Current Biology
Dispatches
trials and those who were smaller in body
size. There was a clear cost to moving up
into the shrubs to avoid predators:
females from islands with predators were
in poorer condition (weighed less relative
to their length) than females from islands
without predators.
How did selection act on morphology
and behavior? First, while each aspect of
behavior and morphology was under
selection, selection acted independently
on them. There was no indication that the
value of an individual’s behavior
depended upon its morphology or vice-
versa. Second, the strength of selection
on behavior and morphology depended
heavily on context. On islands without
predators, 13.9% of the variation in
survival was attributable to behavior
(shorter lag before exploration) and 19.1%
to morphology (longer legs). On islands
with predators, 22.5 % of the variation is
attributable to behavior (avoidance of the
ground) but only 9.8% was attributable to
morphology (smaller body size).
Why is the work of Lapiedra et al. [3]
important? For one reason, the work
described here was a well-controlled
experiment in nature with statistical
controls for what the authors could not
equalize. For example, some of the
A. sagrei used in the experiment came
from islands with Leiocephalus and others
did not. The authors were able to show
Development: Cell Polarity Is Coordinated
over an Entire Plant Leaf
Joseph Cammarata and Adrienne H.K. Roeder*
Weill Institute for Cell and Molecular Biology and School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca,
NY, USA
*Correspondence: ahr75@cornell.edu
https://doi.org/10.1016/j.cub.2018.07.007
Models of leaf development have long predicted the existence of an organ-wide polarity field. Now, a robust
analysis in a developing Arabidopsis leaf reveals the presence of a general and persistent cell polarity
coordinated over the entire leaf.
In the spring, leaves burst forth with
diverse shapes and sizes. These leaves
can be compound with many leaflets, like
those of a tomato, or simple and smooth,
R884 Current Biology 28, R871–R894, August 20, 2018 ª 2018 Elsevier Ltd.
that the island of origin had no effect on
the results. For another, the authors’ show
that the effects of behavior on survival
were a function of individual differences,
not momentary behavioral decisions.
They did so because they performed their
assay of behavior before the experiment
was initiated and showed that the
behavioral differences among individuals
were repeatable.
Taken together, these virtues reveal the
importance of looking at the dynamics of
selection, rather than just the end product.
The dynamics revealed that selection on
behavior and morphology were
statistically independent of one another.
The end product, which is what prior
studies have examined, would have
shown that behavior and morphology
evolved together, which would have led
naturally to the conclusion that the
evolution of behavior either buffered (in the
presence of predators) or accelerated (in
the absence of predators) morphological
evolution. This new study reveals instead
that behavior and morphology are different
features of the phenotype that can be
selected independently of one another.
REFERENCES
1. Wcislo, W.T. (1989). Behavioral environments
and evolutionary change. Annu. Rev. Ecol.
Syst. 20, 137–169.
like those of a lilac. These diverse plant
forms are thought to be made by tuning
or variably applying developmental
mechanisms that are common across
2. Mayr, E. (1963). Animal Species and Evolution
(Cambridge, MA: Belknap Press of Harvard
University).
3. Lapiedra, O., Schoener, T.W., Leal, M., Losos,
J.B., and Kolbe, J.J. (2018). Predator-driven
natural selection on risk-taking behavior
in anole lizards. Science 360, 1017–1020.
4. Huizinga, M., Ghalambor, C.K., and Reznick,
D.N. (2009). The genetic and environmental
basis of adaptive differences in shoaling
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5. McGhee, K.E., and Travis, J. (2011). Early food
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6. Fraser, B.A., Janowitz, I., Thairu, M., Travis, J.,
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7. Brodie, E.D. (1992). Correlational selection for
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8. Huey, R.B., Hertz, P.E., and Sinervo, B. (2003).
Behavioral drive versus behavioral inertia in
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161, 357–366.
9. Munoz, M.M., and Losos, J.B. (2018).
Thermoregulatory behavior simultaneously
promotes and forestalls evolution in a tropical
lizard. Am. Nat. 191, E15–E26.
10. Losos, J.B., Warheit, K.I., and Schoener, T.W.
(1997). Adaptive differentiation following
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lizards. Nature 387, 70–73.
plants [1–4]. Studying how these
mechanisms can be tweaked to generate
diverse leaf forms raises an even greater
question: how does any organ reliably
Current Biology
Dispatches
acquire a genetically encoded
morphology starting from only a few
cells?
Several plausible models for how
leaves modulate their growth to attain
specific shapes have been proposed.
Some focus largely on the periodic
placement of vasculature, determined at
the expanding leaf margin. If these points
of vascular origin have the highest
growth rate, and tissue between
vasculature has lower growth rates, then
models can generate many realistic leaf
shapes by varying the frequency or
spacing of veins [3]. Other models have
proposed that different leaf shapes can
be attained by modulating tissue growth
relative to a polarity field within the leaf
[5,6]. In these models, growth rates can
be further modified by position or time in
development. For example, in the
Growing Polarized Tissue framework
model, a chemical or protein gradient
from the base of the organ could
establish a longitudinal axis on the
growing organ [5]. Cells would then
expand or divide anisotropically using
this axis as a reference, and local signals
emanating from the leaf tip or midrib
could refine different longitudinal or
lateral expansion rates of cells in
different zones [6] (Figure 1A). Adjusting
the polarity field, regulatory regions
defined by gradients, and growth
parameters in these models can
produce leaves and petals with realistic
clonal sectors and three-dimensional
shapes [7–9]. These theoretical models
postulate a persistent polarity field
existing across the organ and throughout
leaf development; however, direct
evidence for such a polarity field has
been lacking.
In this issue of Current Biology,
Mansfield et al. demonstrate that growing
leaves of Arabidopsis thaliana possess a
persistent tissue-wide cell polarity field as
predicted by the models [10]. As a tool to
detect cell polarity, they turn to the
protein BREAKING of ASYMMETRY IN
THE STOMATAL LINEAGE (BASL).
During the development of stomata (small
pores on leaves to facilitate gas
exchange), a transient stem cell is
established, makes several asymmetric
cell divisions, and then divides
symmetrically to produce two guard cells
flanking the stoma. During each
asymmetric division, BASL localizes to a
crescent at one corner of the mother cell
such that it is inherited by one daughter
cell. The cell that inherits BASL then
differentiates into a pavement cell, while
the daughter cell that does not continues
on as a transient stem cell [11,12].
Although BASL is normally only
expressed in stomatal lineage cells, it
also polarly localizes if expressed
ectopically [10,11]. Using an inducible
BASL:GFP line ectopically expressed
throughout the leaf epidermis (of a spch
mutant [13] with no stomata so that
stomatal lineage cells did not obscure the
analysis), Mansfield et al. clearly
demonstrated that BASL localized
preferentially to a single proximal lobe of
puzzle piece-shaped epidermal
pavement cells throughout the epidermis
of the leaf (Figure 1B).
In addition to this exciting evidence for
an organ-wide polarity field, the authors
show that BASL polarity is reversed in the
distal edge of leaf serrations, where the
polar localization of the PIN1 auxin efflux
transporter is also reversed (Figure 1C).
By examining the localization of BASL
together with PIN1 the authors find that
BASL localizes opposite PIN1 both in
young expanding leaves and in
serrations. This implies that the ‘proximal
molecular address’ to which BASL
localizes is part of a more broadly present
polarity machinery. Additionally, whereas
PIN1 expression usually diminishes after
early leaf development, the continued
polarity of BASL indicates that this
polarity machinery is still present,
suggesting that PIN1 establishes or taps
into a more general cell polarity
mechanism revealed by ectopic BASL
expression.
The discovery of a persistent, tissue-
wide polarity field is crucial to our
understanding of development and
raises many questions for future
research. Chief among these is the
question of how the polarity field is
generated. One plausible mechanism
unifying both PIN and BASL polarity, and
thus the polarity field in general, is
mechanical stress. Bringmann et al.
demonstrated that the localization of
BREVIS RADIX LIKE2 (BRXL2), which is
also polarly localized and functions in
concert with BASL in the stomatal
lineage, can be altered by applying
mechanical stress to a cotyledon or by
manipulation of the local mechanical
Current Biology 28, R871–R894, August 20, 2018 R885
A
Convergent polarity field model
Proximodistal patterning
signal
Growth response to
polarity field varies based
on signals from tip, midrib,
or base
B Tissue-wide proximal localization of BASL
demonstrated by Mansfield et al.
Polarity reversal at serrations
C
Polarity reversal
Growth
PIN1 auxin efflux carrier
BASL
Current Biology
Figure 1. BASL localization reflects
predicted patterns of tissue-wide cell
polarity.
(A) Models predicting a proximodistal polarity field
converging at the tip that patterns growth in
a region-specific manner can generate realistic
organ shapes. Proximodistal patterning here is
represented by a gradient, but it can also be
established by polar cell–cell interactions. (B) In
this issue of Current Biology, Mansfield et al. [10]
use ectopic expression of GFP-tagged BASL
(green crescent) to reveal the existence of a
persistent, tissue-wide polarity field. Throughout
the leaf, BASL localized to a proximal lobe of the
puzzle-shaped pavement cells, except at
serrations. (C) Cell polarity, reflected both by
PIN1 (blue crescent) and BASL localizations,
reverses distal to emerging leaf serrations.
environment with laser ablations [14].
Growth-derived stresses are also
thought to orient PIN1 polarity [15]. It is
possible that mechanical axial
information is paired with other tissue-
organizing mechanisms, such as the
presence of a tissue-scale polarity
organizer.
In Drosophila, a similar tissue-wide cell
polarity field generated by the planar cell
polarity (PCP) machinery functions in
various developmental processes [16].
 Current Biology

Dispatches

A
Developing epidermal cell

Necessary for polarity field?

Anisotropic growth
Depolymerize microtubules for MT-mediated vesicular trafficking
two days during development Oryzalin
MT-mediated stress sensing

BASL

B
Developing leaf

Loss of serrations
Inhibition of PIN activity
Block polar auxin transport NPA
Proximal BASL localization remains
during early leaf development

Current Biology

Figure 2. Proximal localization of BASL is robust to loss of microtubules and polar auxin transport during development.
(A) Long-term depolymerization of microtubules by treatment with oryzalin for two days did not alter proximal BASL localization, despite altering cell growth,
endomembrane trafficking, and mechanics. (B) While PIN polarity and the polar auxin transport it mediates are promising candidates for polarity field
organizers, inhibition of PIN activity by NPA does not disrupt the general polarity field, although it does prevent normal serration growth.

Models predict that PCP, and polarity
fields more broadly, can arise from
systems with three main properties [17].
First, the cells must themselves become
polarized. This can occur by a process
called intracellular partitioning, whereby
each pole of the cell is enriched for factors
that both auto-activate and inhibit factors
from the other pole. Second, through cell–
cell coupling, the polarity of each cell can
be propagated along a longitudinal axis.
Finally, lateral coordination (between
ranks of cells coordinated through cell–
cell coupling) is achieved by basins of
polarity attraction or repulsion — polarity
organizers.
Cell–cell coupling in Drosophila is
thought to occur through direct
intercellular interactions of
transmembrane polarity proteins [16].
In plant tissues, where cell walls
substantially separate the plasma
membranes of adjacent cells, such
direct interactions are harder to imagine.
It has been previously shown that cell–
cell coupling can be indirectly achieved
by a diffusible chemical signal that is
asymmetrically pumped out of cells, and
that can inhibit the activity of these
pumps [18]. In plants, the system best
resembling this theoretical coupling
mechanism is auxin transport by
polarized PIN proteins, although the
control of PIN localization appears more
complex than the theoretical indirect
coupling mechanism, and the proposed
autoinhibitory action has not been
demonstrated.
PIN1 expression in leaves is transient,
while the polarity field found by
Mansfield et al. persists, suggesting that
if PIN1 plays a role in establishing
tissue-wide polarity, something else
must act to maintain it. Even if PIN
proteins do mediate cell–cell coupling,
the other two requirements for organized
tissue-wide polarity (intracellular
partitioning and polarity organizers) are
still unaccounted for. Evidence for
intracellular partitioning is lacking. The
localization of BASL in pavement cells
does not appear to reflect an interaction
with such a specific partitioning
mechanism, as BASL expressed in other
tissues can localize with PIN1 rather
than away from it [11]. Genetics
and modeling have identified some
potential polarity organizers, such as
the transcription factor CUC2 [6,19].
Experiments in which these candidates
are expressed in sectors of developing
organs, possibly in conjunction with the
ectopic BASL line used by Mansfield
et al., will be pivotal for determining
whether these genes are sufficient to
locally reorient polarity.
Indeed, it will be interesting to see
whether the polarity field can even be
reoriented once established. Attempts
by Mansfield et al. thus far to alter the
proximal polarity of BASL by disrupting
microtubule stability (with oryzalin) or
auxin trafficking (with NPA) during leaf
development have left the polarity field
surprisingly intact (Figure 2) [10]. These
results were especially fascinating, as
oryzalin application was sustained for
multiple days — long enough to disrupt
not only intracellular trafficking, but cell
shape and intercellular mechanics as well.
Overall, not only have Mansfield et al.
revealed the existence of a long-
predicted organ-scale polarity field in
Arabidopsis, but they have also provided
a key tool that will be needed to further
dissect and understand how this polarity
field is established.
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Thermal Biology: Melanin-Based Energy Harvesting
across the Tree of Life
Stefan Pinkert1,2,* and Dirk Zeuss3
1Department
of Ecology – Animal Ecology, Philipps-Universita
2Department of Biodiversity and Species Conservation, University of Applied Sciences Erfurt, 99085 Erfurt, Germany
3Department of Zoology, Stockholm University, 10691 Stockholm, Sweden
*Correspondence: stefanpinkert@posteo.de
https://doi.org/10.1016/j.cub.2018.07.026
Recent results on the thermal biology of unicellular fungi provide evidence that pigmentation is an ancient
adaptation for harvesting solar radiation. A new model system promises novel opportunities for
quantifying radiative heat transfer and improving biophysical models.
Most children love chocolate ice cream
but are dismayed to learn that this frozen
delight melts faster than the lighter-
colored vanilla ice cream under the hot
summer sun. Indisputably more alarming
is the recognition that Greenland’s ice
sheet is melting more rapidly than
hitherto predicted. A dark film of
microorganisms and dust that covers a
considerable part of its surface (Figure 1)
control of organ shape and tissue polarity.
PLoS Biol. 8, e1000537.
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Sablowski, R., and Coen, E. (2013). JAGGED
controls arabidopsis petal growth and shape
by interacting with a divergent polarity field.
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Tissue-wide mechanical forces influence the
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€t Marburg, 35043 Marburg, Germany
is to blame for the higher melting rate [1].
Such observations intuitively suggest
that the dark pigmentation (melanism) of
organisms is an adaptation to cold
environments, where darker-colored
species absorb more solar radiation and
benefit from higher heating rates, which
leads to higher overall body
temperatures [2]. By contrast, lighter-
colored species in warm environments
Current Biology 28, R871–R894, August 20, 2018 ª 2018 Elsevier Ltd. R887
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should benefit from enhanced reflection
of radiation and hence a reduced risk of
overheating. Textbook examples of
organisms using this mechanism—called
thermal melanism—for harvesting solar
radiation include butterflies, dragonflies,
and reptiles, which often bask in the sun
while at rest [3]. The theory of thermal
melanism dates back to the first half of
the last century [2] but has only recently