a single plane divides the organism into two identically reflected halves (reflective symmetry) (Fig. 1a), whereas a radially symmetric structure can be halved at multiple planes to produce identical parts (n-fold rotational symmetry) (Fig. 1b). Radially symmetric bodies can occur from three-fold up to ∞-fold radial symmetry (axial symmetry), as in the case of a completely spherical organism. Examples of bilateral symmetric organisms are found among the majority of animals on earth, such as humans, butterflies and sharks, because this type of symmetry is particularly suitable for actively moving organisms. Moreover, from an evolutionary point of view, bilaterality has favoured the cephalisation process by grouping sense organs and main nerve centres at one end of the body, and therefore leading to the establishment of the antero-posterior body axes (Lowe et al., 2006; Ferrier, 2012; Duttke et al., 2014). However, radial symmetry is seen in sessile organisms such as sea anemone, floating organisms such as jellyfish, and slow-moving organisms such as sea stars (McClay, 2011; Technau & Steele, 2011). The equal distribution of body parts and sense organs make them better able to react to environmental stimuli coming from all around their bodies. As shapes of organs and cells are strictly connected to their activities and functions, symmetry is an important matter also at those scales. The dorso-ventrally flattened leaves of most angiosperms (flowering plants) usually have approximately bilateral symmetry, that is, their left and right sides mirror each other along a central axes (Chitwood et al., 2012; Kalve et al., 2014) (Fig. 2a,c). Their main function is to absorb light in order to fix carbon via photosynthesis New Phytologist (2015) 207: 985–990 www.newphytologist.com
and, in the process, to release oxygen and water vapour into the environment. However, in extremely hot environments, a change in organ symmetry has been adopted by some flowering plants, such as Senecio rowleyanus, whose leaves are small and rounded like peas, in order to minimise water loss. An example that links symmetry type to cellular activities is given by the male and female reproductive cells, which generally adopt bilateral and radial symmetry, respectively. Indeed, the animal spermatozoon has a head and a tail and actively moves to reach and fertilize the big, round nonactively moving female egg cell. Examples such as these highlight the importance of patterning genes that impose the establishment and maintenance of the symmetry characteristic of an organism, an organ or a cell, in order to maximise fitness. Indeed, several examples in the literature describe mutations in plant genes that lead to radialisation of bilaterally symmetric organs, such as flowers and leaves (Luo et al., 1996; Cubas et al., 1999; Kerstetter et al., 2001). A single epigenetic mutation in both Antirrhinum majus and Linaria vulgaris has been implicated in the transformation of their bilaterally symmetric flowers into five-fold symmetric ones, thus leading to a radially symmetric peloric organ (Luo et al., 1996; Cubas et al., 1999). In Arabidopsis, leaf polarity, and thus bilateral symmetry, is guaranteed by the expression of key identity factors in the upper (adaxial) and under (abaxial) sides of the leaf, and their reciprocal inhibitions (Fig. 2c). Class III homeodomain-leucine zipper (HD-ZIPIII) proteins PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV), are expressed (and constrained) in the adaxial domain where they inhibit (and are constrained by) the abaxial fate factors belonging to the KANADI and YABBY families (Siegfried et al., 1999; Eshed et al., 2001, 2004; Kerstetter et al., 2001) (Fig. 2c). Indeed, gain-of-function mutants of the PHB, PHV and REV genes show rod-like or trumpet-shaped leaves, thus interfering with bilateral symmetry (McConnell et al., 2001; Emery et al., 2003). It is noteworthy that one symmetry-breaking event based on constrained HD-ZIP III expression may influence symmetry along three axes (Grigg et al., 2009). Within this molecular framework, the leaf-margin identity gene WUS-RELATED HOMEOBOX1 (WOX1) titrates the balance between the abaxial and adaxial fates, by repressing both identity gene types (Nakata et al., 2012; Kalve et al., 2014) (Fig. 2c). This setup is strongly reminiscent of the genetic interaction that has been unveiled to control the medio-lateral development of the Arabidopsis ovary. In this developmental context, the reciprocal inhibition of genes such as FRUITFULL, REPLUMLESS and INDEHISCENT, necessary for valve, replum and valve margin identity, respectively, controls ovary development (Liljegren et al., 2004; Girin et al., 2010). On the other hand, the radial symmetry of the Arabidopsis root apical meristem can become bilateral by affecting cell cycle progression; mutations in the tonsoku gene provide an example of a split root-tip phenotype where twin root tips, that are mirror images of each other, form at the distal end of the meristem (Fig. 2a, d) (Suzuki et al., 2004, 2005). In the aerial part of the plant, several examples of split-style phenotypes are observed when genes important for the development of the radial distal tip of the female reproductive structure are Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
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(a)
(b)
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PAT
PAT
PAT
SPT–IND
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Lateral
PHV–PHB–REV Bilateral symmetry
WOX1 Adaxial
KAN–YAB
Medial
Abaxial Proximal
Distal
(d) Outer
TSK
Inner
Cell division
Radial symmetry
Fig. 2 Symmetry establishment during plant development. (a) Five-week old Arabidopsis thaliana (Col-0) plant. White frames indicate (starting from the top) flowers, leaf and root tip, respectively, with developmental and molecular details provided in panels (b–d). (b) Transition from bilateral to radial symmetry at the gynoecium apex through control of auxin distribution mediated by inhibition of polar auxin transport (PAT) by SPT/IND bHLH transcription factors via repression of PID expression. Auxin signalling maxima are depicted in red. Sections from style and ovary of a mature gynoecium are depicted to show radial and bilateral symmetries, respectively. Apical-basal and medio-lateral orientations are indicated. (c) Bilateral symmetry in the leaf (inset) is controlled by interactions among adaxial (PHV, PHB, REV) and abaxial (KAN, YAB) identity factors and factors at the adaxial–abaxial interface such as WOX1. The leaf has been depicted partially folded to allow visualization of the abaxial side (in dark green). Proximal-distal, medio-lateral and adaxial–abaxial orientations are indicated. (d) Radial symmetry in the root stem cell niche is ensured by cell arrangements organised by the LRR protein TSK. Cells in the quiescent centre are shown in purple. Outer–inner orientation is indicated. SPT is SPATULA, IND is INDEHISCENT, PID is PINOID, PHV is PHAVOLUTA, PHB is PHABULOSA, REV is REVOLUTA, KAN is KANADI, YAB is YABBY, WOX1 is WUSCHEL-RELATED HOMEOBOX1 and TSK is TONSOKU.
mutated, such as STYLISH1 (STY1) and STY2, ETTIN, CRABS CLAW and TOUSLED kinase (Roeder & Yanofsky, 2006). These examples suggest that obtaining radial or bilateral symmetries from the reciprocal status is not necessarily a complicated process. However, strong selective pressure may be in place to prevent it, when there are obvious advantages to do so, such as in maintaining a fertile reproductive organ, a flat and photosynthetically efficient leaf or a directionally growing root.
III. Symmetry breaking Symmetry breaking of a bilaterally symmetric organism is the process by which the right and left halves lose their sameness. The most familiar examples are some species of flat fish, such as the sole Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
that has both eyes located on the same side of the head, and the male fiddler crab that has a big size difference between their claws (Fig. 1c). Symmetry breaking can be observed also at a cellular level, that is, in asymmetric cell divisions or when cellular compounds are polarly distributed to one side of the cell, thus driving cell and tissue specification and polarity as well as organ morphogenesis (Wennekamp et al., 2013; van den Brink et al., 2014; Kajala et al., 2014). For example in plants, asymmetric cell divisions are a common mechanism generating different cell types and tissues from a common progenitor cell (Kajala et al., 2014). Furthermore, the cellular asymmetric distribution of phytohormone transporters can direct the flux of hormones, thereby orchestrating plant development. In Arabidopsis the hormone auxin acts as a morphogen through careful modulation of its New Phytologist (2015) 207: 985–990 www.newphytologist.com
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biosynthesis, transport and cellular response (Benjamins & Scheres, 2008). In particular, it has been shown that transportdependent auxin distribution, via PIN auxin efflux carriers, connects cell polarity and patterning processes in Arabidopsis. The subcellular localisation of PIN proteins determines the direction of intercellular auxin transport, thereby connecting polarity of individual cells of the whole tissues or organs (Benjamins & Scheres, 2008; Abley et al., 2013). PIN proteins continuously cycle between the plasma membrane and endosomes. The sorting of PIN proteins into apical or basal trafficking pathways depends on the phosphorylation status of PINs, which is controlled by the PID protein kinase and PP2A phosphatases (Friml et al., 2004; Benjamins & Scheres, 2008). Interestingly, the asymmetric distribution of the PIN proteins, and therefore the directional flux of auxin, is absolutely required to establish and maintain the bilateral symmetry of an organ, such as in the case of the Arabidopsis ovary where the cellular symmetry breaking of polar PIN localisation promotes bilaterality of the organ. Indeed, interfering with PIN polarity, as in the pid mutant, leads to a break of symmetry in the ovary (Moubayidin & Østergaard, 2014).
IV. Symmetry transitions Symmetry transitions are common in the development of vertebrates, invertebrates and plants, particularly during embryogenesis. In most cases the transition is from radial to bilateral symmetry and controlled by homeotic (Hox) genes and decapentaplegic (dpp) morphogen in animals (Holley et al., 1995; Collins & Valentine, 2001). In Arabidopsis, a radially symmetric embryo structure turns into a bilateral heart-shaped form due to the activity of master gene regulators of the root and shoot apical meristems, as well as auxin dynamics. An example is given by the activity of CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 putative transcription factors and the PIN1 auxin efflux carrier that are necessary for promoting the separation of the two embryonic leaves, the cotyledons. Indeed, the cuc1 cuc2 pin1 triple mutant embryo exhibits a perfectly radial fusion of cotyledons and vascular bundles radially distributed, thus impairing the naturally occurring transition from radial-to-bilateral symmetry (Aida et al., 2002). By contrast, echinoderm embryogenesis involves a transition from bilaterally symmetric larvae to a radial adult animal. During the late larvae stage, discrete populations of tissues on the left side of the body proliferate to form the imaginal adult rudiment, where the first radially symmetric structure appears. During metamorphosis, many larval tissues are lost, and the rudiment gives rise to the major parts of the juvenile animal (Lowe & Wray, 1997). Although these are examples of conversion of an entire structure from one type of symmetry to another, a different kind of symmetry transition can be observed when the apex of a primordium changes its symmetry and thus the primordium continues its growth with a different symmetry. The Arabidopsis gynoecium, is so far the only molecularly documented example of a developing structure that exhibits different symmetries from its base to its tip (Moubayidin & Østergaard, 2014). The gynoecium is derived from the fusion of two carpels and forms in the centre of the flower as a ridge of raised cells around a central cleft (Roeder & Yanofsky, 2006). The main New Phytologist (2015) 207: 985–990 www.newphytologist.com
New Phytologist patterning events of the gynoecium take place before fertilisation and occur along three axes: apical-basal, medio-lateral and abaxial– adaxial (equivalent to dorso-ventrality in animals) (Fig. 2b). At a particular stage of gynoecium development, the distal part becomes topped with stigmatic papillae. The stigmatic tissue functions to attract pollen and mediate pollen germination. It also marks the beginning of the pollen-guiding transmitting tract, which runs down the centre of the ovary allowing fertilisation. A solid style with radial symmetry supports the next segment of the transmitting tract and is required for efficient fertilisation. Below the style, the ovary is formed as a longitudinal cylinder with medio-lateral symmetry that reflects the origin of the gynoecium as two fused leaves. The ovary is composed of two compartments divided by the septum and placenta from which the ovules arise (Roeder & Yanofsky, 2006). We have recently unveiled the biological mechanism that underpins this rare switch from bilateral to radial symmetry occurring at the style region during gynoecium development. We first verified that the bilateral symmetry is the default state during the first gynoecium growth phase, and that two basic helix-loop-helix (bHLH) transcription factors SPATULA (SPT) and INDEHISCENT (IND) are necessary to repress the activity of margin identity genes in order to obtain radiality specifically at the distal part. Coherently, loss-of-function mutations in the SPT and IND genes lead to a failure in radial symmetry establishment at the style region. Remarkably, the misexpression of those genes in a bilateral leaf was sufficient to impose a change to radial symmetry, demonstrating that IND and SPT are necessary and sufficient for mediating organ radialisation. It was previously shown that SPT and IND regulate the transport of auxin in the context of fruit opening by directly repressing PID expression, thus controlling the plasma membrane localisation of PINs and therefore the auxin flux (Sorefan et al., 2009; Girin et al., 2011). At the gynoecium apex auxin distribution is tightly controlled in both time and space. In particular we noticed that auxin distribution precedes and mimics the bilateral-to-radial transition occurring at the gynoecium apex, because it is bilaterally distributed in two lateral foci in the very young gynoecium, while subsequently forming a ring of radial symmetry by passing through a four-foci stage (Fig. 2b). The bilaterally symmetric lateral foci are established due to the polar distribution of PINs in the ovary that drives auxin from the bottom to the top of the organ. These lateral foci guarantee coordinated growth of the two halves along the apical–basal axis. Subsequently, the establishment of the medial foci at the four-foci stage is controlled by the downregulation of PID by SPT and IND, allowing PINs to localise in a nonpolar manner in the cells of the apex, thus generating the auxin ring (Moubayidin & Østergaard, 2014) (Fig. 2b). It is still unclear how the four auxin foci can communicate at a distance and how the polarity of cells at the gynoecium apex is reprogrammed. However, our study showed that the activity of the lateral auxin foci bilaterally distributed function upstream from the activity of the medial foci, which are established later in development. This suggests that a sink and a source of cell polarity are required in order to commit to a symmetry transition. Mathematical and computational predictions may be a powerful tool in the understanding of how this auxin spatio-temporal dynamic is Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
New Phytologist achieved and how it drives the radiality process. The sequentially occurring auxin foci may act as tissue polarity organisers coordinating and coupling cell-to-cell (Abley et al., 2013; Grieneisen et al., 2013).
V. Conclusions Controlling symmetry is an integral part of the development of multicellular organisms. Here we have described that a symmetry transition in the Arabidopsis gynoecium is determined by distribution of a molecule with morphogenic characteristics, auxin. To what extent morphogens control symmetry establishment in plants and animals remains to be established. However, given that communication between cells must be an essential part in coordinating symmetry formation, it is likely that mobile signals as provided by morphogens play prominent roles. Unravelling how short- and long-distance signals function in establishing symmetry in both whole organisms and in individual organs will undoubtedly be a complex task. We therefore predict that efforts to combine experimental biology with mathematical approaches will become increasingly important, thus continuing a millennium-long tradition of mathematicians’ fascination of symmetry in biological structures.
Acknowledgements We thank Mr Andrew Davis for photographic assistance and Drs Veronica Grieneisen and Raffaele Dello Ioio for constructive comments on the manuscript. This work was supported by grant BB/K008617/1 to L.Ø. from the Biotechnological and Biological Sciences Research Council and by the Institute Strategic Programme grant (BB/J004553/1) to the John Innes Centre.
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Tansley insight Symmetry matters Author for correspondence: Lars Østergaard Tel: +44 1603 450572 Email: [email protected]
Laila Moubayidin and Lars Østergaard Department of Crop Genetics, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK
Received: 14 February 2015 Accepted: 26 March 2015
Contents Summary
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Introduction
II. III.
Conclusions
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Acknowledgements
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Bilateral and radial symmetries
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Symmetry breaking
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IV. Symmetry transitions
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Summary New Phytologist (2015) 207: 985–990 doi: 10.1111/nph.13526
Key words: Arabidopsis gynoecium, bilateral symmetry, plant development, radial symmetry, symmetry breaking, symmetry transition.
The development of multicellular organisms depends on correct establishment of symmetry both at the whole-body scale and within individual tissues and organs. Setting up planes of symmetry must rely on communication between cells that are located at a distance from each other within the organism, presumably via mobile morphogenic signals. Although symmetry in nature has fascinated scientists for centuries, it is only now that molecular data to unravel mechanisms of symmetry establishment are beginning to emerge. As an example we describe the genetic and hormonal interactions leading to an unusual bilateral-to-radial symmetry transition of an organ in order to promote reproduction.
I. Introduction The word ‘symmetry’ was coined in Greece to describe the harmonic arrangement of parts that have same measures and proportions. It is therefore no surprise that such a geometric feature has been extensively used in scientific disciplines, such as mathematics, chemistry and biology, as well as in arts and architecture, through human history since then. In addition to being extensively associated with beauty and harmony, symmetry is a functional necessity in biology as it also provides fitness advantages to organisms. For example, a symmetric wingspan is a prerequisite for birds to fly, and humans would find it hard not to be walking in circles if one leg was shorter than the other. On a smaller scale, various types of symmetry can also be observed at the level of single organs and cells, promoting their functions and determining developmental advantages. The number of duplicated body parts or shapes that make an organism/organ symmetric determine the type of symmetry the body has got, for example, bilateral or radial symmetry (Fig. 1a,b). Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
However, symmetry type is not always fixed for life: it can be either broken or changed from one type to another through an organism’s lifespan (Fig. 1c,d) (Lowe & Wray, 1997; Palmer, 2004; Li & Bowerman, 2010; Moubayidin & Østergaard, 2014). The latter can be the case when an apex of a primordium changes its symmetry through development, resulting in different symmetries from base to tip. Transitions where a whole radially symmetric individual is converted into a bilaterally symmetric one are relatively common, for example, during embryogenesis of both animals and plants (Lau et al., 2012; Campos-Ortega & Hartenstein, 2013), whereas transitions from bilateral to radial symmetry are more rarely observed. The Arabidopsis thaliana female reproductive organ, the gynoecium, is so far the only molecularly documented example of a developing structure that reprograms its development over time to achieve a bilateral-to-radial symmetry transition (Fig. 2a,b) (Moubayidin & Østergaard, 2014). In this review we provide examples of symmetries found in nature within organisms, organs and cells, as well as examples of symmetry breaking and transitions. New Phytologist (2015) 207: 985–990 985 www.newphytologist.com
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(a) Bilateral symmetry
(b) Radial symmetry
(c) Symmetry breaking
(d) Symmetry transition
Fig. 1 Shadow representations of symmetry formation found in nature. (a) Butterfly with bilateral symmetry along the body axis, and (b) star fish with five-fold radial symmetry. Axes of symmetry in (a) and (b) are indicated by pink lines. The image in (c) shows a male fiddler crab with differentiallysized claws (brown) as an example of symmetry breaking, whereas the style (brown) of the Arabidopsis gynoecium (d) undergoes a transition in symmetry.
II. Bilateral and radial symmetries In bilateral symmetry only a single plane divides the organism into two identically reflected halves (reflective symmetry) (Fig. 1a), whereas a radially symmetric structure can be halved at multiple planes to produce identical parts (n-fold rotational symmetry) (Fig. 1b). Radially symmetric bodies can occur from three-fold up to ∞-fold radial symmetry (axial symmetry), as in the case of a completely spherical organism. Examples of bilateral symmetric organisms are found among the majority of animals on earth, such as humans, butterflies and sharks, because this type of symmetry is particularly suitable for actively moving organisms. Moreover, from an evolutionary point of view, bilaterality has favoured the cephalisation process by grouping sense organs and main nerve centres at one end of the body, and therefore leading to the establishment of the antero-posterior body axes (Lowe et al., 2006; Ferrier, 2012; Duttke et al., 2014). However, radial symmetry is seen in sessile organisms such as sea anemone, floating organisms such as jellyfish, and slow-moving organisms such as sea stars (McClay, 2011; Technau & Steele, 2011). The equal distribution of body parts and sense organs make them better able to react to environmental stimuli coming from all around their bodies. As shapes of organs and cells are strictly connected to their activities and functions, symmetry is an important matter also at those scales. The dorso-ventrally flattened leaves of most angiosperms (flowering plants) usually have approximately bilateral symmetry, that is, their left and right sides mirror each other along a central axes (Chitwood et al., 2012; Kalve et al., 2014) (Fig. 2a,c). Their main function is to absorb light in order to fix carbon via photosynthesis New Phytologist (2015) 207: 985–990 www.newphytologist.com
and, in the process, to release oxygen and water vapour into the environment. However, in extremely hot environments, a change in organ symmetry has been adopted by some flowering plants, such as Senecio rowleyanus, whose leaves are small and rounded like peas, in order to minimise water loss. An example that links symmetry type to cellular activities is given by the male and female reproductive cells, which generally adopt bilateral and radial symmetry, respectively. Indeed, the animal spermatozoon has a head and a tail and actively moves to reach and fertilize the big, round nonactively moving female egg cell. Examples such as these highlight the importance of patterning genes that impose the establishment and maintenance of the symmetry characteristic of an organism, an organ or a cell, in order to maximise fitness. Indeed, several examples in the literature describe mutations in plant genes that lead to radialisation of bilaterally symmetric organs, such as flowers and leaves (Luo et al., 1996; Cubas et al., 1999; Kerstetter et al., 2001). A single epigenetic mutation in both Antirrhinum majus and Linaria vulgaris has been implicated in the transformation of their bilaterally symmetric flowers into five-fold symmetric ones, thus leading to a radially symmetric peloric organ (Luo et al., 1996; Cubas et al., 1999). In Arabidopsis, leaf polarity, and thus bilateral symmetry, is guaranteed by the expression of key identity factors in the upper (adaxial) and under (abaxial) sides of the leaf, and their reciprocal inhibitions (Fig. 2c). Class III homeodomain-leucine zipper (HD-ZIPIII) proteins PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV), are expressed (and constrained) in the adaxial domain where they inhibit (and are constrained by) the abaxial fate factors belonging to the KANADI and YABBY families (Siegfried et al., 1999; Eshed et al., 2001, 2004; Kerstetter et al., 2001) (Fig. 2c). Indeed, gain-of-function mutants of the PHB, PHV and REV genes show rod-like or trumpet-shaped leaves, thus interfering with bilateral symmetry (McConnell et al., 2001; Emery et al., 2003). It is noteworthy that one symmetry-breaking event based on constrained HD-ZIP III expression may influence symmetry along three axes (Grigg et al., 2009). Within this molecular framework, the leaf-margin identity gene WUS-RELATED HOMEOBOX1 (WOX1) titrates the balance between the abaxial and adaxial fates, by repressing both identity gene types (Nakata et al., 2012; Kalve et al., 2014) (Fig. 2c). This setup is strongly reminiscent of the genetic interaction that has been unveiled to control the medio-lateral development of the Arabidopsis ovary. In this developmental context, the reciprocal inhibition of genes such as FRUITFULL, REPLUMLESS and INDEHISCENT, necessary for valve, replum and valve margin identity, respectively, controls ovary development (Liljegren et al., 2004; Girin et al., 2010). On the other hand, the radial symmetry of the Arabidopsis root apical meristem can become bilateral by affecting cell cycle progression; mutations in the tonsoku gene provide an example of a split root-tip phenotype where twin root tips, that are mirror images of each other, form at the distal end of the meristem (Fig. 2a, d) (Suzuki et al., 2004, 2005). In the aerial part of the plant, several examples of split-style phenotypes are observed when genes important for the development of the radial distal tip of the female reproductive structure are Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
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(a)
(b)
Radial symmetry transition PID
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Fig. 2 Symmetry establishment during plant development. (a) Five-week old Arabidopsis thaliana (Col-0) plant. White frames indicate (starting from the top) flowers, leaf and root tip, respectively, with developmental and molecular details provided in panels (b–d). (b) Transition from bilateral to radial symmetry at the gynoecium apex through control of auxin distribution mediated by inhibition of polar auxin transport (PAT) by SPT/IND bHLH transcription factors via repression of PID expression. Auxin signalling maxima are depicted in red. Sections from style and ovary of a mature gynoecium are depicted to show radial and bilateral symmetries, respectively. Apical-basal and medio-lateral orientations are indicated. (c) Bilateral symmetry in the leaf (inset) is controlled by interactions among adaxial (PHV, PHB, REV) and abaxial (KAN, YAB) identity factors and factors at the adaxial–abaxial interface such as WOX1. The leaf has been depicted partially folded to allow visualization of the abaxial side (in dark green). Proximal-distal, medio-lateral and adaxial–abaxial orientations are indicated. (d) Radial symmetry in the root stem cell niche is ensured by cell arrangements organised by the LRR protein TSK. Cells in the quiescent centre are shown in purple. Outer–inner orientation is indicated. SPT is SPATULA, IND is INDEHISCENT, PID is PINOID, PHV is PHAVOLUTA, PHB is PHABULOSA, REV is REVOLUTA, KAN is KANADI, YAB is YABBY, WOX1 is WUSCHEL-RELATED HOMEOBOX1 and TSK is TONSOKU.
mutated, such as STYLISH1 (STY1) and STY2, ETTIN, CRABS CLAW and TOUSLED kinase (Roeder & Yanofsky, 2006). These examples suggest that obtaining radial or bilateral symmetries from the reciprocal status is not necessarily a complicated process. However, strong selective pressure may be in place to prevent it, when there are obvious advantages to do so, such as in maintaining a fertile reproductive organ, a flat and photosynthetically efficient leaf or a directionally growing root.
III. Symmetry breaking Symmetry breaking of a bilaterally symmetric organism is the process by which the right and left halves lose their sameness. The most familiar examples are some species of flat fish, such as the sole Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
that has both eyes located on the same side of the head, and the male fiddler crab that has a big size difference between their claws (Fig. 1c). Symmetry breaking can be observed also at a cellular level, that is, in asymmetric cell divisions or when cellular compounds are polarly distributed to one side of the cell, thus driving cell and tissue specification and polarity as well as organ morphogenesis (Wennekamp et al., 2013; van den Brink et al., 2014; Kajala et al., 2014). For example in plants, asymmetric cell divisions are a common mechanism generating different cell types and tissues from a common progenitor cell (Kajala et al., 2014). Furthermore, the cellular asymmetric distribution of phytohormone transporters can direct the flux of hormones, thereby orchestrating plant development. In Arabidopsis the hormone auxin acts as a morphogen through careful modulation of its New Phytologist (2015) 207: 985–990 www.newphytologist.com
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biosynthesis, transport and cellular response (Benjamins & Scheres, 2008). In particular, it has been shown that transportdependent auxin distribution, via PIN auxin efflux carriers, connects cell polarity and patterning processes in Arabidopsis. The subcellular localisation of PIN proteins determines the direction of intercellular auxin transport, thereby connecting polarity of individual cells of the whole tissues or organs (Benjamins & Scheres, 2008; Abley et al., 2013). PIN proteins continuously cycle between the plasma membrane and endosomes. The sorting of PIN proteins into apical or basal trafficking pathways depends on the phosphorylation status of PINs, which is controlled by the PID protein kinase and PP2A phosphatases (Friml et al., 2004; Benjamins & Scheres, 2008). Interestingly, the asymmetric distribution of the PIN proteins, and therefore the directional flux of auxin, is absolutely required to establish and maintain the bilateral symmetry of an organ, such as in the case of the Arabidopsis ovary where the cellular symmetry breaking of polar PIN localisation promotes bilaterality of the organ. Indeed, interfering with PIN polarity, as in the pid mutant, leads to a break of symmetry in the ovary (Moubayidin & Østergaard, 2014).
IV. Symmetry transitions Symmetry transitions are common in the development of vertebrates, invertebrates and plants, particularly during embryogenesis. In most cases the transition is from radial to bilateral symmetry and controlled by homeotic (Hox) genes and decapentaplegic (dpp) morphogen in animals (Holley et al., 1995; Collins & Valentine, 2001). In Arabidopsis, a radially symmetric embryo structure turns into a bilateral heart-shaped form due to the activity of master gene regulators of the root and shoot apical meristems, as well as auxin dynamics. An example is given by the activity of CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 putative transcription factors and the PIN1 auxin efflux carrier that are necessary for promoting the separation of the two embryonic leaves, the cotyledons. Indeed, the cuc1 cuc2 pin1 triple mutant embryo exhibits a perfectly radial fusion of cotyledons and vascular bundles radially distributed, thus impairing the naturally occurring transition from radial-to-bilateral symmetry (Aida et al., 2002). By contrast, echinoderm embryogenesis involves a transition from bilaterally symmetric larvae to a radial adult animal. During the late larvae stage, discrete populations of tissues on the left side of the body proliferate to form the imaginal adult rudiment, where the first radially symmetric structure appears. During metamorphosis, many larval tissues are lost, and the rudiment gives rise to the major parts of the juvenile animal (Lowe & Wray, 1997). Although these are examples of conversion of an entire structure from one type of symmetry to another, a different kind of symmetry transition can be observed when the apex of a primordium changes its symmetry and thus the primordium continues its growth with a different symmetry. The Arabidopsis gynoecium, is so far the only molecularly documented example of a developing structure that exhibits different symmetries from its base to its tip (Moubayidin & Østergaard, 2014). The gynoecium is derived from the fusion of two carpels and forms in the centre of the flower as a ridge of raised cells around a central cleft (Roeder & Yanofsky, 2006). The main New Phytologist (2015) 207: 985–990 www.newphytologist.com
New Phytologist patterning events of the gynoecium take place before fertilisation and occur along three axes: apical-basal, medio-lateral and abaxial– adaxial (equivalent to dorso-ventrality in animals) (Fig. 2b). At a particular stage of gynoecium development, the distal part becomes topped with stigmatic papillae. The stigmatic tissue functions to attract pollen and mediate pollen germination. It also marks the beginning of the pollen-guiding transmitting tract, which runs down the centre of the ovary allowing fertilisation. A solid style with radial symmetry supports the next segment of the transmitting tract and is required for efficient fertilisation. Below the style, the ovary is formed as a longitudinal cylinder with medio-lateral symmetry that reflects the origin of the gynoecium as two fused leaves. The ovary is composed of two compartments divided by the septum and placenta from which the ovules arise (Roeder & Yanofsky, 2006). We have recently unveiled the biological mechanism that underpins this rare switch from bilateral to radial symmetry occurring at the style region during gynoecium development. We first verified that the bilateral symmetry is the default state during the first gynoecium growth phase, and that two basic helix-loop-helix (bHLH) transcription factors SPATULA (SPT) and INDEHISCENT (IND) are necessary to repress the activity of margin identity genes in order to obtain radiality specifically at the distal part. Coherently, loss-of-function mutations in the SPT and IND genes lead to a failure in radial symmetry establishment at the style region. Remarkably, the misexpression of those genes in a bilateral leaf was sufficient to impose a change to radial symmetry, demonstrating that IND and SPT are necessary and sufficient for mediating organ radialisation. It was previously shown that SPT and IND regulate the transport of auxin in the context of fruit opening by directly repressing PID expression, thus controlling the plasma membrane localisation of PINs and therefore the auxin flux (Sorefan et al., 2009; Girin et al., 2011). At the gynoecium apex auxin distribution is tightly controlled in both time and space. In particular we noticed that auxin distribution precedes and mimics the bilateral-to-radial transition occurring at the gynoecium apex, because it is bilaterally distributed in two lateral foci in the very young gynoecium, while subsequently forming a ring of radial symmetry by passing through a four-foci stage (Fig. 2b). The bilaterally symmetric lateral foci are established due to the polar distribution of PINs in the ovary that drives auxin from the bottom to the top of the organ. These lateral foci guarantee coordinated growth of the two halves along the apical–basal axis. Subsequently, the establishment of the medial foci at the four-foci stage is controlled by the downregulation of PID by SPT and IND, allowing PINs to localise in a nonpolar manner in the cells of the apex, thus generating the auxin ring (Moubayidin & Østergaard, 2014) (Fig. 2b). It is still unclear how the four auxin foci can communicate at a distance and how the polarity of cells at the gynoecium apex is reprogrammed. However, our study showed that the activity of the lateral auxin foci bilaterally distributed function upstream from the activity of the medial foci, which are established later in development. This suggests that a sink and a source of cell polarity are required in order to commit to a symmetry transition. Mathematical and computational predictions may be a powerful tool in the understanding of how this auxin spatio-temporal dynamic is Ó 2015 Crown copyright New Phytologist Ó 2015 New Phytologist Trust
New Phytologist achieved and how it drives the radiality process. The sequentially occurring auxin foci may act as tissue polarity organisers coordinating and coupling cell-to-cell (Abley et al., 2013; Grieneisen et al., 2013).
V. Conclusions Controlling symmetry is an integral part of the development of multicellular organisms. Here we have described that a symmetry transition in the Arabidopsis gynoecium is determined by distribution of a molecule with morphogenic characteristics, auxin. To what extent morphogens control symmetry establishment in plants and animals remains to be established. However, given that communication between cells must be an essential part in coordinating symmetry formation, it is likely that mobile signals as provided by morphogens play prominent roles. Unravelling how short- and long-distance signals function in establishing symmetry in both whole organisms and in individual organs will undoubtedly be a complex task. We therefore predict that efforts to combine experimental biology with mathematical approaches will become increasingly important, thus continuing a millennium-long tradition of mathematicians’ fascination of symmetry in biological structures.
Acknowledgements We thank Mr Andrew Davis for photographic assistance and Drs Veronica Grieneisen and Raffaele Dello Ioio for constructive comments on the manuscript. This work was supported by grant BB/K008617/1 to L.Ø. from the Biotechnological and Biological Sciences Research Council and by the Institute Strategic Programme grant (BB/J004553/1) to the John Innes Centre.
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