A Unified Hypothesis of Mechanoperception in Plants

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A Unified Hypothesis of Mechanoperception in PlantsAuthor(s): Frank W. TelewskiSource: American Journal of Botany, Vol. 93, No. 10 (Oct., 2006), pp. 1466-1476Published by: Botanical Society of America

Stable URL: http://www.jstor.org/stable/4123130 .

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American

Journal f

Botany

93(10):

1466-1476. 2006.

A UNIFIED HYPOTHESIS OF

MECHANOPERCEPTION

IN

PLANTS1

FRANK

. TELEWSKI2

W. J.

Beal

Botanical

Garden,

Department

f Plant

Biology,

Michigan

State

University,

ast

Lansing,

Michigan

48824 USA

The perceptionf mechanical timulinthe nvironmentscrucial othe urvival fall living rganisms. ecent dvances have

led to

the

proposal

of

a

plant-specific

mechanosensory

etworkwithin

lant

cells

that s

similar o the

previously

escribed

network

n animal

ystems.

his

sensory

etworks

thebasis for

unifying ypothesis,

hich

may

accountfor he

perception

f

numerous

mechanical

ignals

ncluding

ravitropic,

higmomorphic,higmotropic,elf-loading,

rowth

trains,

urgor ressure,

xylempressure otential,

nd

sound.

The current

tate

f

our

knowledge

f

a

mechanosensory

etworkn

plants

s

reviewed,

nd

two

mechanoreceptor

models

are

considered:

a

plasmodesmata-based

ytoskeleton-plasma

membrane-cell

wall

(CPMCW)

network

s. stretch-activatedon channels.

Post-mechanosensory

hysiologicalresponses

to

mechanical tresses

re

also re-

viewed,

and future esearch irections

n

the area of

mechanoperception

nd

response

re

recommended.

Key

words:

gravitropism;ravity;mechanoperception;

ound;

thigmomorphogenesis;

higmotropism;

urgor

ressure;

wind.

The

ability

osense nd

respond

o

physical

timuli

s of

key

importance

to

all

living

things. Among

the

common

environmentaltimuli etected

y living rganisms

re

light,

temperature,nd a varietyfchemical ignals.A number f

these timuli

ppear

o be

closely

elated nd

can

be considered

as

physical-mechanical

timuli,

hat

is

differences

n a

mechanical

orce r

pressure

erceived

y

the

iving

ell.

A

cell

may perceive ravity;

trains

aused

by

self-loading

nd

internal

rowth;

mechanical

oading

by

snow, ce,

and

fruit,

wind, ainfall,ouch, ound;

nd the

tate

f

hydration

ithin

cell

(turgor ressure).

ll

organisms

ppear

o

perceive

hese

mechanical

ignals,

egardless

f their

axonomiclassification

or lifehabit

sessile

vs.

motile).

The

significant

ifferences

between

axonomic

roups, pecificallylants

nd

animals,

re

found

in

the individual molecular

components

of the

microstructure

f the nternalellular

ensing

network

Jaffe

et

al.,

2002;

Balu

ka et

al.,

2003)

and inthe

response

f

an

individualrganismo each mechanicaltimulus.

Internal mechanical

forces-The

sensing

of

gravitropic

signals

yplants

as been tudied

or

00

years

Knight,

806).

Since

the

first

tudy,

he

elucidation

f the mechanism f

gravitropic

erception

as been

researched

n

a

broad

rray

f

plants

rom

lgae

to

trees

nd

n a

variety

f

plant rgans.

o

date,

wo

compelling ypotheses

xist

regardingravipercep-

tion

in

plants:

the starch-statolith

ypothesis

nd the

hydrostatic

odel

of

gravisensing

for

reviews,

ee

Sack,

1991, 1997;

Balu'ka

and

Hasenstein, 997;

Staves t

al.,

1997;

MacCleery

nd

Kiss,

1999;

Boonsirichait

l.,

2002;Drobak

t

al.,

2004).

Both

hypotheses

ltimately

ely

n

the

ensing

f

a

mechanical

ignal

t the

cytoskeleton-plasma

embrane-cell

wall interface

CPMCW)

interface.n the case

of

statoliths,

falling tarch rainsor other rganelles mpact heplasma

membrane

hus

nducing

n internal echanical

ignal

Sack,

1991,

1997;

Balu'ka

and

Hasenstein,

997;

Perbal

t

al.,

2004).

Similarly,

the reorientation

f

a

plant organ

within

a

gravitational

ield is

proposed

to induce

internal

ressure

differencest the

CPMCW

interface,

hich

an be considered

an

externalmechanical

ignal

Staves

et

al., 1997;

MacCleery

and Kiss, 1999; Balu'ka et al., 2005). Therefore, more

broadly nifying

echanism

may

underlie

raviperception

n

plants

han hat voked

by

a

hypothesis

hat elies n how the

mechanical

ignal

is

initiated;

n actual

sensory

tructure

withinhe ell

may

llow for

mechanoperception

s

the

plant

s

reoriented

ith

espect

o

gravity.

upporting

he

oncept

f a

unified

ypothesis

or

mechanical

ensing

n

the

gravitropic

response

s thework

f

Massa and

Gilroy

2003)

who

reported

when root

ap

came

in

contactwith

horizontal

lass plate

(inducing higmotropic

timulus),

he root cells behind he

growingipbegan

o

growhorizontally.

his

allowed heroot

cap

to maintainontact

ith he

plate,

while

he

est

f

the oot

grew

over nd

parallel

o

theobstaclewith

step-like

rowth

form.

he

authors

uggested

hat he

gravisensitive

ells of the

root

ap

also sensethe ouch nd

signal

he

olumella ells to

altertheir

ravitropicesponse,

o that

hey

ct

together

o

redirect oot

growth

o

avoid obstacles while

continuing

general

ownward

attern

f

growth.

In

plants,gravitropism

an occur

in

either

primary

r

secondary

issues.

n

primaryrowth,

he

gravitropic

urvature

results

rom ifferentialell

elongation

n

opposite

idesof the

displaced

organ.

In

the case of

secondarygrowth,

he

gravitropic

esponse

ncludes heformation

f

reaction

ood;

tensionwood n

porous

ngiosperms

nd

compression

ood

n

nonporous

ngiosperms

nd

gymnosperms

Timell, 1986a).

Tensionwood

forms n

the

upper

ide of a

displaced

tem

nd

is

characterized

y

the

formation

f

gelatinous

iberswith

lower

ignin

ontent,

maller

iameter,

nd

fewer

essels nd

by

a

realignment

f

cellulose

microfibrilsnto

a

vertical

orientationithin hegelatinousayer,whichforms nside

partially

eveloped

nd

lignified

2

layer

of

secondary

ell

walls

of

gelatinous

fibers.

Compression

wood forms n

response

o

gravity

n

the ower ide of

displaced

tems nd

is

characterized

y

tracheids ith thickened

econdary

ell

wall with

higher ignin

content,

round cross

section,

intracellular

paces

at cell

corners,

nd

a

realignment

f

cellulosemicrofibrils

n

the

2

layer

o a

450

to

600orientation

with

espect

o

the

xis of

the tem.

The

formation

f

reactionwood

in

stems, ranches,

nd

roots

s

not n exclusive

esponse

o

gravity

n

woodyplants.

The

formation

f reaction

wood

has also

been observed o

Manuscript

eceived 1 March

006;

revision

ccepted

6

August

006.

The author thanks J. S.

Kilgore,

L.

Koehler,

and two

anonymous

reviewers

for

critically

valuating

this

manuscript.

he research was

supported

y

the

National

Research nitiative f the USDA

Cooperative

State

Research,

ducation

nd

Extension

ervice,

grant

os.

2002-35103-

11701

nd

2005-35103-15269.

2

E-mail:

[email protected]

1466

This content downloaded from 128.248.155.225 on Thu, 31 Oct 2013 09:56:52 AMAll use subject to JSTOR Terms and Conditions






October

006]

TELEWSKI-MECHANOPERCEPTION

N

PLANTS

1467

develop

n

branches nd stems s a means f

reshaping

rowns

and as a

possible hototropicesponseEngler,

924).

Tension

wood

has been

reported

o formn theverticaltems f

rapidly

growing oplar

Populus)

trees

for

review,

ee Telewski t

al.,

1996).

Timell

1986c)

suggested

hat he reactionwood

may

form

o

keep woodyplants

n

balancewith heir

hysical

environment

e.g., gravity,

wind,

and

light), ubsequently

generatingnternal rowthtrains hat esult n thephysical

reorientationf

woodyplant rgans.

The maturationf

xylem

ells

n

the ambial one

involves

the lteration

f

ndividual

ell

engths.

n

many

nstances,

here

is

intrusive

rowth

n which the cells

elongate

within he

relatively igid

structure

f the

stem,

inducing

nternal

compressive

orces

Boyd,

1985; Archer, 987; Fournier

t

al.,

1991

, b; Larson,

994).

n other

ases,

he ells hrink

pon

maturation

nducing

tensile force within he

stem. The

generation

fthese

nternal

rowth

trainss

responsible

or he

realignment

f stems in the

gravitropic esponse,

with

compression

ood

developing compressive rowth

train

and tensionwood

forming

tensile

growth

train

Wilson,

1981;

Almdras t

al.,

2005).

Growth trains lso

develop

n

stems

aligned

vertically

with

respect

o

gravity

nd

may

functionomaintain echanical alancewithin oody lantss

part

f

phototropicesponse,elf-loading,

r from ifferential

loading

aused

by

crown

symmetry

Archer,

987).

Within

vertically ligned

stem,

here re two

potential

sources f

compressive

orce

oading.

he

most bvious s due

to

self-loadinglong

hevertical

xis of

the tem s a result f

the

ccelerating

orce f

gravity.

second

ompressive

orce

has been

uggested

o be induced

y

the onstrictiveature f

bark issues

referred

o as bark

ressure),

esulting

n

a radial

compressive

orce hat ffects

ylogenesis

n the

ambial one

(DeVries,

1875).

nearlier

tudies,

he adial

ompressive

orce

of a

constricting

uter bark was

hypothesized

o increase

during

he

growing

eason from he radial

growth

f the

cambium nd to be

responsible

or

heformationf

smaller,

denser atewood ells and the ultimate ormationf annual

growth ings

for

review, ee Larson,1960). In

subsequent

studies,

his

hypothesis

as

refuted,

nd annual

growth

ings

were found o form

n

response

o external nvironmental

stimuli

ncluding ay length

nd

changes

n

plant growth

regulator

ontent

for

review,

ee Little nd

Savidge,

1987;

Roberts

t

l.,

1988;

Larson,

994).

Although

he ark

ressure

hypothesisppears

o bear ittle n the formationf

annual

growth ings,

he

pplication

f

compressive

orce o cambial

explants

tissue ulture)

ppears

o functionn

maintaining

he

structurend

organization

f the vascular

ambium

n

vitro,

ensuring

he ontinued

roduction

f

apparently

ormal

ylem

(Brown

nd

Sax, 1962; Brown, 964;

Makino t

al.,

1983).

Additionally,elf-loadinglong

a vertical xis contributes

significantly

o

development

n

plants.

he

ability

f a

tree

o

perceive ts own weightmustplay a significantole in

determining

verall

allometry

nd mechanical

roperties

f

wood

(density

nd elastic

modulus)

produced y

a mechani-

cally

oaded vascular

ambium,

n

the absenceof

any

ateral

loading

nduced

y

windor other xternal

mechanical orces

(McMahon,

1973;

Wainwright

t

al., 1976;

Niklas,

1992,

1994).

n

a few

tudies,

he

pplication

f a

compressive

orce

induced ifferentiationf cambium nitialswithin mass of

dedifferentiatedallus cells

and within

raft

nions

Lintilhac

and

Vesecky,

981;

Barnett

nd

Asante,

000).

The notion hat

self-loading

ill

mpact

heformationf a vascular ambium

and

subsequent econdaryxylogenesis

has

recently

een

further

upportedy

a

study

n wood

formation

n

Arabidopsis

in

which he

application

f

weight,

nd thus

compressive

force n the

tem,

nduced

econdary rowth

n

a

species

hat

only produces

herbaceous

rowth

nder normal

nviron-

mental onditions

Ko

et

al.,

2004).

Ko et al.

suggested

hat

he

mechanical timulus f

self-weight

s

perceived

y

the

stem

and induces

the differentiation

f a

secondary

vascular

cambium nd subsequent ormationf secondary ylem nd

that

self-weightmay play

a

more

important

ole in

the

development

f the

woodyplant

rowth

abit.

The

self-loading

nduced

by

the

bearing

f

fruit as been

shown o influence

rowth

n

branches

Alm6ras

t

al.,

2004;

Vaast et

al.,

2005).

The forces ssociatedwith he

bearing

f

fruit re

primarilyerceived

n

branches nd

at branch

ases

and consist f an

alternate

ompressive

orce n the

ower

ide

ofthe ranch nd tensile

orce n the

upper

ideof

the ranch

so

that he branch cts like

a

cantilever

Wainwright

t

al.,

1976;

Niklas,

1992).

The additional

oad will

stimulate

increased eaction ood

formationn

thebranches.

Each

living

cell within

plant,

with ts

organelles

nd

protoplasm,

unctions

echanically

ike a water-filled

alloon

(hydrostat),xerting

circumferentialensile orce

nd radial

compressiveorcewithin heplasmamembranendpressing

against

the

surrounding

ell

wall. The

plasma

membrane

controls

urgor y

regulating

he flow

of

water nd

solutes

between he

apoplast

nd

symplast. urgor

ressure

an be

increased

hypertonic)

r decreased

hypotonic) y

ltering

he

osmotic

potential

f the

apoplast

or

symplast,

hus

either

forcing

ater nto

cell

increasingurgor

r

by

drawing

ater

outof a

cell and

decreasingurgorplasmolysis).

urgor

s also

decreased

y

drought

tress,

ometimes

esulting

n

the oss

of

mechanical

trength

f

plant

issues,

which

esults

n

wilting.

Under these

conditions,

turgor

pressure

can

contribute

significantly

o the

mechanical

roperties

f

plants,

specially

in

soft,

on- r

ow-lignified

issues

nd

organs

haracteristic

of

primary

rowth

for

reviews,

ee

Niklas, 1989,

1991).

Sensing hanges

n

turgor

s

crucial o

survival

n

plants.t

is

possible

hat

hanges

n

turgormpart

mechanicaltresses n

the

CPMCW,

which erves s the

mechanosensory

etwork

or

plant

ells.

Sensing

water

otential

ithin he

plant

ia

nternal

mechanical tresses t the

ellular evel could

be the

means or

what

s

termed

ydraulicignaling,

roviding

faster

ignaling

and stomatal

esponse

o the

nset

f

drought

tress

han

ould

be

predicted y

a

root-generated

hemical

signal

such as

abscisic

cid

Comstock,002).

Hayashi

t al.

2006)

provided

data to

support

he role of both

the CPMCW and

Ca2+-

mechanosensitive

tretch-activatedon channels n

plant

ells

under

hypotonic

nd

hypertonic

onditions.

They report

stretch-activated

on channels function n

sensing

both

hypotonic

nd

hypertonic

onditions,

here

s the

CPMCW

is

only

nvolved n

sensing ypertonic

onditions.

Externalmechanical

orces-Numerous

xternalmechan-

ical stimulian be

perceived y

n

organism.

ome re

nduced

by gradients

n

pressure

within he

atmosphere

nd

are

responsible

or

wind,

while

pressuregradients

n

aquatic

systems

re created

y

currents

r tidalflows. ressure

aves

that

form ound waves are transmittedn

both aerial and

aquatic

nvironments.thermechanical

timulire nduced

y

gravity,

uch as the

accumulationf ice or

snow,

butdo not

necessarily

nduce

gravitropicesponse.

third

ategory

an

be classified s

touch,

uch as

that nduced

y

the

mpact

f

raindrops,

ailstones,

ther nanimate

bjects,

or

by

other







1468

AMERICAN JOURNALOF BOTANY

[Vol.

93

organisms.

hese

mechanical

timuli ave

collectively

een

termed

ouch

or

thigmo

timuli

nd

produce

number f

thigmo

esponses

n

plants,

ncluding

higmomorphogenesis,

thigmotropism,

higmonasty,

nd

the

thigmotactic

esponse

(Jaffe

t

al.,

2002;

Braam,

005).

Once

again,

he

perception

f

an

external

ouch or mechanical

ignalsdepends

upon

the

CPMCW

mechanosensing

etwork.

Vogel (1994) outlined heparametersnfluencingife in

moving

fluidsand

provided

the fundamentalseeded to

understand

he

physics

f

fluid

dynamics

n

aquatic

systems

and

the

tmosphere.

s mentioned

reviously,

ifferentialsn

atmospheric ressure

esult

n

pressure

waves

defined s

currents

f air

or

wind.

Currents

n

aquatic cosystems

re lso

pressure

waves.

Waves

in

aquatic systems

r wind

can

be

laminar r turbulent

Vogel,

1994).

Due to

the

greater ensity

and

viscosity

f

water,

heforce

mposed

y

a

wave

at

a

given

velocity

n

a

structure

s

much

greater

han

by

wind.

Denny

and

Gaylord

2002)

gave

the

xample

f

2 m

-

s-'

(4.5

miles

?

h-')

velocity

ave

as

being oughlyquivalent

o

a 58 m

-

s-1

(130

miles

h-'

or between

category

and

4

hurricane)

ind

in terms

f

applied

force.

hey

go

on

to state hat

5

m

s-'

wave

velocities

re

notuncommon

n

shoreline nvironments

andthat uch wave exerts he

quivalent

orce f that

early

equal

to a

wind

nexcessofMach 2. One

ofthe

omplexities

f

studying

he

esponse

f

plant

mechanical tresses

mposed

y

wind r wave

s

dissecting

he ndividual

orces

cting

pon

he

structure

f

plant.

Wind

places

n

asymmetricressure

nthe

side

of a

plant

reating

cantilever ith he rotation

oint

located

n

theroot

late Vogel,

1994).

Wind

nduced

way

s

considered

the

primary

mechanical stress

inducing

an

alternatingompressive

nd tensional

orce,

with ometorsion

applied

n

stems nd roots

Telewski,

1995).

Pressurewaves

can

also

displace

he stem

within he

gravitational

ield

ong

enough

to

induce

a

gravitropicesponse,

which shouldbe

considered

s

a

secondary

wind-inducedmechanical tress

(Telewski,

1995).

Due to the

neutrally uoyant

nature

f

aquaticsystems,macrophytes aynotrequire significant

gravitropic

esponse

pon displacement y

waves. The weak

and

highly ompliant

tems

f

arge

lgae

allow

for hem

o be

highly

lexible atherhan

rotective

nd

rigid

ike he tems f

most errestrial

lants

Denny

nd

Gaylord,

002).

This

highly

flexible tructurellows

algae

to

floatback

to the vertical

orientation

hen wave action

ceases,

without he need

to

induce

specialized train-generating

issues

uch

as reaction

wood that

s

needed to re-orient

terrestrial

lant

within

gravitational

ield.

The

ability

f a

plant

o

respond

o wind

for

reviews,

ee

Jaffe, 985;

Biddington,

986;

Vogel,

1994; Telewski,

995)

or

waves

Vogel,

1994; Koehl,

1999;

Puijalon

nd

Bornette,

2004;

Puijalon

t

al.,

2005)

by altering

orphology,

natomy,

and biomechanicalropertiesnables theplant o withstand

additionalmechanical

oading. eople

have

ong

observed hat

wind

influences he

morphology

nd

growth

of

plants,

especially

rees,

reatingmetaphors

nd

lyrics

bout trees

growing

n

windy

nvironments

eing tougher

nd able to

endure

hardship.

he first cientific

tudy

o document he

influence

f

wind on tree

growth

was

published y Knight

(1803)

in

which taked

pple

rees

Malus)

produced

ess radial

growth

han rees llowed

to

sway freely

n the

wind.

When

Knight

estrictedind-induced

otion o the

bilateral

north

o

south),

he tem ormedn oval

with he

proportion

f

13:11.

Knight

went n tostate

p.

281):

If tree e

placed

n a

high

nd

xposed

ituation,

heret s

much

kept

n

motion

y

winds,

henewmatter

hich t

generates

ill e

depositedhiefly

n

he ootsnd

ower

arts

of he

runk;

nd

he iameterf he atter ill

iminish

apidly

in its ascent.

..

the

growth

f

the insulated

ree on

the

mountain

ill

e,

s

we

lways

ind

t,

ow

nd

turdy,

ndwell

calculatedo

resist

he

heavy

ales

to whichts

situation

constantlyxposes t.

The alterationn

growth

nd

stem

llometry

n

response

o

windfirst

escribed

y

Knight

s

an increase

n

radial

growth

and a decrease n

height rowth

would be

defined 70

years

later

y

Jaffe

1973)

as

thigmomorphogenesis

nd

ater s the

thigmomorphogeneticheory

Jaffe,

984).

This

term s now

used

to

describe he

response

f

plants

o

wind and

other

mechanical

erturbations,

ncluding

mechanical

ending

or

flexing

r

by

touching

r

brushing

y

passing

nimals. imilar

to

the

opic

f

gravitropism,

he

ntervening

03

years

ince he

printing

f

Knight's

higmomorphogenetictudy

ave

seen a

multitudef

papersreporting

he nfluence f

wind

or

other

mechanical

perturbations

n

plant

growth,

many

of

them

summarized

n

the

reviews

by

Grace

(1977),

Jaffe

1984,

1985), Biddington1986), Vogel (1994), Telewski 1995),

Mitchell

1996),

Jaffe t al.

(2002),

and Braam

2005).

The

perception

f a

thigmomorphogenetic

tress

y

the

mechano-

sensing

network s

rapidly

ollowed

by

a

mechanoresponse

cascade,

which

as been hown o be

dose

dependent

Erner

t

al., 1980;

Jaffet

al.,

1980;

Braam

nd

Davis, 1990;

Knight

t

al., 1992;

Telewski

t

al.,

1997;

Telewski nd

Pruyn,

998;

Hepworth

nd

Vincent, 999; Telewski,

000).

The

mechano-

physiological-response

ascade will be

addressed ater n

this

manuscript.

haracterizationf

the

forceswithin

bending

r

flexing lant rgan

an be

difficulto characterizend

quantify

due to the

differing

ature

f

the

pplied

force,

eometry,

nd

morphology

f

the

rgan

nd the

nisotropic

ature f different

tissues,

which

omprise

he

plant rgan

s a

cellular

omposite

material

Niklas

and

Moon, 1988;

Beusmans

nd

Silk,

1988;

Niklas, 1992;Vogel, 1992;Moulia et al., 1994; Moulia and

Fournier, 997;

Coutand t

al., 2000;

Coutand nd

Moulia,

2000; Telewski,

000).

In

a detailed

nalysis

f

themechanical

stimulus f

bending

nd

resulting

rowth

esponse

n

tomato

(Lycopersicon

esculentum Mill. Var.

VFN8),

Coutand and

Moulia

2000)

reported

hat

mechanosensing

s

both ocal and

scattered

hrough

he tem nd

explained

he

variability

f the

growth esponse

y

the

ntegrals

f the

ongitudinal

train

ield

within

he

bending

tem.Jaffe t al.

(1980),

Telewski and

Puryn

1998),

and

Coutand and

Moulia

(2000)

reported

logarithmic

elationship

f

the

sensory

unction

etween he

dose of

mechanical timulus

nd

growth esponse.

outand t

al.

(2000)

reported

hat

ncreasing

heforce

pplied

o

tomato

stems

rom

to 175

g

or stem

isplacement

rom

00

o250did

not nfluenceheduration f thegrowthesponse. herefore,

thedose

response ppears

o be

sensitive o the number f

perturbations

nd not ensitive o the mount

fforce

pplied

in

each individual

erturbation

Coutand

t

al.,

2000).

By

definition,

ound s

acoustic

nergy

n

the form

f

an

oscillatory

oncussive

pressure

wave

transmitted

hrough

gases, iquids,

nd solids. t

is

audible o the

human ar and

falls nto he

requencyange

f

20-2000 Hz. Sound

bove this

range

s

classified s

ultrasound,

nd soundbelow his

ange

s

infrasound. ne

only

needs

to

hold one's hand n front f a

base

speaker

r be next o a car n which he

volume s

turned

up

to feelthe

pressure

wave in the near

nfrasound

ange.







October

006]

TELEWSKI-MECHANOPERCEPTIONN

PLANTS

1469

Vegetation

s known o absorb coustic

nergy

Eyring,

946;

Martens nd

Michelsen,

981;

Price t

al.,

1988)

and

has

been

employed

o deaden henoise

f

urban nvironments

Huisman

and

Attenborough,

991;

Attenborough,

002).

However,

unlikewind or

waves,

the level of sound

energynormally

experienced

y plants

n theenvironment

oes not

appear

o

invoke

significant

ompromising

echanical

tress o

plant

structure. echanical nergy mpartedo a plantstem caninduce t to

sway

to its resonant

requencies,

sually

n

the

infrasound

ange,

which

will

be a functionf the

height

nd

mechanical

roperties

f its tissues. hese

multiple

esonance

frequencies

an

be

used,

n

turn,

o calculate he

height,

lexural

stiffness,

ndmodulus f

lasticity

f he tem

for

review,

ee

Niklas nd

Moon,

1988).

As

discussed,

lants

eed o

perceive

and

respond

o wind rwave nduced

movement

o

cclimate o

a

given

nvironment.

hey

will

ven

way

n

harmonic

otion

at low resonant

requencies. lthough lants

an

effectively

absorb sound

and even

generate

ound

via wind-induced

resonance

f

various

tructuresuch s

needles nd

spines

for

example,

he

whispering

inds n a

pine

forest),

an

they

perceive

ound,

nd,

f

perceived,

ill

hey

espond

o ound? s

there

developmentaldvantage

o

responding

o

ound

eading

to acclimationosonic tressesnthe nvironment?

Ultrasound as been shown o have the

greatest

ffect n

plants, pecifically

n

seed

germination

for

reviews,

ee

Davidov,1961;Timonin,

966;

Halstead nd

Vicario,

1969;

Hageseth,

974;

Weinberger

nd

Burton,

981;

Miyoshi

nd

Mii,

1988).

Timonin

1966)

reported

hat ltrasound

reatment

altered he

viscosity

f macromoleculeolutions

n

seeds.Near

ultrasound

1.4

kHz,

0.095

kdb)

was

reported

o

increase

metabolism

n

chrysanthemum

oots,

haracterized

y

ncreas-

es

in

amylase ctivity,

oluble

sugar,

nd

protein

Yi

et

al.,

2003).

The treatmentf

chrysanthemum

allus

with 1.4

kHz

sound increases ndoleacetic cid levels while

decreasing

abscisic

cid

levels

Wang

et

al.,

2004).

The

perception

nd

response

of

plants

to

sound,

more

specifically usic,

as been

part

f folklore

see WeinbergerandGraefe,

973)

andthe ource f

inspiration

or ountless

primary

nd

secondary

chool student cience fair

projects

beginning

n the

1940s

(Klein

and

Edsall, 1965;

personal

observation).

he

influence

f

music,

complex

mixture f

notes,

ones,

mplitudes,

nd

harmonics,

n

plant rowth

as

been the

subject

f scientific ebatefordecades.

Singh

and

Ponniah

1955a,

b,

1963)

reported

n the

timulatory

nfluence

of

music

on

plant

growth

n

a

number f

species.

Klein

and

Edsall

(1965)

reported

o

influence

f a

diverse

election

f

music,

rom

lassical

o rock

nd

roll,

n the

growth

f

Tagetes

erectaL.

Weinberger

nd

colleagues

onducted

number

f

studies n the nfluence f bothmusic

and

singlefrequency

sound,

both

n

the audible and ultrasound

ange,

n

plant

growth

nd

seed

germination

nd

reported

hat ound can

influence lant growth Weinbergernd Measures, 1968;

Measures nd

Weinberger,

970;

Weinberger

nd

Das,

1971;

Weinberger

nd

Graefe, 1973;

Weinberger

t

al., 1979;

Weinberger

nd

Burton,

981).

Most

recently,

reath,

nd

Schwartz

2004)

reported

music ncreased he rate of seed

germination

n zucchini

(Cucurbita

pepo

L.)

and okra

(Abelmoschus

sculentus

L.) Moench).

Touch,

defined

s

the act of

making hysical

ontactwith

another

olid

object

nd

nducing

mechanical

timulus,

eads

to two ther

higmoresponses

n

plants

for

eviews,

ee

Jaffet

al., 2002; Braam,

2005).

This

group

of

two

responses

o

mechanical

timuli

ncludes ne of hemost ramatic

esponses

in the

plant

kingdom,

higmonastic

ovements,

most com-

monly

associated with the

rapid

movement n

plants

in

response

o

touching.

umerous

lant

raps

re

thigmonastic

in

nature nd weredescribed

y

Darwin

1893).

These

nclude

the Venus'

flytrap

Dionaea

muscipula

Ellis ex

L.),

first

described

y

Curtis

1834),

which

produces trap

from

modifiedeaf.On the abaxial surface f

each halfof

the eaf

trapsare threemechanosensingrigger airs,which,when

stimulated,

lose

the

rap

within second

Brown,1916).

The

movement

y

the

modified

eaf

trap

nd

the

tentacles f the

sundew

Drosera

rotundifolia

.)

incorporates

oth

thigmo-

nastic and

thigmotropicesponses

Lloyd,

1942).

Darwin

(1880,

1893)

reported

hat

he force

mparted

o the

tentacles

covering

he urface f the eaf

rap y

the

weight

f a

human

hair

was sufficiento

supply

he

mechanostimuluso

induce

response,

et

neither ind

norrain

riggered

response.

he

sensitive

plant

(Mimosa

pudica

L.)

also

has

a

rapid

thigmonastic

esponse

with

the

rapid

folding

f

its

leaflets

and movement f the entire

ompound

eaf at

the

pulvinus

upon

ouch. imilar

higmonastic

esponses

avebeen

reported

in

Blopytum

ensitivum

L)

DC

(syn.

Cassia sensitivum

.)

and

in

certain

xalis

species

Umrath,

958).

Thigmotropicovements,nduced yunilateralontact ith

another

iving

organism

uch as a

pollinator

r

mechanical

structure,

esult n

alterationsn

plant

rowth

hat

nclude

he

bending

f

floral

arts

owards

ollinators,

he

wining

f tems

or rootsfor

physical upport,

nd the

coiling

of

tendrils

for

review,

ee

Jaffet

al.,

2002).

Structure

f

the

mechanosensing

etworkn

plant

cells-

Morris

nd

Homann

2001)

reviewed he

concepts

f cell

surface rea

regulation

nd membrane

ension,

providing

insight

nto heroleof membrane

ension n cell

biomechanics

and the

potential

ole

of

membrane

ension

n

mechanoper-

ception

n

both

plants

nd

animals.To

provide

cale,

the

resting

ension

f a

plant

rotoplast

embrane as

reported

o

be

0.12

mN

-

m

'

(Kell

and

Glaser, 993),

he orce

equired

o

activatemechanosensitivehannels s

approximately

mN -

m-'

(Sachs

and

Morris,

998),

nd the

ytic

ension or

plant

protoplasts

s 4 mN

-

m-'

(Kell

and

Glaser,

1993).

The

stretching

ndrelaxation f the ell

membrane

n

response

o

changes

nthe

mechanicalnvironmentf

ells s a

component

of

mechanosensing

itswell

with arlier

eports

f

therole of

stretch-activatedembrane

hannels

n

the

response

f

plants

to

mechanical

tresses

Edwards

nd

Pickard, 987;

Ding

and

Pickard,

993).

The

perception

f a

mechanical

ignal

y

cells

is

a

rapidprocess

with

rapid

ranslationf

the

mechanical

force nto

biochemical

r

bioelectric

essage

Balu'ka

et

al.,

2003;

Ingber,

003a,

b).

Significant

rogress

as been

reported

in

the elucidation f themolecular asis

of

mechanosensory

perception

nd

transductionn animal

ystems,

articularly

he

physical ouplingbetween hecytoskeletonnd cell mem-

brane,

which

provides

a

continuous

tructural/mechanical

network

hroughout

he cell

(for

reviews,

ee

Janmey,

998;

Gillespie

and

Walker, 001;

Baluika et

al., 2003;

Ingber,

2003a,

b).

Jaffe t al.

(2002)

proposed

that

a similar

mechanosensing

etworkxistswithin

lant

ells,

inking

he

cytoskeleton-plasma

embrane-cellwall structures. heir

model

proposed

inkermoleculeswithin

lant

ells as

RGD

(arg-gly-asp)-containingeptides,

imilar to the

integrins,

RGD-containingroteins

nmulticellular

ukaryotes

hat ack

a

cell wall.

n

non-plant

nd

non-fungalystems,

he

ntegrins

facilitate

idirectional

ignaling

nd bind o

actins

for

eview







1470 AMERICAN JOURNAL

OF BOTANY

[Vol.

93

see

Baluka et

al., 2003).

In

plants,

he RGD

integrin-like

peptide

inkages

were

proposed

o

connectmicrotubuleso the

plasma

membrane,

hich ontains

a++

on

channels. echtian

strands

plasma

membrane

leeves

containing

ndoplasmic

reticulum,

ctin

microfilaments,

nd microtubules

Lang

et

al.,

2004)]

then ind he

plasma

membrane

o the ell wall via the

actin-binding,

ntegrin-like

eptides

ttached

o the nterior

f

themembrane, hichfacilitatedheopening nd closingof

stretch-activated

embranehannels

Jaffe

t

al.,

2002).

Balu'ka

et al.

(2003)

compared

nd contrasted

he

inker

moleculesbetween

he

cytoskeleton

nd cell membranen

animal nd

plant ystems.

hey

rgued

hat hefailure o find

true

ntegrinomologs

n

plants

r

fungi recluded

heir ole n

the

lant

r

fungi

mechanosensing

etwork

Hussey

t

l.,

2002)

and

that

lantsmay

have their

wn

unique

et

of

actin-binding

proteins. mong

hemolecules

unctioning

s linkers etween

the

ytoskeleton

nd ell

wall,

roposed

y

Balu'ka

et

l.

2003)

in

their

model,

are

cell-wall-associated

inases

(WAKs),

pectins,

rabinoglactan roteins

AGPs),

cellulose

synthase,

formins,

lant-specific

yosins

f

class

VIII,

phospholipase

,

and callose

ynthase.

n the

ast

hree

ears

inceBaluka et al.

(2003) proposed

heirmodel

of a

mechanosensing

etwork

linking

heCPMCW atcross-walls,urtheresearchndicates

that

lant-specific

yosins

f

class

VIII

and

forminsre the

strongest

andidates

s the lusive dhesive

molecules

Balu'ka

and

Hlava'ka,2005).

Cross-walls,

ocated t

the

nongrowing

axial end of cells are

enrichedwith

plasmodesmata,

ctin,

myosin

III,

and

profilin

reviewed

y

Balu'ka and

Hlavaika,

2005).

Recently,

wo

studies onfirmedherole

of

formins

n

nucleationnd

bundling

f F-actin

Michelot

t

al.,

2005;

Yi

et

al.,

2005).

Deeks et al.

(2005)

reported

hat he rosswalls of

roots,

ypocotyls,

nd

shoot ells of

Arabidopsis

wererich

n

group

formins

proteins

tFH4

nd

AtFH8)

and thatAtFH4

binds

to

profilin,nfluencing

he

polymerization

f actin.

Strengthening

he

putative

role

of

formins

s

adhesive

molecules

linking

the

cell

wall and

cytoskeleton

s

the

extensin-likeomain fthegroup1 forminsredictedo nsert

into

he ell wall

Cvrcikovi,

000;

Cvr'kovai

t

al.,

2004).

Myosin

VIII,

also

located t crosswalls and bound o actin

filaments ithinhe

cytoplasm,

s

reported

o

be

involved

n

callose

synthesis,ossibly inding

with

membrane-spanning

callose

synthase

ubunit

nd

providing

callosic crosslink

between he

ell wall and

cytoskeleton

t

cell

plates, it

fields,

and

plasmodesmata

Balu'ka

et

al., 2003;

Balu'ka and

Hlava'ka,

2005).

Lang

et

al.

(2004)

reported

allose

was

localized

along

the

fibrousmeshwork

overing

Hechtian

strands,

echtian

ecticulum

t the ell

wall,

nd

protoplast

h

after

lasmolysis. lthough

hemeshworkibers

oined

the

cell

wall,

Lang

et

al.

2004)

failed oobserve allose

directly

n

the

plasma

membrane.

allose

synthesis

s

associated

with

numberfwound, hermal,ndmechanicaltress esponsess

well s with

ungal

ttack

nd

pollen

ube

longation.

affe

nd

Telewski

1984)

reported

allose

deposition

ncreased

n

the

phloem

of bean

(Phaseolus vulgaris

L.)

and

loblollypine

(Pinus

taeda

L.)

stems

1

h aftermechanical

timulation,

peaking

fter

h,

nd

was

completely

eabsorbed

y

25

h. Jaffe

and

Leopold

(1984)

similarly eported

allose

deposition

within

min

of

gravity

timulation

n

response

o

gravity

n

Zea

mays

. andPisum ativum . Callose and

aricinan,

hich

is similar

o

callose,

re

components

f

compression

oodcell

walls

Hoffmann

nd

Timell,

970).

The

deposition

f callose

inhibits

ell-to-cell

ommunicationt

plasmodesmata

Siva-

guru

et

al., 2000).

These

studies

upport

role

for

callose

synthesis

n

mechanoperception.

The

complex

tructurendfunctionfthe ctin

ytoskeleton

in

plants

nd

its

inkage

o the cell

membrane

nd

cell wall

continues

o be

elucidated. ne

of theroles

appears

o be in

endocytosis

s

well

as

in

signaling?amaj

et

al.,

2004,

2005).

Baluka

et

al.

(2005,

p

106)

proposed

hat he

ombined oleof

the actincytoskeletonn both signaling nd endocytosis,

combined

with

he

ctin- nd

pectin-rich

dhesive omains f

cross

walls

at the

polar

ends of

cells,

comprise ...'plant

developmental

ynapse'

in

which auxin and

pectin-derived

signaling

molecules

ct as

plant-specific

ransmittersor ell-

to-cell ommunications. n

their eview

f

cell

surface rea

and

membrane

ension,

Morris

nd Homann

2001)

reported

that

igh

ension f

the

ell

membrane

romotes

xocytosis

nd

low

tension

promotes

ndocytosis.

hese

observationsead

Balu'ka

et

al.

(2005)

to

further

ropose

a

mechanical

mechanism

o

explain

he

perception

f

a

gravitational

ignal

in

plants.

isplacement

f

plant

ell from

he ertical

osition

alters the

gravitationaloading imposed upon

its

plasma

membrane,

ncreasing

ension r

stretching

he

upper

ide of

the

plasma

membranend

decreasing

ension

n the

ower

ide.

This, he uthorsropose,will hift hepositionfthe ynaptic

domains

that secrete

auxin,

resulting

n the

observed

accumulation

f

auxin

at the

bottom f the

displaced

cell

(Friml

et

al., 2002;

Ottenschliger

t

al.,

2003)

and

the

inductionf a

gravitropicesponse.

Balu'ka

et al.

(2003)

never

ncluded

role

for stretch-

activatedmembranehannelsn their

mechanosensing

etwork

model.A second model for

mechanosensing,

ased on

the

adhesion of the

cell membrane o the cell

wall

involves

arabinogalactanroteins

AGPs),

and

wall-associated inase

(WAK),

does include stretch-activatedhannels

Ding

and

Pickard, 993;

Pickard

nd

Fujiki,

005).

Gens et

al.

(2000)

provided

vidence rom

Y-2

tobacco

ells that

mechanosen-

sory

stretch-activated)

alcium-selectiveation

channels re

grouped

n

the

cell membrane

nd are associated

withAGPsand

WAKs,

which

ppear

ofasten hecellmembraneo the

cell

wall. The

grouping

f

thesemolecules nd

channelswas

termed

he

plasmalemmal

eticulum

Gens

et

al.,

2000).

Mechanosensory

alcium-selectiveation hannels

lso have

been

reported

n

the

guard

cells of Vicia

(Cosgrove

and

Hedrich,

991)

and

lily pollen

tubes

Dutta

and

Robinson,

2004);

however,

he

plasmalemmal

eticulum as

only

been

observed n the BY-2 cells

(Pickard

nd

Fujiki,

2005).

The

putative

oleof WAKs

and

AGPs in the

ytoskeleton-plasma

membrane-cell all continuum nd

mechanosensing

was

reviewed

y

Balu'ka

et al.

(2003).

Physiological

memory f

mechanoperception-Most

tud-

ies

designed

o

nvestigate

he

growth esponse

ssociatedwith

mechanoperceptionave beenconductedn actively rowing

plants.Very

ittle s known

egarding

he

bility

f

a

plant

o

perceive

a mechanical

ignal

during

a

nongrowing

r

dormant

eriod

and to

respond

n the

subsequent

rowing

season.

Valinger

t al.

(1994)

provide

he first

vidence f a

possiblememory

n

plants

o recordmechanical

oading uring

winter

dormancy. hey

reported

n their

tudy

on Pinus

sylvestris

.,

that rees an

perceive periodic ending

tress

when

kept

t-60C.

When

he reesweremoved o conditions

favorable

or

growth,

he

bent reeshad

a

thigmomorphoge-

netic

response

when

compared

o nonbent ontrol

rees. ast

studies n

dormancy

nd seasonal mitotic

ctivity

n

apical







October

006]

TELEWSKI-MECHANOPERCEPTIONN

PLANTS

1471

buds

(Carlson

t

al., 1980; Carlson,

1985)

and more

recent

genomic

tudies

see

for

xample

Ko et

al.,

2006)

have

shown

that even

during

so-called

periods

of

dormancy, lants

maintain n active evel of

metabolism.

owever,

he

nature

ofthe toredmechanical

message

nd how t timulates

rowth

after

ormancy

s still

unknown.

Physiological esponses omechanoperception-A ener-alized flow hart f

physiological esponses

o

thigmomecha-

noperception

s

presented

n

Fig.

1. The firstdetectable

response

o a mechanical

ignal

s a

change

n

action

otentials

and electrical

esistance,

hichoccurs within

econds after

perturbation

Sibaoka,

1966; Pickard,

971; Jaffe,

976),

while

mechanical

haking

f stems

locks

phloem

ransport

ithin

to

2

min

fter

erturbation

Jaffe

nd

Telewski, 984;

Jaeger

t

al.,

1988).

The nextmeasurable

hange

ccurs s an ncrease n

intracellulara2+

(for

review, ee

Knight,

000).

For this

reason,

t s

currently

nclear

f

tretch-activateda2+ channels

(Ding

and

Pickard, 993;

Pickard nd

Fujiki,

005)

functionn

the

primaryerception

r are

triggeredy

the

mechanosensing

network

roposed

y

Balu'ka et

al.

(2003).

The function

f

stretch-activatedhannels

s

to facilitatehe

ransport

f Ca2+

Thigmo-Mechanoresponse

ascade

Time

Response

Growth

Increase

n

ction

1

to 10

potentials

nd lectrical

resistance

I

Phloem

ransport

lock

Sto 2

Increasen ntracellulara

Increasen

hydrogeneroxide

(H202)

nd

ther eactive

oxygen pecies

ROS)

4

to 8

nmin

Elongation

ceases

Expression

f almodulinnd

10 o

0

min

calmodulin-related

enes

(TCHI,

TCH2,

TCH3)

ACC and

ethylene iosynthesis

Recovery

30 to

60 min

of hoot

elongation

Expression

f

TCHI, TCH2,

TCH3returns

tobase evels

Phytoalexin-like

ubstances

eak

Lipoxygenase

LOX)

mRNA

ranscription

Callose

ynthesis

nd

deposition

2 to9 h

Ethyleneynthesiseaks

Increase

n

ell

6 to24 h

division

y

vascular

cambium

Callose nd

thylene

eturn

o

pre-

24 h

mechanicaltressevels

Fig.

1. Flow chartof the

time

course of

physiological

nd

growth

response

o mechanical

tress. ee

text or

itation

nformation.

across the cell membrane

nd into thecell in

response

o

mechanical

tress

Ding

and

Pickard, 993;

Pickard nd

Fujiki,

2005).

An

increase

n

cytoplasmic

alcium n

response

o

mechanical

tress has been

documented n

several

plant

systems

Toriyama

nd

Jaffe,

972;

Knight

et

al.,

1991,

1992;

Trewavas nd

Knight,

994;

Legu6

et

al., 1997;

Pickard

and

Fujiki,

005).

Hydrogenperoxide H202) and otherreactiveoxygen

species

ROS)

are

part

f the

defense

esponse

f

plants,

or

example,

n

fungal

ttack

nvolving

mechanical

nsertion

ia

growth

f a

fungal

enetration

eg through

hehost ell

wall

(for

eview,

ee

Sutherland,991;

Mehdy,

994).

Yahraus

t

al.

(1995)

inducedan oxidative

burst

n

cultured

oybean

[Glycine

max

L.)

Merrill]

ells in

response

o

osmotic tress

(altered

urgor ressure)

nddirect

hysical

ressure

mechan-

ical

stress).

he

inductionf

ROS and an

increase n

cytosolic

Ca2+

appear

o be

concurrent,

nd

ROS havebeen

uggested

o

regulate

a2+ channel

ating

Mori

and

Schroeder,

004).

Jaffe

1976)

reported

mechanical tress

aused a

complete

cessation f

longation

rowth

min

fter orce

pplication,

ith

the

growth

ate

resuming

fter15 to 30

min

in

Phaseolus

vulgaris.

outand t

al.

(2000)

reported

imilar

esultswith

cessationfelongationrowth.3 ? 3.7min fternductionf

a mechanicaltressn

the asal tem

f omato

lants;

longation

ceased and

subsequently

equired

0.3

?

3.5

min

of

recovery

time efore

normal ate

f

elongation rowth

esumed.

hey

concludedthat this is

evidence for a

rapid,

acropetally

transmitted

ignal

from

he

point

of

flexure o the

actively

elongating

one

directly

elow the

apical

meristem.

he

existence f

an

acropetally

ransmitted

higmomorphogenetic

signal

was first

eported y

Erner

t

al.

(1980),

who

also

concluded he

transportable

actor

was not

ethylene.

ubse-

quently,

akahashi

nd Jaffe

1984)

reported

he

presence

f

phytoalexin-like

ubstances

n

xtractsf

mechanically

erturbed

plants,

hich

eaked

n

concentrationh

after

application

f

mechanical

tress

nd,

when

applied

to

nonstressed

lants,

elicited

thigmomorphogenetic-likeesponse.

Apparently,

essation f

elongation rowth

may

actually

precede

he

apid p regulation

expression)

f

calmodulin

nd

calmodulin-related

enes

TCHI,

TCH2,

TCH3),

which

was

observed n

Arabidopsis

0 to 30

min

fter

mechanoperception

of

touch,wind,

r rain timulus

ndreturnedo

base

evels

by

1 to 2 h

(Braam

nd

Davis,

1990).

Arabidopsis

CH3

encodes

for

Ca2+

binding rotein

hich s

expressed

n

response

o

both

externally

pplied

mechanical forces

and

internally

generated rowth

trains

uring

issue

development

n

the

absence f

n

external

echanicaltress

Sistrunk

t

al.,

1994).

Arabidopsis

CH4 encodesfor

xyloglucan

ndotransglyco-

sylase

ndwas

co-expressed

ith he

ther

CH

genes

Xu

et

al.,

1995).

The

expression

f

xyloglucan

ndotransglycosylase

in

response

o

windwas located

n

cells

undergoing

xpansion

(Antosiewicztal., 1997).

Touch, wind,

nd

wounding

ll

induced ncreased

ipoxy-

genase

(LOX)

mRNA

transcription

n wheat

(Triticum

aestivum

.)

seedlings

Mauch

et

al.,

1997).

The

mechanical

stress

nduced

esponse

ccurred

ithin hafter

reatment,

nd

the amount f

transcript

as

reported

o be

strongly

ose-

dependent.

OXs are involved r

implicated

n

a number f

metabolic

athways

ssociatedwith

plantgrowth

nd devel-

opment,

BA

biosynthesis,

enescence,

mobilization f

lipid

reserves,

wound

responses,

resistance o

pathogens,

formation

of

fatty

cid

hydroperoxides,

nd

synthesis

f

asmonic

cid

and traumatic

cid

for

eview,

ee

Mauchet

al.,

1997).







1472

AMERICAN JOURNALOF

BOTANY

[Vol.

93

As

previously

mentioned,

allose

synthesis

nd

deposition

are nduced

y flexing

mechanicaltress

n the

phloem

fbean

(Phaseolus

vulgaris)

nd

oblolly ine

Pinus

taeda)

stems

h

after

mechanical

timulation,

eaking

fter

h and

being

re-

absorbed

y

25 h

Jaffe

nd

Telewski,

984;

Jaffet

al.,

1985).

Callose

deposition

also

occurs within5

min

of

gravity

stimulation

n

Zea

mays

and Pisum

sativum.

eposition

f

calloseoccurredirst n theupper ide ofdisplaced tems,nd

after

-3

h,

the

pattern

as

reversed.

he callose

nhibitor,

-

deoxy-D-glucose

DDG),

blocked callose formation

nd

considerably

educed

ravitropicending

n

both

pecies

Jaffe

and

Leopold,

1984).

Sound

n

the ltrasonic

ange

was

reported

to induce

ransient

allose

formationn

cotton eed

(Currier

and

Webster,

964).

Ethylene iosynthesis

as been

reported

o

be

a

fairly

ubiquitous

esponse

o

a

number

f

environmental

tresses,

including

mechanical tresses

for

review,

ee Abeles

et

al.,

1992;

Bleecker

nd

Kende,

000),

and

several esearchers

ave

suggested

thylene

erves as a

signaling

molecule.

Wind,

touch,

nd

dynamic

lexing

ave

all

been

shown to induce

ethylene

ormation

n

vascular

lants

for

eview,

ee

Telewski,

1995),

and

ethylene

as

been

reported

o

be

involved

n the

gravitropicesponse, response o displacementesultingn

static

bending

with

respect

o

the

gravitational

orce

vector

(Savidge

et

al., 1983;

for

eview,

lso see

Steedet

al.,

2004).

Ethylene roduction

n

response

o mechanicaltress

eaks

2 h

in Phaseolus

vulgaris

Biro

and

Jaffe,

984),

nd 9 h inPinus

taeda

(Telewski

and

Jaffe,

986)

afterforce

application.

Increased

ell divisions

by

the vascular

ambium

ccurred

within

h after

he

application

f mechanical tress

n P.

vulgaris

Biro

et

al.,

1980).

The

roleof

ethylene

n

response

o

mechanical

tresses

ppears

to

affect

econdary rowth

nd

subsequent evelopment

nd differentiationf

the

vascular

cambium

ndnot

mpact rimaryrowthelongation

r

height

growth)

ssociated

with

pical

meristems

Coutand

t

al.,2000;

for

eview,

ee

Braam,

005).

The role

f uxin

n

gravitropism

as

been

tudied or lmost

80

years,

nd ts ole n

plant

ropisms

eading

o the

ostulation

of the

Cholodny-Went

ypothesis

Went

nd

Thimann,

937)

has stood

hetest f

time

Gutjahr

t

al.,

2005;

Esmonet

al.,

2006).

Surprisingly,

ittle

nformationxists

on the role

of

auxin nd

other

lant

rowth egulators

n

the

higmomorpho-

genetic

response.

Erner and Jaffe

1982)

reported

the

accumulation

f auxin-like ubstances nd

higher

evels

of

abscisic cid

ABA)

in

response

o

mechanical

ending.

hese

authors

ypothesized

he

accumulationf these

plantgrowth

regulators

esulted rom

thylene

roduction

arlier

n the

thigmomorphogenetic

esponse

nd was

responsible

or

the

reduction

n nternode

shoot)

longation.

owever,

ohnsont

al.,

(1998)

challenged

his

hypothesis

hen

they

observed

ethylene

utantstill

espond

o mechanical

erturbations

ith

a reductionn shootelongation. he role of plant growth

regulators

n the

post mechanoperception-thigmomorphoge-

netic

esponse

s stillwide

open

for

nvestigation.

Future areas

for investigation-As

s evidenced

n

this

review,

he

fieldof

study

n

mechanosensing

nd mechano-

perception

n

plants

s

progressingapidly

nd

supports

he

proposal

f

a

unified

ypothesis

f

plantperception

f the

mechanical

nvironment.ne area stands

ut,

which

equires

further

lucidation,

pecifically ntegrating

he role of the

sensing

networkt the

cytoskeleton-plasma

embrane-cell

wall

linkage

withthe

plasmodemata

Baluika

et

al.,

2003,

2005)

and

the

presence

f

mechanosensory

alcium-selective

cation

channels

Cosgrove

and

Hedrich,

1991;

Ding

and

Pickard, 993;

Dutta

and

Robinson,

004)

and

the

plasma-

lemmal eticulum

Gens

t

al., 2000;

Pickard nd

Fujiki,

005).

Are

they

ompeting

odelsfor

mechanosensoryystems

n

plants,

r are

they

nterconnectednd

co-functional,

nd what

is

the

pecific ignal

hat

s transmitted

y

the

network?

Anotherrea of nterestocuses nhowplants ifferentiate

between hevariousmechanical

ignals.

At the

most

implistic

level,

from

mechanoperception

f a mechanical

ignal by

a

plant

ell

to

the

ascade

of nitial

hysiological

esponses,

here

appears

o

be

very

ittle ifferencen the

esponse athway

hat

would

llow

fordiscriminationn

programmed

eaction o the

variety

f

mechanical

tresses

resent

n

the

nvironment.

n

example

s

the ifferentiationf

response

etween

ravitropism

vs.

thigmomorphogenesis

n

woody

plants.

Reactionwood

formations

a

well-documented

ravitropicesponse

n

woody

plants

for

eview,

ee

Timell,

1986a-c).

A

multitudef field

observations

uggest

hat wind

can stimulate he vascular

cambiumo

produce

eaction ood nthe ree

runk,

ven f he

tree

howsno

signs

of

having

been

displaced

with

espect

o

gravity

see

Timell,

1986c).

Experimentally,

arson

1965)

also reportedheformationf compressionwood in Larix

seedlings

xposed

o an artificial nilateral

ind.

Although

t

appears

hat

mechanoperception

n

plants

an be

very apid,

he

thresholdf

exposure

r

presentation

o a

gravitropic

timulus

may

require

everalminutes o

hours

the

presentation

ime)

(for

review,

ee

Timell,

1986c).

If a

plant

s

displaced

with

respect

o

gravity

nd returnso its vertical

rientationefore

the

presentation

ime

is

met,

the

plant

will not exhibit

gravitropic

urvature.norder o

solate

gravitropic

esponse

from

a

thigmomorphogeneticesponse,

Telewski

(1989)

carefully

lexed

stems

of Abies

fraseri

Pursh.)

Poir. and

returned

hem o

the

vertical

rientationefore

he

required

presentation

ime or nitiation

f

a

gravitropic

esponse.

he

wood

produced

n

response

o this

dynamic

lexure

ossessed

characteristicshatwere ntermediateetweennormalwood

and

compression

ood.

It would

be

interesting

nd useful o

sort out

how the

mechanoperceptive

ystem

f

plant

cells

discerns

nd

differentiatesetween he variousmechanical

forces

mposed

pon

he

plant.

What

s the

iming

mechanism

required

n

meeting

he

presentation

ime of

the

gravitropic

response

n

response

o static

isplacement

nd

how

does this

differ

rom he

perception

f

dynamic

waying?

or

example,

how

does

the

mechanosensory

ystemdistinguish

etween

gravity,

ind

way,

vibration,

nd

sound?

The

application

f currenttate-of-the-art

nalytical

ools,

such

as

in

situ

hybridization

nd

visualization

methods or

locating

ene expression

nd

plant

growth egulators,

ould

provide

moredetailed nformationn the

putative

oles of

auxins nd other

lant

rowth egulators

o further

haracterize

the thigmomorphogeneticesponse pathway. Finally, as

mentioned

y

Braam

(2005),

the

application

f

molecular

biological

methods,

ncluding

microarrays

nd

bioinfomatics,

willfurtherlucidate he

rray

f

plant esponses

o mechanical

stresses

nd

may help

to

identify

he different

hysiological

responses

hat ccur after

mechanoperception

nd to define

developmental

hanges pecific

o

a

specific

mechanical

ignal.

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F.

B.,

P. W.

MORGAN,

AND

E.

SALTVEIT JR.

1992.

Ethylene

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plant

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Press,

San

Diego,

California,

SA.







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2006]

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R. R.

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