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Plant Behaviour
Theo Elzenga
Ecophysiology of Plants
University of Groningen
Lunteren 16 januari 2016
Hedrich 2015
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Plant Behaviour
“All plants move, but they don’t usually pull themselves out of the ground and chase you.” -Day of the Triffids (1963)
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The singing tomato
What is this talk not about?
Amplifier Frequency
generatorSpeaker
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What is behaviour?
Behaviour /bi-'hA-vy&r/
Function: noun
1 : the manner of conducting oneself
2 a : anything that an organism does involving action
and response to stimulation b : the response of an
individual, group, or species to its environmentEncyclopedia Brittanica
Our bias is caused by the lack of visual movement
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Speed of reactions in
plants and fungi are
limited, depending on
the process involved
Instead of muscle contraction,
plants use hydrostatic pressure to
let organs (leaf, pistal, anthers,
etc) move
Skotheim & Mahadevan, Science 2005
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Exploding Cornus canadensis flowerWhen a pollinator triggers the flower, the
flower burst open accellerating the pollen
2400g
Close up high-speed (10,000 fps) This video covers 13.2 ms and is played at 15 fps.
The wire used to trigger the explosion. Video covers
210 ms and is played at 15 fps.
Edwards et al. 2005
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And some other examples….
BBC motion gallery 2005 Tschumpel et al. 2003
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Some of the signalling is ‘animal-like’….
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Plant ontsnapt aan schaduw door te
groeienNRC 31 december 2015
“Op de microscopische foto is
de blauwlichtgevoelige receptor
in cellen van een tabaksplant
geel aangekleurd. Een receptor
die door gebrek aan blauw licht
wordt geactiveerd produceert
groeifactoren in zijn eigen
celkern.”
Pedmale et al 2015
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Ethylene, low red or blue light induces a shade avoidance response
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A Plant Has to Sense a Wide Array of Signals
bioticabiotic
pathogens
herbivors
competitive species
parasites
partners
symbionts
Exogenous
light(quality, quantity, direction, periodicity)
mechanical stress
temperature
toxic compounds
nutrient status
water status
gravity
Endogenous
hormonesclassical
novel
metabolites physical phenomenonsion-currents
osmotics
developmental
program
How does a plant integrate
all these signals into a
proper respons?
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Plant Behaviour is Phenotypic Plasticity
“Among plants, form may be held to include something corresponding to
behaviour in the zoological field” (Arber, 1950). Behaviour is defined as the
response to signals. In plants, behaviour is phenotypic plasticity-in
animals movement.
light
touch minerals
soil
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The Detectors: the Receptor-like kinases
signalpeptide
receptor-
domain
transmembrane
domain
kinase domain
plasmamembrane
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Mechanism (courtesy of Frank Lanfermeijer)
step 1: ligand binding
step 2: conformationalchanges,dimerizationsignal transduction
step 4: phosphorylation ofdownstream signaltransductioncomponents
step 3: autophosphorylationand activation
receptor-domain
transmembramedomain
kinase domain
Downstream signaling networks
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The number of RLK genes is 610
(2.3% of the whole genome)
417 have the complete RLK
configuration
Torii, 2004
21 different structural classes
roles of characterized RLKs in: a.o.
development, position-dependent
differentiation, self-incompatibility,
defense and disease resistance,
nodulation.
Shiu and Bleecker, 2001
Abundance of RLK genes in Arabidopsis
Sakamoto et al. 2012
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Abiotic Signals Modify the PhenotypeNumerous signals are perceived by plants who discriminate between the
intensity, the length of exposure, direction, integrate with all other
information, process and then adaptively respond.
UV, Blue,Green ,Red, FarRed separately distinguished
7 different stages of water availability
INDIVIDUALITY
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Signal (information) transduction is via a molecular network built around
1000 plant protein kinases and second messengers like [Ca2+]iCritically the strength of connections can be altered controlling information
flow
Complex signal transduction networks allow complex response behaviour
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Shoots searching for resources (light)
Holly growing through Taxus
Photographs by Anthony Trewavas
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Branch DecissionsThose branches most advantageously placed to actively forage light
receive the most root resources.
L D
Predictive
decisions that
determine
distribution of root
resources perceive
future branch
vigour much as
shares are
speculatively
invested in
companies that are
thought likely to
grow more quickly.
Poorly placed branches
receive little root
resource
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Light ForagingSingle Ivy (Hedera). Petiole length
is adjusted to ensure minimal
shading. A: leaf plane faces
direction of sun, B: sunlight vertical
C: leaves placed to cover whole
area
E. Mixture
of two ivys.
Pattern breaks
down with
competition.
A
B
C
D. Low light increases petiole
length and leaf area
D
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“It’s fun to mess with their minds”
Blue and Far-red
Blue and Red
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Single plant Mixed plants
But there is more to this example…
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Klimplant herkent zijn eigen rankenNRC 27 augustus 2015
Charles Darwin in On the Movements
and Habits of Climbing Plants (1875).
„Een van mijn planten had twee stengels
vlakbij elkaar, en de ranken kwamen
meermalen bij elkaar in de buurt, maar
het bijzondere is dat ze geen enkele
keer in elkaar raakten.”
Cayratia japonica ranken worden
meestal vermeden. De plant herkent wel
de eigen soort, maar niet zijn stekjes.
Over hoe een plant zijn eigen soort of
zijn eigen takken herkent is wel
geopperd dat door een plant elektrische
golven schommelen, die in alle eigen
takken en wortels gesynchroniseerd zijn.
Fukano & Yamawo 2015
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Self-recognition of tendrils
Degree of tendril coiling in transplanted C. japonica that touched self plants (connected via stems or roots, or separated),
Cayratia japonica
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Self recognition of tendrils
Proportions of completely
coiled (black), coiled (grey),
slightly coiled (dotted) and
uncoiled (white) tendrils
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Behaviour of climbing vines - placing the tendril at the right spot
is essential
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1
2
3
Passiflora tendril.
Support placed
initially at 1, then 2
and then 3. Each
time the tendril
follows the
movement of the
support. Total
observation 8 hours.(Quantin, 1952)
TENDRIL MOVEMENTS
Recognition of support
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Root Fouraging for Nutrients
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Plants Actively Forage for Environmental Resources (food)
and Competitively Deny them to Others
Stolon changes morphology
according to richness of soilBarley growing
through layer of
soil rich in N
1 4
7
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Fouraging strategies of plants compared to social insects
Both insects and plant roots optimise the
cost-benefit ratio and the data mostly fit
the expectations of the marginal value
theorem. McNickle et al 2009
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Which strategy is used
for nitrogen (best
studied example) is
determined by both
the nutrient status of
the plant and the
nutrient status of the
soil
Molecular decision
network for roots
foraging for nitrogen
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Active Foraging in competition for Soil Resources
If provided with equal mineral and water resources,
plants with more soil space grow substantially
bigger: they minimise self competition.
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Gersani et al.,2001. J Ecol
Application of Game TheoryWith limited space and resources, sharers should (selfishly) produce
more roots/individual and less seed than owners.
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Self and non-Self Discrimination Competition should be reduced for roots from the same plant.
Root mass was measured in
intact seedlings, in twins and
those severed for various time
periods (aliens). Mass of roots,
length of roots, root/shoot ratio
and rientation of laterals towards
aliens was double that of self
roots.
Tota
l ro
ot
mass, le
ngth
, num
bers
and d
irection
Days separated0 60
60
20
Novoplansky 2003 Gruntman & Novoplansky 2004
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So.. ‘self’ is recognised but plants share information…
Novoplansky 2014
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Hunting
Behaviour
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Parasitic plants in the genus Cuscuta. (A) C. pentagona seedling attaching to a
tomato plant. (B) Vines of C. pentagona coiled around the petiole of a tomato
leaf. (C) Growth habit of Cuscuta. (D) C. pentagona seedling growing toward a
tomato plant across a filter-paper disc.
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BBC Secret life of plants
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Foraging by Cuscuta
pentagona seedlings.
A: Summary of C. pentagona
seedling growth responses to a
pot containing moist soil, a
nearby 20-day-old tomato
plant, and tomato volatiles
released from rubber septa.
The position of the target is
indicated by a circled X. The
final position of the apex of
each seedling is highlighted
with a solid black circle. The
numbers of seedlings growing
into each disc half and
quadrant are summarized in
the smaller circles below each
disc.
B: Experimental setup for the
release of plant volatiles while
blocking light cues.
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Days0 2 4
Coils
Haustorial
initials
%T
ota
l
Earliest
uptake
100
50
0
Cost Benefit Analysis in Branch and Root Decision.
Refusal within three
hours even when
offered a suitable
host. Dodder does not
compete with itself.
self recognition!
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% o
f ste
ms r
eje
cting h
ost
Average N content of host
Dodder Exerting Choice over Food Quality of Host(Kelly 1992)
0.72 0.97
60
40
20
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Foraging Model Applied to Dodder Measurements indicate it follows the
marginal value model of foraging using
different hosts. Most crucially predicts
number of coils required . Predictive
modelling increases fitness.
Coil Length. mm.
(investment)
Bio
-ma
ss/
un
it c
oil
len
gth
. (g
m/m
m)
(Energ
y g
ain
ed/2
8 d
ays)
10 20 30 40
0.08
0.06
0.04
0.02
0
Foraging (marginal value)
model developed for animals
(Charnov, 1976).
Replace time-spent-foraging
(energy investment) for
animals, by energy invested
in coil length for Dodder.
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Going back to Mimosa….
The time to reopen after closing
the leaves reflects the functional
choice between resource and
avoiding herbivory
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Thank you for your attention
Time for questions(?)