Plant Behaviour

Theo Elzenga

Ecophysiology of Plants

University of Groningen

Lunteren 16 januari 2016

Hedrich 2015

Plant Behaviour

“All plants move, but they don’t usually pull themselves out of the ground and chase you.” -Day of the Triffids (1963)

The singing tomato

What is this talk not about?

Amplifier Frequency

generatorSpeaker

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

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

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

And some other examples….

BBC motion gallery 2005 Tschumpel et al. 2003

Some of the signalling is ‘animal-like’….

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

Ethylene, low red or blue light induces a shade avoidance response

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?

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

The Detectors: the Receptor-like kinases

signalpeptide

receptor-

domain

transmembrane

domain

kinase domain

plasmamembrane

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

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

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

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

Shoots searching for resources (light)

Holly growing through Taxus

Photographs by Anthony Trewavas

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

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

“It’s fun to mess with their minds”

Blue and Far-red

Blue and Red

Single plant Mixed plants

But there is more to this example…

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

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

Self recognition of tendrils

Proportions of completely

coiled (black), coiled (grey),

slightly coiled (dotted) and

uncoiled (white) tendrils

Behaviour of climbing vines - placing the tendril at the right spot

is essential

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

Root Fouraging for Nutrients

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

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

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

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.

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.

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

So.. ‘self’ is recognised but plants share information…

Novoplansky 2014

Hunting

Behaviour

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.

BBC Secret life of plants

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.

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!

% 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

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.

Going back to Mimosa….

The time to reopen after closing

the leaves reflects the functional

choice between resource and

avoiding herbivory

Thank you for your attention

Time for questions(?)