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study will undoubtedly motivate careful
scrutiny of foveal and parafoveal visual
processing, and the associated
oculomotor activity, in a wide range
of behavioral and neurophysiological
investigations.
References
1. Ahissar, E., and Arieli, A. (2012). Seeing via
miniature eye movements: a dynamic
hypothesis for vision. Front. Comput. Neurosci.
6, 89.
2. Kuang, X., Poletti, M., Victor, J.D., and
Rucci, M. (2012). Temporal encoding of spatial
information during active visual fixation.
Curr. Biol. 22, 510–514.
3. Rucci, M., Iovin, R., Poletti, M., and Santini, F.
(2007). Miniature eye movements enhance fine
spatial detail. Nature 447, 852–855.
4. Collewijn, H., and Kowler, E. (2008). The
significance of microsaccades for vision and
oculomotor control. J. Vis. 8, 1–21.
5. Rolfs, M. (2009). Microsaccades: small steps on
a long way. Vision Res. 49, 2415–2441.
6. Hafed, Z.M. (2011). Mechanisms for generating
and compensating for the smallest possible
saccades. Eur. J. Neurosci. 33, 2101–2113.
7. Poletti, M., Listorti, C., and Rucci, M. (2013).
Microscopic eye movements compensate for
Carnivorous Plants: Trapping,
Digesting and Absorbing All in One
The Venus flytrap digests and absorbs its prey, but how does it coordinate
digestion and absorption to maximise the efficiency of this highly evolved
mechanism? A new study that combines direct recordings from cells within
the trap along with molecular characterization of nutrient transport reveals
a complex and coordinated suite of mechanisms that underlie this elegant
process.
Colin Brownlee
The ability to catch and digest insects
allows insectivorous plants to acquire
nitrogen and other nutrients in very low
nutrient habitats. Since the landmark
studies of Charles Darwin [1], the Venus
flytrap (Dionaea muscipula) has
provided a source of fascination and
is now one of the most commonly
cultivated house plants. It also
provides a unique model for the
study of mechanosensing and the
physiological and structural processes
underlying rapid plant movements. The
Venus flytrap is a remarkable example
of adaptive evolution. Its leaves are
modified to form trap organs that have
the unique ability to snap shut and trap
a fly or other small creature that may
accidentally touch one of the trigger
hair cells located on the inner surface
of the trap. The inner surface of the trap
nonhomogeneous vision within the fovea. Curr.
Biol. 23, 1691–1695.
8. Hafed, Z.M., Goffart, L., and Krauzlis, R.J.
(2009). A neural mechanism for microsaccade
generation in the primate superior colliculus.
Science 323, 940–943.
9. Hafed, Z.M., and Krauzlis, R.J. (2012). Similarity
of superior colliculus involvement in
microsaccade and saccade generation.
J. Neurophysiol. 107, 1904–1916.
10. Kagan, I., Gur, M., and Snodderly, D.M. (2008).
Saccades and drifts differentially modulate
neuronal activity in V1: Effects of retinal image
motion, position, and extraretinal influences.
J. Vis. 8, 1–19.
11. Hafed, Z.M. (2013). Alteration of visual
perception prior to microsaccades. Neuron 77,
775–786.
12. Engbert, R., and Kliegl, R. (2003).
Microsaccades uncover the orientation of
covert attention. Vision Res. 43, 1035–1045.
13. Hafed, Z.M., and Clark, J.J. (2002).
Microsaccades as an overt measure of covert
attention shifts. Vision Res. 42, 2533–2545.
14. Ko, H.-K., Poletti, M., and Rucci, M. (2010).
Microsaccades precisely relocate gaze in a
high visual acuity task. Nat. Neurosci. 13,
1549–1553.
15. Kowler, E., and Collewijn, H. (2010). The eye on
the needle. Nat. Neurosci. 13, 1443–1444.
16. McCamy, M.B., Otero-Millan, J., Macknik, S.L.,
Yang, Y., Troncoso, X.G., Baer, S.M.,
is also lined with secretory gland cells
that are stimulated to produce lytic
enzymes following closure of the trap
[2]. The immediate and rapid snapping
shut of the trap is a perfect
demonstration of a sensory-motor
system that involves neither nerves
nor muscles. It has been known for
some time that the mechanism
underlying the closure of the trap
involves the generation of very fast
electrical depolarizations in the form
of action potentials by the cells of
the trigger hairs which lead to the
rapid closure of the trap [3]. Rapid
closure is brought about by a
combination of elastic properties
and biochemical/biophysical changes
in the motor cells [4]. However,
unlike animal neuronal action
potentials in which Na+/Ca2+ ions
carry the depolarizing phase of
the action potential, the rapid
Crook, S.M., and Martinez-Conde, S. (2012).
Microsaccadic efficacy and contribution to
foveal and peripheral vision. J. Neurosci. 32,
9194–9204.
17. Kagan, I. (2012). Microsaccades and image
fading during natural vision. Electronic
response to McCamy et al. Microsaccadic
efficacy and contribution to foveal and
peripheral vision. J. Neurosci. 32, 9194–9204.
18. Poletti, M., and Rucci, M. (2010). Eye
movements under various conditions of image
fading. J. Vis. 10, 1–18.
19. Chen, C.-Y., and Hafed, Z.M. (2013).
Postmicrosaccadic enhancement of slow eye
movements. J. Neurosci. 33, 5375–5386.
20. Snodderly, D.M., Kagan, I., and Gur, M. (2001).
Selective activation of visual cortex neurons
by fixational eye movements: implications
for neural coding. Vis. Neurosci. 18,
259–277.
1German Primate Center, Kellnerweg 4,
37077 Goettingen, Germany. 2Werner
Reichardt Centre for Integrative
Neuroscience, Otfried-Mueller Str. 25,
72076 Tuebingen, Germany.
E-mail: ikagan@dpz.eu
http://dx.doi.org/10.1016/j.cub.2013.07.038
depolarization component of the
Venus flytrap action potential is most
likely brought about by the opening of
rapid (R-type) anion channels [5] since
plants lack the voltage-sensitive cation
channels that characterise animal
excitability [6].
How these initial signalling events
link with the later events that occur
following closure of the trap has been
less clear. The paper by Scherzer et al.
in this issue of Current Biology [7]
provides new information that allows
us to understand how digestion of
prey and absorption of nutrients
following trap closure are facilitated
and regulated. In an earlier study by
the same group, Escalante-Perez
and co-workers [5] demonstrated
that sealing of the trap and
formation of the ‘external stomach’
was under the regulation of two plant
hormones, abscisic acid (ABA) and
12-oxo-phytodienoic acid (OPDA).
OPDA is a precursor of jasmonic acid
and was shown to trigger secretion
by gland cells as well as making traps
more sensitive to mechanical
stimulation and promoting long-term
trap closure (a requirement for
digestion). The jasmonic acid
mimic coronatine (COR) was also
able to induce secretion. ABA was
shown to counter the stimulatory
effects of OPDA by making traps less
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sensitive to mechanical stimulation.
However, ABA did not affect
OPDA-stimulated gland activity,
suggesting that separate signalling
pathways operate for trap closure and
secretion.
To probe the regulation of digestion
and nutrient absorption Scherzer et al.
[7] set out to identify the major
products of digestion in the flytrap.
By treating insect powder with trap
digestive fluid they showed that the
lytic enzymes produced by the
secretory gland cells give rise to a
complex mixture of amino acids
but also that ammonium (NH4+) is
a major product of digestion.
Further analysis of the amino acid
products of digestion suggests that a
glutamine deaminase may be primarily
responsible for NH4+ production. Using
15
NH4+ they also showed that glands
had the capacity to take up NH4+. An
elegant set of experiments employing
electrophysiological measurements
from single gland cells in intact plants
showed that the membrane potential
depolarised when NH4+ was added.
Significantly, in glands that had not
been activated and were not
undergoing the process of digestion,
NH4+ had little effect on membrane
potential. The authors conclude that
competence to transport NH4+ is linked
to digestion. Although the digestive
fluid has a low pH, the authors showed
that NH4+ uptake was more or less
independent of pH, suggesting that
it was not being driven by the H+
electrochemical gradient across the
secretory cell membrane.
Searching a D. muscipula EST
collection [8] revealed a homologue
of type 1 NH4+ transporters, DmAMT1.
This transporter bears sequence
similarities to plant and animal AMTs
and phylogenetic analysis showed
that the DmAMT1 gene bridges a
gap between animal AMTs and those
from other kingdoms, including
bacteria [7]. In plants, AMTs are
primarily involved with NH4+ uptake
by roots. However, consistent with a
possible role in NH4+ uptake by trap
lobes, DmAMT1 showed enhanced
expression in traps, and in gland cells
in particular. DmAMT1 expression
could also be increased by application
of COR. Scherzer et al. [7] have
cloned DmAMT1 and characterised
it by expression in Xenopus oocytes
and examining its physiological
properties by using voltage clamp
approaches. In these studies they
Acidification
1
5
Digestive
H+ NH4+
juices
Trigger hair
4
JA
COI1 Ca2+
Action
potentials 3
DmAMT1
2
Secretory cell
ABA JA
Trap closure
and sealing
Current Biology
Figure 1. Coordination of trap closure, secretion and NH4+ uptake in the Venus flytrap.
Schematic of the proposed integration of processes underlying prey capture, digestions and
absorption in the Venus flytrap. Mechanosensing by the trap sensory hairs (1) gives rise
to action potentials that lead to trap closure and sealing that involve jasmonic acid (JA)
and ABA (2). Separate activation of jasmonate receptor COI1 (3) along with transient Ca2+
elevations in the gland secretory cells leads to stimulation of digestive enzyme secretion
into the sealed trap (4). Expression of DmAMT1 facilitates increased NH4+ absorption. Parallel
H+ secretion ensures trap acidification and charge balance during NH4+ uptake (5).
confirm that DmAMT1 behaves as The report by Scherzer et al. [7] also
an NH4+ transporter with kinetic allows mechanistic links to be made
and biochemical properties of an between digestion, NH4+ absorption
ion-selective channel that behaves as and trap acidification. It has been
a voltage-dependent high-affinity known for some time that acidification
NH4+ transporter optimised for NH4+ of the trap depends on the presence of
uptake at the membrane potential of prey or elicitor [10]. Scherzer et al. [7]
gland cells. Interestingly, the speculate that NH4+ induces H+ release
recruitment of AMT transporters to into the trap, presumably through the
bring about NH4+ transport by gland activity of a plasma membrane-located
cells seems to be a feature of other H+-ATPase. H+ release would thus
insectivorous plants since the pitcher serve to counter the depolarising
plant (Nepenthes alata) has also been effects of electrogenic NH4+ uptake
shown to express an NH4+ transporter, and help to maintain intracellular
NaAMT1, in its digestive gland pH homeostasis. At the same time,
cells [9]. progressive acidification of the trap
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digestive fluid will allow optimal
digestion of a wide range of protein
and other substrates.
From this and other work on the
Venus flytrap, it is possible to begin to
build a picture of the coordination of
processes leading from fast sensory
perception of touch to digestion and
absorption of nutrients (Figure 1).
This study also broadens our
knowledge of nutrient transport, and
NH4+ transport in particular, from both
functional and evolutionary
perspectives. A number of important
questions remain: What happens to
the NH4+ that is absorbed by the trap
cells? Is it processed by these cells or
transported to other cell types for
processing? What are the similarities
and differences between this NH4+
transport system and those from plant
roots? How are other nutrients (e.g. P,
Fe) dealt with? What other signals are
involved in the coordination of these
complex processes? The continued
Speed Control: Spinal Interneurons
with Crossed Purposes
A recent study has revealed that different populations of commissural spinal
interneurons ensure limb alternation at different speeds of locomotion.
Evdokia Menelaou
and David L. McLean
While every journey begins with a
single step, it is the subsequent
alternating ones that make the trip
possible. Our current understanding of
how this is achieved in limbed animals
was first articulated over a century ago
[1,2]. In his ‘half-center’ hypothesis,
Thomas Graham Brown predicted that
networks of neurons in the spinal cord
would be organized antagonistically,
like the muscles and limbs they control.
A recent study by Talpalar et al. [3] has
now identified fundamental crossing,
or commissural, components of the
hindlimb ‘half-centers’ and revealed
surprising differences in their
contribution to left–right alternation
depending on how fast the animal is
trying to move.
Mice, like many tetrapods, move over
a range of speeds using alternating
gaits. Left–right hindlimb (and forelimb)
application of single-cell and
whole-organ physiology and
biochemistry along with genome
sequencing and functional genomics
approaches will ensure that these and
other questions continue to be
addressed.
References
1. Darwin, C. (1875). Insectivorous Plants
(New York, NY, USA: D Appleton & Co.).
2. Robins, R.J., and Juniper, B.E. (1979). The
secretory cycle of Dionaea muscipula Ellis. I.
The fine structure and the effect of
stimulation on the fine structure of the
digestive gland cells. New Phytol. 86,
279–296.
3. Volkov, A.G., Tejumade, A., Markin, V.S., and
Jovanov, E. (2008). Kinetics and mechanism of
Dionaea muscipula trap closing. Plant Physiol.
146, 694–702.
4. Forterre, Y., Skotheim, J.M., Dumais, J., and
Mahadevan, L. (2005). How the Venus flytrap
snaps. Nature 433, 421–425.
5. Escelante-Perez, M., Krol, E., stange, A.,
Geiger, D., Al-Rasheid, K.A.S., Hause, B.,
Neher, E., and Hedrich, R. (2011). A special pair
of phytohormones controls excitability, slow
closure and external stomach formation in the
Venus flytrap. Proc. Natl. Acad. Sci. USA 108,
15492–15497.
alternation requires that flexors on one
side of the body are silent as those on
the other side are active. The same is
true for extensors. This pattern is
reinforced by mutual antagonism
between flexors and extensors on the
same side of the body. To examine the
circuit basis for left–right alternation,
Talpalar et al. [3] focused on a single
genetically identified population of
cells that are known to have
commissural processes. So-called V0
neurons arise from the p0 progenitor
domain, and contain both excitatory
(glutamate/acetylcholine) and
inhibitory (GABA/glycine)
subpopulations [4,5]. While all V0
neurons are defined by the expression
of the Dbx1 transcription factor in
progenitor cells, the V0 population can
be subdivided into Pax7-derived dorsal
(V0D) inhibitory and Pax7-negative
ventral (V0v) excitatory subgroups
(Figure 1A). Talpalar et al. [3] took
advantage of these differences in
6. Wheeler, G.L., and Brownlee, C. (2008).
Calcium signalling in plants and green algae:
changing channels. Trends Plant Sci. 13,
506–514.
7. Scherzer, S., Krol, E., Kreuzer, I., Kruse, J.,
Karl, F., von Rüden, M., Escalante-Perez, M.,
Müller, T., Rennenberg, H., Al-Rasheid, K.A.S.,
et al. (2013). The Dionaea muscipula
ammonium channel DmAMT1 provides NH4+
uptake associated with Venus flytrap’s prey
digestion. Curr. Biol. 23, 1649–1657.
8. Schulze, W.X., Sanggaard, K.W., Kreuzer, I.,
Knudsen, A.D., Bemm, F., Thøgersen, I.B.,
Brautigam, A, Thomsen, L.R., Schliesky, S.,
et al. (2012). The protein composition of the
digestive fluid from the Venus flytrap sheds
light on prey digestion mechanisms. Mol. Cell
Proteomics 11, 1306–1319.
9. Schultze, W.X., Frommer, W.B., and Ward, J.M.
(1999). Transporters for ammonium, amino
acids and peptides are expressed in pitchers of
the carnivorous plant Nepenthes. Plant J. 17,
637–646.
10. Rea, P.A. (1982). Fluid composition and factors
that elicit secretion by the trap lobes of Dionaea
muscipula Ellis. Z. Pflanzenphysiol. 108, 255–272.
Director, Marine Biological Association of the
UK, Citadel Hill, Plymouth PL1 2PB, UK.
E-mail: cbr@MBA.ac.uk
http://dx.doi.org/10.1016/j.cub.2013.07.026
transcription factor expression and
transmitter phenotype and, through a
clever use of intersectional genetic
approaches, were able to selectively
eliminate subsets of V0 interneurons
and examine the effects on locomotor
behavior.
As a first pass, Talpalar et al. [3]
eliminated the entire V0 population. To
do so, they selectively killed off the V0
cells by expressing a toxin that was
driven by Dbx1. To confirm that the
approach was working, they used an
array of genetic markers to identify V0
cells and found a substantial reduction
in their number, while those derived
from other progenitor domains were
spared. Once they established the
specificity of the ablation approach,
next on the list was an examination of
the consequences. Remarkably,
V0-ablated mice survived the
procedure, which provided a unique
opportunity to test the effect in freely
behaving animals. As you might
expect from previous work [6],
V0-ablated mice lacked the ability
to generate normal alternating
limb movements, and instead
hopped very much like a rabbit
(Figure 1B). Critically, this type of
behavior is never observed in
wild-type mice.