Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
*All authors contributed equally
to this work.
†Present address: Department
of Plant and Environmental
Sciences, Section for Plant
Biochemistry Thorvaldsensvej
40, University of Copenhagen,
Denmark
‡Present address: Department
of Biological Sciences,
University of Illinois at Chicago,
Chicago, IL, USA
Received: 01 July 2022
Revised: 09 September 2022
Accepted: 13 September 2022
Version of Record published:
07 October 2022
Review Article
Eco-Evo-Devo of petal pigmentation patterning
Alice L.M Fairnie1,*, May T.S. Yeo1,2,*, Stefano Gatti1,*, Emily Chan1,*, Valentina Travaglia1,*,†,
Joseph F. Walker1,*,‡ and Edwige Moyroud1,2,*
1The Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge CB2 1LR, U.K.; 2Department of Genetics, Downing Site, University of Cambridge, Cambridge CB2
3EJ, U.K.
Correspondence: Edwige Moyroud (em500@cam.ac.uk, edwige.moyroud@slcu.cam.ac.uk)
Colourful spots, stripes and rings decorate the corolla of most flowering plants and fulfil
important biotic and abiotic functions. Spatial differences in the pigmentation of epidermal
cells can create these patterns. The last few years have yielded new data that have started
to illuminate the mechanisms controlling the function, formation and evolution of petal pat-
terns. These advances have broad impacts beyond the immediate field as pigmentation pat-
terns are wonderful systems to explore multiscale biological problems: from understanding
how cells make decisions at the microscale to examining the roots of biodiversity at the
macroscale. These new results also reveal there is more to petal patterning than meets the
eye, opening up a brand new area of investigation. In this mini-review, we summarise our
current knowledge on the Eco-Evo-Devo of petal pigmentation patterns and discuss some
of the most exciting yet unanswered questions that represent avenues for future research.
Introduction
Petals show striking morphological diversity across the∼350,000 species of flowering plants, sometimes
even within the same flower. When asked to describe flowers, it is often easiest to detail the differences
in their petals. Patterns emerge on the petal surface when different regions of the epidermis develop dis-
tinct characteristics. Most petals are not uniformly coloured; some patterns are hidden from us and only
detected by animals. Pollinating insects can perceive differences in colour, shape, scent and texture, or
a combination of these as well as heat, humidity or even electrical charge gradients on the petal surface
[1–9]. Pattern elements acting in combination can create complex petal surfaces, but to date, most studies
have focused on a single pattern element. The best researched petal patterns are colour patterns, including
patterns in the UV range of the spectrum not visible to the human eye [5,10–15]. These patterns include
spots and arrows, stripes, venations, bullseyes, picotees or complex forms combining simplemotifs (Figure
1).
Spots are formed by restricting pigmentation to small dots or circles of cells on the epidermis. Petal
spots can vary in number, position, size or shape [13,16–18]. The shape of white spots in Lapeirousia
oreogena is highly modified, with pointed tips resembling an arrow [19]. The pigmented midrib of Asi-
atic lilies tepals (equivalent to petals) constitute colourful stripes [17], but striped patterns can also be
created by the absence of pigment [20–22]. As seen in snapdragons [23] andmoth orchids [24], venations
resemble stripes, but these pigmentation bands overlay and follow the vein patterns within the petal. Bulls-
eye patterns result from contrasting rings of colour. The Hibiscus trionum bicolour bullseye is visible to
the human eye, with dark anthocyanin pigmentation at the petal base contrasting with cream-coloured
flavonols at the tip [25]. Sunflowers appear uniformly yellow to humans, but to pollinators, their flowers
feature a bullseye due to theUV-absorbing nature of the ligule (a petal-like structure) base [15]. In extreme
cases, only the outer petal margin contrasts with the centre, forming picotee patterns frequent in petunia
cultivars [26]. By combining simple pattern elements, intricate motifs emerge, such as those found on the
Peruvian lily corolla or the labellum of bee orchids (Figure 1).
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
1
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Figure 1. Diversity of petal pigmentation patterns and co-occurrence with other patterned cues
(A) Examples illustrating the diversity of pigmentation patterning on the corolla of flowering plants. Top left: stripe pattern ofGazania
sp.; Top right: venation pattern of Veronica sp.; Middle left: spots pattern of Kohleria warszewiczii; Middle right: bullseye pattern
of the poached egg plant (Limnanthes douglasii); Bottom left: complex pattern combining spots, stripes and brushed marks in
Peruvian lily (Alstroemeria sp.); Bottom right: Bee orchid (Ophrys apifera) flower displaying a pigmentation pattern participating in
mimicry (female body of pollinator) and/or warning signal against herbivores. (B) Chemical pigments acting in the visible and UV
range coexist with physical tridimensional features (cell shape and texture of the cuticle) that sculpt the petal surface. Heat and
humidity gradients, electrical charges and scent emission patterns have also been reported, adding another layer of complexity to
petal patterning.
Plant pigments belong to three main categories: flavonoids (red to blue anthocyanins and cream-yellow flavonols),
carotenoids and betalains. All three groups participate in petal patterning and are highly diverse with regard to their
chemical structures and the colours they produce. The properties of these pigments, along with their synthesis and
their physiological and ecological roles, have been extensively studied and recently reviewed [27–33]. Patterns emerge
when pigment production only occurs in designated epidermal cells or when distinct regions of the petal synthesise
different amounts of a given pigment or different pigment mixtures. This process relies on restricting the expression
of structural genes (i.e., enzymes from the biosynthetic pathways) or the activity of corresponding proteins to specific
regions of the petal.
Transcriptional regulators of the flavonoid pathway are well-known: biosynthetic gene expression is mainly con-
trolled by MBW complexes consisting of R2R3-MYB, basic-helix-loop-helix (bHLH) and WD-repeat (WDR) pro-
teins, reviewed in [34]. MYB proteins serve dual roles as transcriptional activators and repressors of the biosynthetic
pathway. MYB activators of anthocyanin biosynthesis all belong to one of three subgroups 5, 6 or 27, while most
subgroup 4 members repress compound synthesis [34]. Our understanding of floral regulation of carotenoids and
betalain production lags, but recent studies revealed thatMYBs also take centre stage. The R2R3-MYB genesWHITE
PETAL1 and Reduced Carotenoid Pigmentation 1 can regulate carotenoid-derived petal colour in Medicago and
Mimulus lewisii, respectively [35,36]. MYB transcription factors (TFs) also control the synthesis of betalains but
underwent changes to specialise in betalain production [37]: the mode of action of BvMYB1, a highly expressed sub-
group 6 R2R3-MYB identified in beetroot, is unclear but it fails to interact with known bHLH partners derived from
anthocyanic model organisms [37].
2 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Petal patterns have long been a source of fascination for scientists from various disciplines. This may be why the
functional relevance of those motifs, the molecular and cellular events orchestrating their formation and the evolu-
tionary processes that modify them have often been studied independently from each other. However, the field has
gained incredible momentum in the last 15 years. This is in part due to the rapid and widespread adoption of novel
technologies but also thanks to powerful model systems well-suited for functional investigations at the bench as well
as behavioural studies in the field. Petal patterns are more complex than they may appear to the naked human eye. By
taking a multiscale and interdisciplinary approach, it is now possible to start understanding the wealth of fascinat-
ing biology, until very recently largely unexplorable, that underlies those multifunctional features. In this review, we
attempt to synthesise our current understanding of the roles, development and evolution of the motifs that decorate
petal surfaces. We also identify current bottlenecks and gaps in our knowledge, and we propose future strands of re-
search to move the field forward. Finally, we discuss how recent findings position petal patterns as excellent systems
to ask essential questions that reach far beyond the biology of petal patterning, allowing scientists to directly explore
the inner workings of cells and the basis of biodiversity.
Functional relevance of petal patterning
Pollination
Petal patterns are important in pollinator interactions [13,38–41]. Colour patterns can function as communication
tools between flowering plants and their visitors before or after the animal has landed, and the response of a given
pollinator to a specific pattern can be innate or acquired through learning. Pre-landing signals attract pollinators to a
flowerwhile post-landing signals influence theway pollinators handle the flower. These floral guides direct pollinators
towards rewarding or reproductive flower parts and can even deter robbing behaviour [42].
Pattern-mediated pollinator attraction is well commented on in the literature, but until recently, experimental val-
idation remained scarce. In the 1990s, Dafni and colleagues demonstrated that flowers with a dark centre or with
bilaterally symmetric patterns are more attractive to beetles than flowers without a dark centre, or with radially sym-
metric patterns [43,44]. We now know that different species or even individuals can respond differently to a given
pattern: hawkmoths and swallowtail butterflies are attracted toHemerocallis flowers but for different reasons. Swal-
lowtails prefer H. fulva because of colour contrast within the flower. Hawkmoths prefer H. citrina flowers because
of their UV-reflecting bullseye pattern [45]. Yellow monkeyflowers with a red patch across the nectar guide region
appear more appealing to bumblebees than those producing numerous smaller spots [46]. In contrast, a UV bullseye
in yellow silverweed makes flowers more attractive to bees and syrphid flies [13]. As different animal species some-
times show contrasting preferences for different petal motifs, changes in petal patterning during evolution could in
theory contribute to reproductive isolation and eventually led to speciation.
Pigmentation patterns allow flowers to resemble food-rewarding species [47] ormimic the pollinating insect’smate.
Mate mimicry has been proposed for the South African daisy, Gorteria diffusa, which attracts dipteran flies [48];
Linum pubsecens, which attracts bee flies [49] and Romulea monadelpha, Hesperantha vaginata and Sparaxis
elegans, three species pollinated by monkey beetles [50]. The ecological function of Gorteria dark spots was in-
vestigated experimentally with artificial flowers: circular discs with central black spots were shown to reduce the
inter-floral search time of bumblebees compared with unpatterned orange discs [40].
The prevalence of venation patterns could reflect their role as pollinator guides [51], but observational tests of their
exact contribution to plant–animal interactions have been lacking. Artificial flowers with radiating UV blue lines on
a circular blue background or radiating yellow lines on white circular backgrounds reduce bumblebees’ post-landing
nectar discovery time [42,52]. Guideless mutants in Mimulus lack yellow floral guides. Not only are fewer polli-
nator visits recorded for guideless, but the incorrect entry position of visitors likely reduces pollen transfer to the
insect’s body [53]. Experimental manipulations of the Hypoxis camerooniana pattern alter post-landing pollinator
behaviour [54], demonstrating that UV bullseyes can also influence plant–pollinator interactions post-landing.
To date, only a handful of studies have specifically examined how differential visitation associated with colour pat-
terns, rather than with overall flower colour or other well-studied floral traits such as flower size and shape, translates
into individual fitness. The findings of those studies indicate that the effect of petal patterning on plants reproductive
success varies broadly between species and is likely to depend heavily on the environmental context. For example,
Tremblay and Ackerman [55] found that bicoloured flowers are more common than uniformly pigmented ones in
various populations of a small Puerto Rican orchid. However, the authors could not detect any association between
the presence of a pattern and a positive effect onmale or female fitness (i.e., the ability to export pollen or the capacity
to receive pollen and produce seeds, respectively) [55]. In contrast, Hansen and colleagues [19] found that removing
the arrow-shaped nectar guide from the corolla of the South African iris is sufficient to almost completely suppress
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
3
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
pollen export and to significantly reduce the ability of the plant to set fruits. In this case both male and female fitness
are severely affected when a specific element of the petal pattern disappears. Importantly, the ability of petal patterns
to impact on reproductive success is likely to be context dependant: in silverweed larger UV-absorbing bullseyes re-
ceived twice as many foraging visitors than smaller bullseyes but this difference was only observed in individuals
growing at high altitude [56]. Petal patterns that increase the frequency of foraging visits can potentially affect both
male and female fitness as the chance to export and receive pollen is increased. Thus, a selection acting on pattern
dimensions could act via both male and female functions but whether this is the case may depend on other factors
(i.e., pattern visibility varying as light conditions change with altitude, presence of different plant neighbours).
Recent research suggests that coloured petal patterns could also fulfil functions unrelated to pollination, including
response to environmental factors or interactions with pests and herbivores. These alternative functions are perhaps
better thought of as additional functions because they may act alongside pollinator interactions.
Predation
Colourful displays usually produced by flowers are occasionally found on other plant organs: various carnivorous
plants display patternswithin theUV light range on their trap [57], amodified leaf dedicated to prey capture. Artificial
plantswithUVpatternsmimicking those foundon the rimof pitcher plants capturemore flieswith normal vision than
flies with reduced vision, suggesting that pigmentation patterns can serve as visual cues capable of luring prey [58].
Whether thismechanism is used by other species of carnivorous plants to attract insects remains to be established [59].
Predatory animals can even exploit pollinators’ preferences for certain pigmentation patterns: the UV-reflective body
of the spider crab creates a contrasting pattern on the otherwise uniformly white corolla of daisies. The presence of
the spider crab enhances the flower’s attractiveness to pattern-sensitive honeybees, which could constitute an effective
tactic to ambush prey [60].
Defence
St. John’s wort flowers exhibit a UV pattern on the back of their petals (Figure 2A). This pattern bears a mixture of
de-aromatised isoprenylated phloroglucinols, including hypercalin A, a deterrent toxic to the caterpillar herbivore
of the Bella moth [61]. The UV-absorbing compounds could appeal visually to pollinators by creating a bullseye
involving the flower’s reproductive organs and providing protection against herbivores to pollen and seeds. Animals
commonly use colouration as a strategy to avoid predation. Predation-avoidance strategies also occur in plants, in
particular as defence against herbivores [62,63]. A role for petal colour pattern as a warning signal has been proposed
but needs to be fully tested. Bee orchids (Figure 1) may attract pollinators through scent mimicry alone as the visual
details on the flower seem too delicate for bees which have limited spatial resolution. In this instance, the visual
pattern on the corolla may instead deter herbivorous mammals [64]. Ants are known to protect certain species of
plants from herbivores and nectar thieves, and black markings on the petals of several species of passion fruit flowers
could mimic those beneficial insects [65,66].
Abiotic functions
Petal pigmentation patterns can also fulfil abiotic functions: the size of the UV-absorbing bullseye of silverweed
co-varies with UV incidence as populations experiencing higher UV irradiation display a larger UV-absorbing centre
[12] capable of shielding pollen grains from damaging UV raysmore efficiently than a smaller UV-absorbing bullseye
(Figure 2B). Local pigment accumulation, especially UV-absorbing compounds, can also generate temperature and
humidity gradients on the petal surface by capturing heat from the sun or by reducing water loss [14,67,68]. Patterned
species across the Potentilleae tribe experiencing lower temperatures and sunflower populations growing in drier and
colder sites tend to produce larger UV-absorbing bullseyes [15,69]. These observations support the idea that pattern
dimensions may be adaptive, limiting cooling via transpiration and preventing drought stress. Because bumblebees
can perceive temperature and humidity gradients [1–3], this raises the interesting possibility that pigmentation pat-
terns directly influence the patterning of other cues.
Developmental processes governing petal pattern formation
Variegation, colour flecks and stripes can occur due to viral infections triggering ‘colour breaks’ and genetic instability
caused by transposon activity [10,70,71]. However, pattern formation is usually tightly regulated in place and time.
Thus, petals are emerging models for understanding two intimately linked developmental processes: (i) patterning,
which creates regions of distinct cell types, and (ii) growth, which increases tissue size, generates organ shape and
acts as a modifier of patterning processes [72,73].
4 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Figure 2. Pigmentation patterns can provide defence against herbivores and environmental conditions
(A) The flower of St John’s wort (Hypericum calycinum) produces a UV bullseye that could participate in pollinator attraction (UV
absorption) and provide chemical defence (DIP production) against the caterpillar herbivore of the Bella moth. (B) The flowers of
silverweed cinquefoil (Argentina anserina) appear yellow to the human eye but produce a UV bullseye. The size of the UV absorbing
region can vary between populations: individuals growing at lower latitudes or higher altitudes tend to form larger bullseyes. If big
enough, the bullseye can effectively shield pollen grains against damage caused by UV irradiance: incident UV rays are absorbed by
the bullseye centre instead of being reflected on the pollen-producing anthers in the centre of the flower. The percentage of viable
pollen grains following UV treatment was found to increase with bullseye size, supporting a protective role for petal pigmentation
patterns. Image credit in (A) JJ Harrison via Wikimedia Commons and in (B) Dr Matthew H. Koski.
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
5
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Figure 3. Positional and self-organisation processes regulating pigmentation pattern formation
The formation of pigmentation patterns on the petal epidermis can be orchestrated by positional mechanisms (A,B) and self-or-
ganising processes (C). (A) The venation pattern in a subspecies of snapdragon is specified by overlapping expression domains
of a MYB transcription factor, VENOSA, and its bHLH partner, DELILA. As both components need to be present for the MBW
complex to function, anthocyanin production is only triggered in the few epidermis cells situated just above the petal vascula-
ture. (B) Morphogen diffusion could in theory pre-pattern the epidermis of the developing petal by forming concentration gradients
along their proximo-distal axis. Different morphogen concentrations could activate distinct genetic programs to specify multiple
cell fates and the production of various pigment mixtures in different portions of the petal. Such a mechanism could account for
the production of the striking bullseye of the South African Geissorhiza radians. (C) Left: formation of red anthocyanin spots on the
corolla of monkeyflowers is regulated by a reaction-diffusion system involving an activator of pigment synthesis, NEGAN, and its
diffusing repressor, RED TONGUE (RTO). Right: in rto/rto homozygous mutants, the lack of inhibitor function yields flowers with a
near-uniform patch of anthocyanin colour at the base of their petals.
During petal development, the activities of the transcription factors that regulate pigmentation pathways, cell fate
specification and tissue growth are likely to be set by pre-patterns [10]. These pre-patterns, set by region-specific
expression of upstreamgenes prior to tissue differentiation, define spatiotemporal boundaries and subdomainswithin
the epidermis.Whilemechanisms that could provide this spatial information have been theorised extensively, the true
regulatory mechanisms have remained, until recently, largely unexplored in petals.
Overlapping expression domains
Expression of each component of the MBW complex is critical as the complex is only active when all components
are present. This provides grounds for emergence of precise pigmentation patterns from broadly defined expression
domains. In snapdragon, venation patterning requires the R2R3 MYB VENOSA and its bHLH partner DELILA.
VENOSA is expressed around the vasculature whileDELILA transcription is restricted to the petal epidermis, defin-
ing a narrow overlapping domain in the epidermal cells overlying the vasculature where partners coexist and activate
anthocyanin production [23] (Figure 3A). However, it is unclear what sets the expression domains ofMYB and bHLH
components in the first place. For certain types of patterns, the required positional information could be specified
through signalling from an existing differentiated region. Here, the vasculaturemay provide the localised signal to ac-
tivate VENOSA expression. This signal could be auxin as VENOSA has two auxin-response element-like sequences
in its promoter [23].
Morphogen gradients
Morphogens can also provide positional information (Figure 3B). This notion is well defined in animals where growth
and patterning can be coordinated by diffusible signals produced at a localised source and forming concentration
6 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
gradients across a tissue. These gradients modulate cell fate and proliferation in a concentration-dependent man-
ner to convey positional information [74]. The existence of morphogens in plants is still under scrutiny [75], al-
though auxin, small RNAs, peptides or even transcription factors could fulfil a morphogen-like role [76–79]. In
roots, the combined concentration gradients of auxin and PLETHORA (PLT) transcription factors spatially organ-
ise three distinct zones where cells proliferate, elongate and finally differentiate in a threshold-dependent manner
[80]. In petals, PLETHORA3 also regulates cell proliferation and differentiation in a dose-dependent manner [81].
However, whether a PLT3 concentration gradient exists in developing petals is unclear. Opposite gradients of the
small RNA miR396 and the GIF1/AN3 TF shape GROWTH REGULATORY FACTOR (GRF) activity along the
proximo-distal axis of developing leaves [82]. The gif1/an3 mutation also affects petals, yielding shorter, narrower
petals [83,84]. However, the expression and activity domains of miR396, GRFs and GIFs remain to be characterised
with spatiotemporal resolution in floral organs to determine whether themiR396-GRF/GIFmodule can pattern petal
cell proliferation and differentiation.
Self-organisation
Spontaneous acquisition of positional characteristics without apparent pre-patterns is common in animals and plants
[10,75,85,86]. Self-organising pattern formation is often explained by reaction-diffusionmodels. Thesemodels postu-
late that patterns arise through instabilities generated by the interplay between at least two molecular factors, namely
an activator which activates its own production, and an inhibitor that represses the activator [87,88].
The development of red spots inMimulus guttatus is the product of a two-component reaction-diffusion system
involving an R2R3-MYB activator, NECTAR GUIDE ANTHOCYANIN (NEGAN), and the R3-MYB diffusible in-
hibitor, RED TONGUE (RTO) (Figure 3C). NEGAN activates anthocyanin production at the petal base. NEGAN
also promotes its own transcription along with the expression of RTO, which acts as a long-range inhibitor of NE-
GAN to regulate spot formation [46]. Anthocyanin pigmentation does not extend across the entire petal epidermis
in the rto mutant but is restricted to the proximal half, producing a ‘red tongue’ (Figure 3C). This phenotype reveals
the existence of positional information, acting upstream of the reaction-diffusion mechanism, to restrict the initial
expression of NEGAN to the proximal region. Thus, monkeyflower petals utilise pre-patterning processes (that set
the initial conditions and restrict pattern formation in space) and self-organising mechanisms (that act downstream
and specify the type of pattern) to add spots to the petal base.
Modelling approaches are powerful ways to explore pattern emergence, especially as the processes involved are
often not intuitive. By combining mathematical models of relatively simple mechanisms, Ringham and colleagues
recapitulated a broad range of petal patterns observed across flowers [89]. A theoretical model indicates that an
activator-repressor system could also account for the violet and white pigmentation rings characteristic of passion
flowers, although the molecular players remain to be identified [90]. A modified form of the reaction-diffusion sys-
tem, the substrate-depletion model, has been proposed to explain haloed spot formation in foxgloves, where petal
spots are surrounded by a zone of reduced pigmentation [10]. Models for spot-halo formation are based either on
the export of R3-MYB repressors from the spot cells or depletion of an activator or biosynthetic substrate (e.g., WDR
co-regulators) from cells surrounding the spot. However, whether a substrate-depletion mechanism can account for
spot-halo formation remains to be demonstrated.
Contribution of structural elements
Pigment appearance can change according to their subcellular location and the shape of the cell. Cell shape and cuticle
texture constitute tridimensional structures that impact the path of light entering or exiting the cell, modifying the
visual aspect of the petal or even producing colours through light diffraction and constructive interference [4,91–97].
Thus, colour patterns could, in theory, emerge not bymodifying pigment production locally but by varying cell shape
and texture across the petal surface (Figure 1B). Much remains to be understood about the mechanisms controlling
cell shape geometry and nanopatterning of the cell surface [92]. Whether and how the processes regulating the dis-
tribution of physical features or the production of chemical compounds across the petal epidermis are coordinated is
unknown and represents an exciting strand of investigation.
Mechanisms of petal pattern evolution
Petal pigmentation patterns can be gained, lost or experience changes in colouration hue or intensity during evo-
lution. The relative position of pattern elements or their proportions can be altered, and pigmentation patterns can
convert from one type into another (Figure 4A). By investigating pattern variations between species, varieties or even
populations, we are beginning to identify the molecular and cellular processes that mediate pattern modifications.
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
7
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Figure 4. Mechanisms associated with pigmentation pattern evolution
(A) Possible modifications affecting petal pigmentation patterns (centre) and examples from the literature corresponding to each
case. (B) A shift in petal spot position in Clarkia gracilis occurred following mutation(s) in the regulatory region of CgMYB1: expres-
sion of an ancestral CgMYB1b allele is thought to have been activated by an unknown TF, TF X, restricted to the petal base. This
results in the production of basal petal red spots similar to the one of subspecies albicaulis. Mutations in the promoter of CgMYB1
would have resulted in the loss of TF X cis-elements, but a gain of binding sites for another unidentified activator, TF Y, expressed
in the middle of the petal. The new allele CgMYB1c is capable of triggering spot production higher up along the proximo-distal axis
of the sonomensis subspecies.
Shifts in colour patterning appear predominantly linked tomodified expression patterns of R2R3-MYB regulatory
genes. Mimulus lewisii flowers display a white ring around their corolla throat, but the resulting picotee pattern is
absent inM. cardinalis. Such difference between closely relatedmonkeyflowers is due to cis-regulatory variation that
triggers the expression of LIGHT AREAS1, an R2R3-MYB that promotes flavonol production, around the throat
margin of M. lewisii [16].
Members of the Clarkia gracilis species complex can be distinguished by the position of their petal spot [18]
(Figure 4B). The basal position is thought to be ancestral, and the shift likely occurred via cis-regulatory rewiring:
the position of the spot is governed by distinct alleles of the CgMYB1 gene, whose expression patterns match either
the basal (CgMYB1b) or central (CgMYB1c) regions accumulating anthocyanins [18]. The authors postulate the
existence of two upstream regulators, TF-X and TF-Y, whose expression is limited to the proximal or mid-section of
the petal, respectively, in earlier stages of petal development. Changes affecting the regulatory region of an ancestral
CgMYB1b-like allele led toMYB1 losing its ability to be activated byTF-Xwhile becoming controlled byTF-Y (Figure
4B). The identities of such pre-patterned regulators and the mechanisms accounting for their localised expression
remain to be understood.
Mutations affecting gene coding regions can also trigger changes in petal patterning. The transition from pink to
white in the petal base of Clarkia gracilis ssp. sonomensis is due to a truncated CgsMYB12 (1bp deletion in exon
3 leading to an early stop codon), which normally regulates anthocyanin production [98]. M. guttatus populations
from Oregon and California show variation in patterning of their yellow flowers, ranging from having a fully red
corolla throat (red-tongue bullseye) to a red spotted corolla throat. The transition from spot to bullseye across those
wild populations is due to different alleles of RTO, with the red-tongue bullseye morph only carrying non-functional
rto alleles [46] (Figure 3C).
8 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Figure 5. A possible role for growth as a modifier of pigmentation pattern during evolution
Change in pigmentation pattern dimensions can result from modifications in early pre-patterning mechanisms that divide the petal
primordia in subregions and/or local variation in cell proliferation or expansion in developmental stages following the pre-patterning
phase. (A) Schematic representation of a theoretical petal primordium at very early stages of development, prior to pigmentation
pattern formation. In this early phase, pre-patterningmechanisms act to divide the petal surface in subregions that can later develop
distinct cell fates. Here proximal and distal regions are specified: the white triangle indicates boundary position along a line of 8
cells going from the base to the tip of the petal. As development progresses, cell division increases total cell number and cells
acquire distinct identities in each compartment: cells in the distal region synthesises pigments while cells in the proximal domain
remain unpigmented, forming a visible bullseye pattern. (B) Larger bullseyes can be obtained by at least two modes: in (1), the early
pre-patterning processes remain unchanged and the boundary between proximal and distal regions is specified as in (A) but in later
stages, an increase in either cell division rate (top lane) or cell expansion (bottom lane) in the proximal region would modify the final
proportions, yielding a larger unpigmented region. Alternatively, in (2), the early boundary is specified higher along the proximo-distal
axis (e.g. increase in morphogen production) so that a larger proximal compartment is specified. (C) Similar scenarios can lead to a
reduction in bullseye size: (3) cell division (top lane) or expansion (bottom lane) can be increased in the distal region post-patterning
or (4) the early developmental boundary can be specified closer to the petal base during the pre-patterning phase.
White triangle: position of the early developmental boundary; purple triangle: position of the bullseye boundary in the mature petal;
squares and rectangles: individual cells along the proximo-distal axis; numbers under each line of cells: cell number in each petal
subregion.
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
9
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Recently, gene duplication of R2R3-MYB was put forward as a facilitator of pattern diversification [99]: duplicates
can retain their ability to activate pigment production but gainmore restricted expression domains, providing numer-
ous possibilities to create new pigmentation patterns – for instance, the uniform pink background pigmentation of
Clarkia gracilis ssp. sonomensis petals results from the combined action of not one but two close paralogs, MYB11
and MYB12 [98]. Both TFs can induce pigment synthesis when ectopically expressed in Arabidopsis. CgsMYB11,
is normally expressed across the petal epidermis, except at the very base. CgsMYB12 by contrast is only expressed
in the proximal portion of the petal. Expression patterns of these two MYBs together led to uniform anthocyanin
production across the petal in the wild-type. But a ‘white cup’ phenotype is observed in individuals with a mutated
CgsMYB12 locus preventing anthocyanin synthesis in the basal region. Similar studies in different species scattered
across the angiosperm phylogeny are now required to identify possible trends and to evaluate the relative contribution
of gene duplication to the emergence of novel petal patterns. Contraction of the expression domain of MYB12 and
MYB11 in other Clarkia subspecies has also been proposed [99], but our ability to test such hypotheses is currently
limited by the lack of knowledge regarding the regulatory mechanisms acting upstream of MYB genes.
Petal pigmentation patterns also evolve through selection on small regulatory RNAs. Bradley and colleagues re-
vealed that the SULF locus drives the production of a yellow highlight on the corolla of the pseudomajus subspecies
of snapdragon, guiding pollinating bees to the flower entrance [100]. This locus is under selection and emerged from
a genomic inverted duplication event. SULF codes for small RNAs that target the transcripts of Am4’CGT, the enzyme
that produces the yellow pigment, leading to its post-transcriptional silencing. In pseudomajus, SULF is transcrip-
tionally active throughout the corolla except for a small portion of the ventral petal marking the flower entrance,
forming the nectar guide emblematic of this subspecies of snapdragon.
From an evolutionary viewpoint, petals can be seen asmodified leaves [101] and gene regulatory networks control-
ling lateral organ patterning could be shared between petals and leaves. Pigmentation pattern on leaves is less conspic-
uous than those displayed by flowers and their function remains unclear. As such, the production of leaf pigmentation
patterns has received little attention. Work in clover and Medicago identified R2R3-MYBs linked to different types
of leaf markings [102,103]. One of those factors, RED HEART1 (RH1), interacts with bHLH andWD40 members to
activate anthocyanin production [103]. This points towards a role for MBW complexes in leaf pigmentation pattern-
ing and supports the idea that floral MBW complexes could have evolved from leaf MBW complexes. It remains to
be seen whether this only applies to the MBW complex or whether the upstream regulatory processes that divide the
petal into sub-regions are also inherited from a leaf-like ancestor. While we know little about pigmentation pattern
regulation in the leaf, the upstream processes that regulate lateral organ polarity and patterning have been extensively
studied in leaves [104,105]. Future studies should test to what extent the mechanisms dividing emerging leaves and
petals into subdomains are variations from a common ancestral system that creates boundaries across all flowering
plant lateral organs.
Changes in petal pigmentation patterns could lead to reproductive isolation and speciation [106–108]. Studying
the mechanisms leading to variation in petal motifs is therefore important to understand the sources of natural di-
versity. Data generated in the last few years indicate that changes in pigmentation patterns also represent adapta-
tions to environmental factors such as geography and climate [12,69]. A study exploiting herbaria collections from
North America, Europe and Australia indicated that UV-absorbing bullseyes have increased in size globally since the
mid-twentieth century: in saucer-shaped flowers, the proportion of UV-absorbing pigment in the petal epidermis
increased when ozone levels declined and decreased in locations where ozone levels increased. This trend identifies
floral pattern variations as a rapid response of plants to anthropogenic climate changes [14]. The UV bullseye pattern
size in some sunflowers is defined by roles in both pollinator attraction and desiccation resistance withmedium-sized
UV-absorbing centres attracting more pollinators. In contrast, larger-sized UV-absorbing centres offer better protec-
tion against desiccation [15]. These findings perfectly illustrate that overall changes in petal pigmentation patterns
are likely to be under the influence of multiple, and sometimes opposing, biological and environmental factors.
Future directions
Colourful flower patterns are major contributors to the diversity of the natural world. The last decade has greatly
expanded our understanding of the development and evolution of flower patterns, but many questions remain. Func-
tional investigations in novel model systems suggest that changes affecting MYB genes are often associated with
variations in petal patterning during evolution. MYBs are well-known regulators of pigment synthesis hence family
members are often selected first as candidate genes, but other family of pigment patterns regulators are likely to ex-
ist and could also contribute to the evolution of colourful motifs on the corolla of flowering plants. Several studies
have shown that petal patterns can be modified when MYB coding sequence or regulatory elements are modified.
10 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
Whether gene duplication followed by neo/subfunctionalisation or co-option of existing MYBs are equally likely to
contribute to the emergence of new pattern elements remains to be tested. Importantly, identifying whichMYB gene
regulates pigment production in each sub-domain of the petal is important, but to understand the evolution of petal
patterns it is now crucial to resolve the upstream mechanisms that regulate the spatio-temporal expression of those
MYBs. Hence, it will be essential to uncover the identity of the pre-patterned regulators and signalling processes that
partition the petal surface in early phases of primordia development and this represents an exciting venue for future
evo-devo research.
The petal epidermis is a sensory billboard that combines diverse cues animals can perceive. Localised synthesis
of chemical pigments is only one component of flowering plants’ palette. It is now evident that the elaboration of
physical features such as cell shape and texture, scent emission and the distribution of heat and humidity can also be
precisely patterned across the petal surface [2,3,7,9,92]. How these elements impact each other, and to what extent
the production of these distinct features is regulated by shared or independent processes remain to be investigated.
Patterns displayed onmature tissues of opened flowers result from the combined effects of patterning mechanisms
that specify cell fate and pattern modifiers such as growth. The roles that cell proliferation and expansion play in
controlling pattern proportions and whether or not those processes can also be targeted by evolution to generate
diversity remain to be understood. In Figure 5, we illustrate possible roles for growth as amodifier of coloured pattern
dimensions during evolution. The development of novel model systems amenable to both lab work and field studies,
along with technological breakthroughs such as single cell RNAseq and live imaging to study differentiation and
growth at the cellular resolution, opens unprecedented paths to address these questions.
Although it is now clear that visiting animals can discriminate flowers based on presence/absence of petal pat-
terns, it remains to be seen to which extent variation in pattern dimension influence pollinator behaviour before and
after landing. In addition, differential visitation does not automatically translate into effects on the fitness of indi-
viduals. First, not all visitors perform a pollination services and distinguishing mere visitors from actual pollinators
require careful experimental designs. Petal patterns acting as long-range signals that increase flower conspicuousness
would be expected to increase male fitness (i.e., pollen export capability). Similarly, pigmentation motifs acting as
post-landing guides could positively affect female fitness (i.e., pollen reception and seed production capabilities) by
manipulating the position of the insect body in a way that maximise pollen deposition on stigmata, enhancing the
chance of ovule fertilization and seed formation. However, the roads to male and female fitness are complexes: many
external factors such as abiotic environmental conditions or the presence of different neighbour competing for ani-
mal attention as well as circumstances intrinsic to each species (e.g., the ability self-pollinate) all play a role and must
be accounted for. One of the most exciting challenges for future studies will be to disentangle the contribution, if any,
of petal patterns to reproductive fitness and identify precisely, in a diversity of systems, the mechanisms by which
colourful motifs can influence pollination success to see if trends can be identified.
Petal patterns provide experimental and theoretical scientists with numerous opportunities for collaborative and
interdisciplinary work. They also constitute excellent systems to understand how decisions made by minute cells
are coordinated at the tissue and organ scale, how the execution of different developmental programs impact each
other, and how evolutionary processes and diverse biotic and abiotic factors can drive and shape biodiversity. Thus,
studying petal patterns help address fundamental questions of modern biology that reach far beyond understanding
how flowering plants paint their surface.
Summary
• Underlying petal pigmentation patterns is a wealth of fascinating biology that until very recently
has been largely unexplorable.
• Petal patterns are multifunctional: they participate in plant–pollinator communication but also me-
diate interactions with herbivores, protect pollen grains from UV radiation, or enhance resistance
to desiccation.
• Pigmentation motifs coexist with other patterns inconspicuous to the human eye because they are
microscopic (i.e., cell shape) or because they are by nature invisible (i.e., temperature gradients).
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution
License 4.0 (CC BY).
11
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
• The petal epidermis is an excellent system to study the dynamics of cellular decision-making
processes because the outcomes of decisions made by cells at the microscopic level are readily
observable and can directly impact reproductive success at the macroscale.
• Petal pigmentation patterns can vary between populations and species: they can be lost or gained
but also change in shape and dimension during evolution. Those changes can be adaptive with
both abiotic and biotic factors able to exert selective pressures. Pattern variations can be used as
markers of climate change but also lead to reproductive isolation and speciation.
• Future research will aim at understanding the mechanisms used by epidermal cells to make de-
cisions, how these decisions are coordinated at the tissue and organ scale, what the origins of
regulatory networks that govern petal patterning are and how rewiring of these networks con-
tribute to plant fitness and the creation of biodiversity.
Competing Interests
The authors declare that there are no competing interests associated with the manuscript.
Funding
Our research is supported by the Gatsby Charitable Foundation, the Isaac Newton Trust/Wellcome Trust ISSF and the BBSRC
Doctoral Training Program.
Open Access
Open access for this article was enabled by the participation of University of Cambridge in an all-inclusive Read & Publish agree-
ment with Portland Press and the Biochemical Society under a transformative agreement with JISC.
Author Contribution
M.T.S.Y., A.L.M.F., V.T., E.C., S.G., J.F.W. and E.M. wrote the manuscript. S.G. and E.M. prepared the figures with inputs from all
other authors.
Acknowledgements
We apologize to the researchers whose work was unable to be included due to space constraints. We are grateful to Dr Renske
Vroomans, Dr Alistair McGregor and Dr Alexandra Buffry for inviting us to contribute to this issue on evolutionary developmental
biology of Essays in Biochemistry. We would like to thank Dr Matthew H. Koski for kindly providing us with the images of Argentina
anserina included in Figure 2B and all members of the Moyroud lab for comments and feedback on earlier version of this review.
We also thank two anonymous reviewers for taking time to review our manuscript and for making constructive suggestions which
help to enhance the review.
Abbreviations
bHLH, basic-helix-loop-helix; MBW, MYB-bHLH-WD40 complex; TF, transcription factor; WDR, WD-repeat.
References
1 Harrap, M.J.M., Hempel de Ibarra, N., Whitney, H.M. and Rands, S.A. (2020) Floral temperature patterns can function as floral guides. Arthropod-Plant
Interact. 14, 193–206, https://doi.org/10.1007/s11829-020-09742-z
2 Harrap, M.J.M., Hempel de Ibarra, N., Knowles, H.D., Whitney, H.M. and Rands, S.A. (2021) Bumblebees can detect floral humidity. J. Exp. Biol. 224,
jeb240861, https://doi.org/10.1242/jeb.240861
3 Harrap, M.J., Rands, S.A., Hempel de Ibarra, N. and Whitney, H.M. (2017) The diversity of floral temperature patterns, and their use by pollinators.
Dicke M, Editor. eLife 6, e31262, https://doi.org/10.7554/eLife.31262
4 Moyroud, E. and Glover, B.J. (2017) The physics of pollinator attraction. New Phytol. 216, 350–354, https://doi.org/10.1111/nph.14312
5 Wester, P. and Lunau, K. (2017) Chapter Nine - Plant-Pollinator Communication. In Advances in Botanical Research (Becard, G., ed.), pp. 225–257,
Academic Press, (How Plants Communicate with their Biotic Environment; vol. 82). Available from:
https://www.sciencedirect.com/science/article/pii/S0065229616301124
6 von Arx, M., Goyret, J., Davidowitz, G. and Raguso, R.A. (2012) Floral humidity as a reliable sensory cue for profitability assessment by
nectar-foraging hawkmoths. Proc. Natl. Acad. Sci. 109, 9471–9476, https://doi.org/10.1073/pnas.1121624109
12 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
7 Skaliter, O., Kitsberg, Y., Sharon, E., Shklarman, E., Shor, E., Masci, T. et al. (2021) Spatial patterning of scent in petunia corolla is discriminated by
bees and involves the ABCG1 transporter. Plant J. 106, 1746–1758, https://doi.org/10.1111/tpj.15269
8 Clarke, D., Whitney, H., Sutton, G. and Robert, D. (2013) Detection and learning of floral electric fields by bumblebees. Science 340, 66–69,
https://doi.org/10.1126/science.1230883
9 Lawson, D.A., Chittka, L., Whitney, H.M. and Rands, S.A. (2018) Bumblebees distinguish floral scent patterns, and can transfer these to corresponding
visual patterns. Proc. R. Soc. B. Biol. Sci. 285, 20180661, https://doi.org/10.1098/rspb.2018.0661
10 Davies, K.M., Albert, N.W., Schwinn, K.E., Davies, K.M., Albert, N.W. and Schwinn, K.E. (2012) From landing lights to mimicry: the molecular regulation
of flower colouration and mechanisms for pigmentation patterning. Funct. Plant Biol. 39, 619–638, https://doi.org/10.1071/FP12195
11 Albert, N.W., Davies, K.M. and Schwinn, K.E. (2014) Gene regulation networks generate diverse pigmentation patterns in plants. Plant Signal Behav. 9,
e29526, https://doi.org/10.4161/psb.29526
12 Koski, M.H. and Ashman, T.L. (2015) Floral pigmentation patterns provide an example of Gloger’s rule in plants. Nat. Plants 1, 1–5,
https://doi.org/10.1038/nplants.2014.7
13 Koski, M.H. and Ashman, T.L. (2014) Dissecting pollinator responses to a ubiquitous ultraviolet floral pattern in the wild. Funct. Ecol. 28, 868–877,
https://doi.org/10.1111/1365-2435.12242
14 Koski, M.H., MacQueen, D. and Ashman, T.L. (2020) Floral pigmentation has responded rapidly to global change in ozone and temperature. Curr. Biol.
30, 4425.e3–4431.e3, https://doi.org/10.1016/j.cub.2020.08.077
15 Todesco, M., Bercovich, N., Kim, A., Imerovski, I., Owens, G.L., Dorado Ruiz, O´. et al. (2022) Genetic basis and dual adaptive role of floral pigmentation
in sunflowers. Ross-Ibarra J, Kleine-Vehn J, Baldwin IT, editors. eLife 11, e72072, https://doi.org/10.7554/eLife.72072
16 Yuan, Y.W., Rebocho, A.B., Sagawa, J.M., Stanley, L.E. and Bradshaw, H.D. (2016) Competition between anthocyanin and flavonol biosynthesis
produces spatial pattern variation of floral pigments between Mimulus species. Proc. Natl. Acad. Sci. 113, 2448–2453,
https://doi.org/10.1073/pnas.1515294113
17 Yamagishi, M., Toda, S. and Tasaki, K. (2014) The novel allele of the LhMYB12 gene is involved in splatter-type spot formation on the flower tepals of
Asiatic hybrid lilies (Lilium spp.). New Phytol. 201, 1009–1020, https://doi.org/10.1111/nph.12572
18 Martins, T.R., Jiang, P. and Rausher, M.D. (2017) How petals change their spots: cis-regulatory re-wiring in Clarkia (Onagraceae). New Phytol. 216,
510–518, https://doi.org/10.1111/nph.14163
19 Hansen, D.M., Van der Niet, T. and Johnson, S.D. (2012) Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behaviour and
plant fitness. Proc. R. Soc. B. Biol. Sci. 279, 634–639, https://doi.org/10.1098/rspb.2011.1349
20 Ohta, Y., Atsumi, G., Yoshida, C., Takahashi, S., Shimizu, M., Nishihara, M. et al. (2021) Post-transcriptional gene silencing of the chalcone synthase
gene CHS causes corolla lobe-specific whiting of Japanese gentian. Planta 255, 29, https://doi.org/10.1007/s00425-021-03815-w
21 Morita, Y., Saito, R., Ban, Y., Tanikawa, N., Kuchitsu, K., Ando, T. et al. (2012) Tandemly arranged chalcone synthase A genes contribute to the spatially
regulated expression of siRNA and the natural bicolor floral phenotype in Petunia hybrida. Plant J. 70, 739–749,
https://doi.org/10.1111/j.1365-313X.2012.04908.x
22 Koseki, M., Goto, K., Masuta, C. and Kanazawa, A. (2005) The star-type color pattern in petunia hybrida ‘red star’ flowers is induced by
sequence-specific degradation of chalcone synthase RNA. Plant Cell Physiol. 46, 1879–1883, https://doi.org/10.1093/pcp/pci192
23 Shang, Y., Venail, J., Mackay, S., Bailey, P.C., Schwinn, K.E., Jameson, P.E. et al. (2011) The molecular basis for venation patterning of pigmentation
and its effect on pollinator attraction in flowers of Antirrhinum. New Phytol. 189, 602–615, https://doi.org/10.1111/j.1469-8137.2010.03498.x
24 Hsu, C.C., Chen, Y.Y., Tsai, W.C., Chen, W.H. and Chen, H.H. (2015) Three R2R3-MYB transcription factors regulate distinct floral pigmentation
patterning in phalaenopsis spp. Plant Physiol. 168, 175–191, https://doi.org/10.1104/pp.114.254599
25 Vignolini, S., Moyroud, E., Hingant, T., Banks, H., Rudall, P.J., Steiner, U. et al. (2015) The flower of hibiscus trionum is both visibly and measurably
iridescent. New Phytol. 205, 97–101, https://doi.org/10.1111/nph.12958
26 Saito, R., Fukuta, N., Ohmiya, A., Itoh, Y., Ozeki, Y., Kuchitsu, K. et al. (2006) Regulation of anthocyanin biosynthesis involved in the formation of
marginal picotee petals in Petunia. Plant Sci. 170, 828–834, https://doi.org/10.1016/j.plantsci.2005.12.003
27 Timoneda, A., Feng, T., Sheehan, H., Walker-Hale, N., Pucker, B., Lopez-Nieves, S. et al. (2019) The evolution of betalain biosynthesis in
Caryophyllales. New Phytol. 224, 71–85, https://doi.org/10.1111/nph.15980
28 Stanley, L. and Yuan, Y.W. (2019) Transcriptional regulation of carotenoid biosynthesis in plants: so many regulators, so little consensus. Front. Plant
Sci. 10, 1–17, https://doi.org/10.3389/fpls.2019.01017
29 Wen, W., Alseekh, S. and Fernie, A.R. (2020) Conservation and diversification of flavonoid metabolism in the plant kingdom. Curr. Opin. Plant Biol. 55,
100–108, https://doi.org/10.1016/j.pbi.2020.04.004
30 Sun, T. and Li, L. (2020) Toward the ‘golden’ era: The status in uncovering the regulatory control of carotenoid accumulation in plants. Plant Sci. 290,
110331, https://doi.org/10.1016/j.plantsci.2019.110331
31 Tossi, V.E., Martı´nez Tosar, L., Pitta-A´lvarez, S.I. and Causin, H.F. (2021) Casting light on the pathway to betalain biosynthesis: A review. Environ. Exp.
Bot. 186, 104464, https://doi.org/10.1016/j.envexpbot.2021.104464
32 Yin, X., Wang, T., Zhang, M., Zhang, Y., Irfan, M., Chen, L. et al. (2021) Role of core structural genes for flavonoid biosynthesis and transcriptional
factors in flower color of plants. Biotechnol. Biotechnol. Equip. 35, 1214–1229, https://doi.org/10.1080/13102818.2021.1960605
33 Sun, T., Rao, S., Zhou, X. and Li, L. (2022) Plant carotenoids: recent advances and future perspectives. Mol. Hortic. 2, 3,
https://doi.org/10.1186/s43897-022-00023-2
34 Liu, J., Osbourn, A. and Ma, P. (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8, 689–708,
https://doi.org/10.1016/j.molp.2015.03.012
35 Meng, Y., Wang, Z., Wang, Y., Wang, C., Zhu, B., Liu, H. et al. (2019) The MYB activator WHITE PETAL1 associates with MtTT8 and MtWD40-1 to
regulate carotenoid-derived flower pigmentation in medicago truncatula. Plant Cell. 31, 2751–2767, https://doi.org/10.1105/tpc.19.00480
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
13
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
36 Sagawa, J.M., Stanley, L.E., LaFountain, A.M., Frank, H.A., Liu, C. and Yuan, Y.W. (2016) An R2R3-MYB transcription factor regulates carotenoid
pigmentation in Mimulus lewisii flowers. New Phytol. 209, 1049–1057, https://doi.org/10.1111/nph.13647
37 Hatlestad, G.J., Akhavan, N.A., Sunnadeniya, R.M., Elam, L., Cargile, S., Hembd, A. et al. (2015) The beet Y locus encodes an anthocyanin MYB-like
protein that activates the betalain red pigment pathway. Nat. Genet. 47, 92–96, https://doi.org/10.1038/ng.3163
38 Hempel de Ibarra, N., Langridge, K.V. and Vorobyev, M. (2015) More than colour attraction: behavioural functions of flower patterns. Curr. Opin. Insect.
Sci. 12, 64–70, https://doi.org/10.1016/j.cois.2015.09.005
39 Papiorek, S., Junker, R.R., Alves-dos-Santos, I., Melo, G.A.R., Amaral-Neto, L.P. et al. (2016) Bees, birds and yellow flowers: pollinator-dependent
convergent evolution of UV patterns. Plant Biol. 18, 46–55, https://doi.org/10.1111/plb.12322
40 de Jager, M.L., Willis-Jones, E., Critchley, S. and Glover, B.J. (2017) The impact of floral spot and ring markings on pollinator foraging dynamics. Evol.
Ecol. 31, 193–204, https://doi.org/10.1007/s10682-016-9852-5
41 Lunau, K., Scaccabarozzi, D., Willing, L. and Dixon, K. (2021) A bee’s eye view of remarkable floral colour patterns in the south-west Australian
biodiversity hotspot revealed by false colour photography. Ann. Bot. 128, 821–824, https://doi.org/10.1093/aob/mcab088
42 Leonard, A.S., Brent, J., Papaj, D.R. and Dornhaus, A. (2013) Floral nectar guide patterns discourage nectar robbing by bumble bees. PLoS ONE 8,
e55914, https://doi.org/10.1371/journal.pone.0055914
43 Dafni, A., Bernhardt, P., Shmida, A., Ivri, Y., Greenbaum, S., O’Toole, C. et al. (1990) Red Bowl-spahed flowers: convergence for beetle pollination in
the mediterranean region. Isr. J. Plant Sci. 39, 81–92
44 Dafni, A., Lehrer, M. and Kevan, P.G. (1997) Spatial flower parameters and insect spatial vision. Biol. Rev. 72, 239–282,
https://doi.org/10.1017/S0006323196005002
45 Hirota, S.K., Miki, N., Yasumoto, A.A. and Yahara, T. (2019) UV bullseye contrast of Hemerocallis flowers attracts hawkmoths but not swallowtail
butterflies. Ecol. Evol. 9, 52–64, https://doi.org/10.1002/ece3.4604
46 Ding, B., Patterson, E.L., Holalu, S.V., Li, J., Johnson, G.A., Stanley, L.E. et al. (2020) Two MYB Proteins in a self-organizing activator-inhibitor system
produce spotted pigmentation patterns. Curr. Biol. 30, 802.e8–814.e8, https://doi.org/10.1016/j.cub.2019.12.067
47 Ma, X., Shi, J., Ba¨nziger, H., Sun, Y., Guo, Y., Liu, Z. et al. (2016) The functional significance of complex floral colour pattern in a food-deceptive orchid.
Funct. Ecol. 30, 721–732, https://doi.org/10.1111/1365-2435.12571
48 Ellis, A.G. and Johnson, S.D. (2010) Floral mimicry enhances pollen export: the evolution of pollination by sexual deceit outside of the orchidaceae.
Am. Nat. 176, E143–E151, https://doi.org/10.1086/656487
49 Johnson, S.D. and Dafni, A. (1998) Response of bee-flies to the shape and pattern of model flowers: implications for floral evolution in a
Mediterranean herb. Funct. Ecol. 12, 289–297, https://doi.org/10.1046/j.1365-2435.1998.00175.x
50 Van Kleunen, M., Na¨nni, I., Donaldson, J.S. and Manning, J.C. (2007) The role of beetle marks and flower colour on visitation by monkey beetles
(hopliini) in the greater cape floral region, South Africa. Ann. Bot. 100, 1483–1489, https://doi.org/10.1093/aob/mcm256
51 Whitney, H.M., Milne, G., Rands, S.A., Vignolini, S., Martin, C. and Glover, B.J. (2013) The influence of pigmentation patterning on bumblebee foraging
from flowers of Antirrhinum majus. Naturwissenschaften 100, 249–256, https://doi.org/10.1007/s00114-013-1020-y
52 Leonard, A.S. and Papaj, D.R. (2011) ‘X’ marks the spot: The possible benefits of nectar guides to bees and plants. Funct. Ecol. 25, 1293–1301,
https://doi.org/10.1111/j.1365-2435.2011.01885.x
53 Owen, C.R. and Bradshaw, H.D. (2011) Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod-Plant Interact. 5,
235, https://doi.org/10.1007/s11829-011-9133-8
54 Klomberg, Y., Dywou Kouede, R., Bartosˇ, M., Mertens, J.E.J., Tropek, R., Fokam, E.B. et al. (2019) The role of ultraviolet reflectance and pattern in the
pollination system of Hypoxis camerooniana (Hypoxidaceae). AoB PLANTS 11, plz057, https://doi.org/10.1093/aobpla/plz057
55 Tremblay, R.L. and Ackerman, J.D. (2007) Floral color patterns in a tropical orchid: Are they associated with reproductive success? Plant Species Biol.
22, 95–105, https://doi.org/10.1111/j.1442-1984.2007.00181.x
56 Koski, M.H. and Ashman, T.L. (2015) An altitudinal cline in UV floral pattern corresponds with a behavioral change of a generalist pollinator
assemblage. Ecology 96, 3343–3353, https://doi.org/10.1890/15-0242.1
57 Kurup, R., Johnson, A.J., Sankar, S., Hussain, A.A., Kumar, C.S. and Sabulal, B. (2013) Fluorescent prey traps in carnivorous plants. Plant Biol. 15,
611–615, https://doi.org/10.1111/j.1438-8677.2012.00709.x
58 Carney, C.L., Antonson, N., Alvarez, J., Foss, K., Kettler, K., Lloyd, A.J. et al. (2019) Fatal attraction: what is the role of visual cues in attracting prey to
carnivorous plants? BIOS 90, 79–86, https://doi.org/10.1893/0005-3155-90.2.79
59 Hatcher, C.R., Ryves, D.B. and Millett, J. (2020) The function of secondary metabolites in plant carnivory. Ann Bot 125, 399–411,
https://doi.org/10.1093/aob/mcz191
60 Heiling, A.M., Herberstein, M.E. and Chittka, L. (2003) Crab-spiders manipulate flower signals. Nature 421, 334–334,
https://doi.org/10.1038/421334a
61 Gronquist, M., Bezzerides, A., Attygalle, A., Meinwald, J., Eisner, M. and Eisner, T. (2001) Attractive and defensive functions of the ultraviolet pigments
of a flower (Hypericum calycinum). Proc. Natl. Acad. Sci. 98, 13745–13750, https://doi.org/10.1073/pnas.231471698
62 Niu, Y., Chen, G., Peng, D.L., Song, B., Yang, Y., Li, Z.M. et al. (2014) Grey leaves in an alpine plant: a cryptic colouration to avoid attack? New Phytol.
203, 953–963, https://doi.org/10.1111/nph.12834
63 Lev-Yadun, S. (2021) Avoiding rather than resisting herbivore attacks is often the first line of plant defence. Biol. J. Linn. Soc. 134, 775–802,
https://doi.org/10.1093/biolinnean/blab110
64 Lev-Yadun, S. and Ne’eman, G. (2012) Does bee or wasp mimicry by orchid flowers also deter herbivores? Arthropod-Plant Interact. 6, 327–332,
https://doi.org/10.1007/s11829-012-9199-y
65 de Castro, E´.C.P., Zagrobelny, M., Cardoso, M.Z. and Bak, S. (2018) The arms race between heliconiine butterflies and Passiflora plants - new insights
on an ancient subject. Biol. Rev. 93, 555–573, https://doi.org/10.1111/brv.12357
14 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
66 Lev-Yadun, S. (2016) Defensive (anti-herbivory) Coloration in Land Plants. Available from https://link.springer.com/book/10.1007/978-3-319-42096-7,
https://doi.org/10.1007/978-3-319-42096-7
67 Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T. et al. (2014) Enhancement of oxidative and drought
tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77, 367–379, https://doi.org/10.1111/tpj.12388
68 Nakabayashi, R., Mori, T. and Saito, K. (2014) Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal Behav.
9, e29518, https://doi.org/10.4161/psb.29518
69 Koski, M.H. and Ashman, T.L. (2016) Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic
factors. New Phytol. 211, 708–718, https://doi.org/10.1111/nph.13921
70 Uchiyama, T., Hiura, S., Ebinuma, I., Senda, M., Mikami, T., Martin, C. et al. (2013) A pair of transposons coordinately suppresses gene expression,
independent of pathways mediated by siRNA in Antirrhinum. New Phytol. 197, 431–440, https://doi.org/10.1111/nph.12041
71 Kuriyama, K., Tabara, M., Moriyama, H., Kanazawa, A., Koiwa, H., Takahashi, H. et al. (2020) Disturbance of floral colour pattern by activation of an
endogenous pararetrovirus, petunia vein clearing virus, in aged petunia plants. Plant J. 103, 497–511, https://doi.org/10.1111/tpj.14728
72 Kicheva, A. and Briscoe, J. (2015) Developmental Pattern Formation in Phases. Trends Cell Biol. 25, 579–591,
https://doi.org/10.1016/j.tcb.2015.07.006
73 Galipot, P., Damerval, C. and Jabbour, F. (2021) The seven ways eukaryotes produce repeated colour motifs on external tissues. Biol. Rev. 96,
1676–1693, https://doi.org/10.1111/brv.12720
74 Rogers, K.W. and Schier, A.F. (2011) Morphogen gradients: from generation to interpretation. Annu. Rev. Cell Dev. Biol. 27, 377–407,
https://doi.org/10.1146/annurev-cellbio-092910-154148
75 Vadde, B.V.L. and Roeder, A.H.K. (2020) Can the French flag and reaction-diffusion models explain flower patterning? Celebrating the 50th anniversary
of the French flag model. J. Exp. Bot. 71, 2886–2897, https://doi.org/10.1093/jxb/eraa065
76 Skopelitis, D.S., Benkovics, A.H., Husbands, A.Y. and Timmermans, M.C.P. (2017) Boundary formation through a direct threshold-based readout of
mobile small RNA gradients. Dev. Cell. 43, 265.e6–273.e6, https://doi.org/10.1016/j.devcel.2017.10.003
77 Czyzewicz, N., Yue, K., Beeckman, T. and Smet, I.D. (2013) Message in a bottle: small signalling peptide outputs during growth and development. J.
Exp. Bot. 64, 5281–5296, https://doi.org/10.1093/jxb/ert283
78 Benkova´, E., Ivanchenko, M.G., Friml, J., Shishkova, S. and Dubrovsky, J.G. (2009) A morphogenetic trigger: is there an emerging concept in plant
developmental biology? Trends Plant Sci. 14, 189–193, https://doi.org/10.1016/j.tplants.2009.01.006
79 Klesen, S., Hill, K. and Timmermans, M.C.P. (2020) Chapter Fifteen - Small RNAs as plant morphogens. In Current Topics in Developmental Biology
(Small, S. and Briscoe, J., eds), pp. 455–480, Academic Press, (Gradients and Tissue Patterning; vol. 137). Available from:
https://www.sciencedirect.com/science/article/pii/S0070215319300882
80 Ma¨ho¨nen, A.P., Tusscher, K., ten, Siligato, R., Smetana, O., Dı´az-Trivin˜o, S., Saloja¨rvi, J. et al. (2014) PLETHORA gradient formation mechanism
separates auxin responses. Nature 515, 125–129, https://doi.org/10.1038/nature13663
81 Krizek, B.A. and Eaddy, M. (2012) AINTEGUMENTA-LIKE6 regulates cellular differentiation in flowers. Plant Mol. Biol. 78, 199–209,
https://doi.org/10.1007/s11103-011-9844-3
82 Kawade, K., Tanimoto, H., Horiguchi, G. and Tsukaya, H. (2017) Spatially Different Tissue-Scale Diffusivity Shapes ANGUSTIFOLIA3 Gradient in
Growing Leaves. Biophys. J. 113, 1109–1120, https://doi.org/10.1016/j.bpj.2017.06.072
83 Kim, J.H. and Kende, H. (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc. Natl.
Acad. Sci. 101, 13374–13379, https://doi.org/10.1073/pnas.0405450101
84 Horiguchi, G., Kim, G.T. and Tsukaya, H. (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf
primordia of Arabidopsis thaliana. Plant J. 43, 68–78, https://doi.org/10.1111/j.1365-313X.2005.02429.x
85 Kondo, S. and Miura, T. (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616–1620,
https://doi.org/10.1126/science.1179047
86 Green, J.B.A. and Sharpe, J. (2015) Positional information and reaction-diffusion: two big ideas in developmental biology combine. Development 142,
1203–1211, https://doi.org/10.1242/dev.114991
87 Turing, A.M. (1952) The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 237, 37–72,
https://doi.org/10.1098/rstb.1952.0012
88 Gierer, A. and Meinhardt, H. (1972) A theory of biological pattern formation. Kybernetik 12, 30–39, https://doi.org/10.1007/BF00289234
89 Ringham, L., Owens, A., Cieslak, M., Harder, L.D. and Prusinkiewicz, P. (2021) Modeling flower pigmentation patterns. ACM Trans. Graph. TOG 40,
1–14, https://doi.org/10.1145/3478513.3480548
90 Bhati, A.P., Goyal, S., Yadav, R. and Sathyamurthy, N. (2021) Pattern formation in Passiflora incarnata: an activator-inhibitor model. J. Biosci. 46, 84,
https://doi.org/10.1007/s12038-021-00202-1
91 Cavallini-Speisser, Q., Morel, P. and Monniaux, M. (2021) Petal cellular identities. Front. Plant Sci. 12, 745507,
https://doi.org/10.3389/fpls.2021.745507
92 Riglet, L., Gatti, S. and Moyroud, E. (2021) Sculpting the surface: structural patterning of plant epidermis. iScience 24, 103346,
https://doi.org/10.1016/j.isci.2021.103346
93 Moyroud, E., Wenzel, T., Middleton, R., Rudall, P.J., Banks, H., Reed, A. et al. (2017) Disorder in convergent floral nanostructures enhances signalling
to bees. Nature 550, 469–474, https://doi.org/10.1038/nature24285
94 Wilts, B.D., Rudall, P.J., Moyroud, E., Gregory, T., Ogawa, Y., Vignolini, S. et al. (2018) Ultrastructure and optics of the prism-like petal epidermal cells
of Eschscholzia californica (California poppy). New Phytol. 219, 1124–1133, https://doi.org/10.1111/nph.15229
95 Noda, K., ichi, Glover, B.J., Linstead, P. and Martin, C. (1994) Flower colour intensity depends on specialized cell shape controlled by a Myb-related
transcription factor. Nature 369, 661–664, https://doi.org/10.1038/369661a0
© 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
15
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022
Essays in Biochemistry (2022) EBC20220051
https://doi.org/10.1042/EBC20220051
96 Stavenga, D.G., Staal, M. and van der Kooi, C.J. (2020) Conical epidermal cells cause velvety colouration and enhanced patterning in Mandevilla
flowers. Faraday Discuss. 223, 98–106, https://doi.org/10.1039/D0FD00055H
97 van der Kooi, C.J., Elzenga, J.T.M., Dijksterhuis, J. and Stavenga, D.G. (2017) Functional optics of glossy buttercup flowers. J. R. Soc. Interface 14,
20160933, https://doi.org/10.1098/rsif.2016.0933
98 Lin, R.C. and Rausher, M.D. (2021) R2R3-MYB genes control petal pigmentation patterning in Clarkia gracilis ssp. sonomensis (Onagraceae). New
Phytol. 229, 1147–1162, https://doi.org/10.1111/nph.16908
99 Lin, R.C. and Rausher, M.D. (2021) Ancient gene duplications, rather than polyploidization, facilitate diversification of petal pigmentation patterns in
Clarkia gracilis (Onagraceae). Mol. Biol. Evol. 38, 5528–5538, https://doi.org/10.1093/molbev/msab242
100 Bradley, D., Xu, P., Mohorianu, I.I., Whibley, A., Field, D., Tavares, H. et al. (2017) Evolution of flower color pattern through selection on regulatory
small RNAs. Science 358, 925–928, https://doi.org/10.1126/science.aao3526
101 Goethe, J.W. (1790) Versuch die Metamorphose der Pflanzen zu erkla¨ren, Gotha, C.W. Ettinger
102 Albert, N.W., Griffiths, A.G., Cousins, G.R., Verry, I.M. and Williams, W.M. (2015) Anthocyanin leaf markings are regulated by a family of R2R3-MYB
genes in the genus Trifolium. New Phytol. 205, 882–893, https://doi.org/10.1111/nph.13100
103 Wang, C., Ji, W., Liu, Y., Zhou, P., Meng, Y., Zhang, P. et al. (2021) The antagonistic MYB paralogs RH1 and RH2 govern anthocyanin leaf markings in
Medicago truncatula. New Phytol. 229, 3330–3344, https://doi.org/10.1111/nph.17097
104 Sarvepalli, K., Das Gupta, M., Challa, K.R. and Nath, U. (2019) Molecular cartography of leaf development — role of transcription factors. Curr. Opin.
Plant Biol. 47, 22–31, https://doi.org/10.1016/j.pbi.2018.08.002
105 Richardson, A.E. and Hake, S. (2019) Drawing a line: grasses and boundaries. Plants 8, 4, https://doi.org/10.3390/plants8010004
106 Sheehan, H., Moser, M., Klahre, U., Esfeld, K., Dell’Olivo, A., Mandel, T. et al. (2016) MYB-FL controls gain and loss of floral UV absorbance, a key trait
affecting pollinator preference and reproductive isolation. Nat. Genet. 48, 159–166, https://doi.org/10.1038/ng.3462
107 Borghi, M., Fernie, A.R., Schiestl, F.P. and Bouwmeester, H.J. (2017) The Sexual advantage of looking, smelling, and tasting good: the metabolic
network that produces signals for pollinators. Trends Plant Sci. 22, 338–350, https://doi.org/10.1016/j.tplants.2016.12.009
108 Trunschke, J., Lunau, K., Pyke, G.H., Ren, Z.X. and Wang, H. (2021) Flower color evolution and the evidence of pollinator-mediated selection. Front
Plant Sci. 12, 617851, https://doi.org/10.3389/fpls.2021.617851
16 © 2022 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons
Attribution License 4.0 (CC BY).
D
ow
nloaded from
 http://portlandpress.com
/essaysbiochem
/article-pdf/doi/10.1042/EBC
20220051/938097/ebc-2022-0051c.pdf by U
niversity of C
am
bridge user on 28 N
ovem
ber 2022