General relations of stomatal responses to xylem sap abscisic acid under stress in the rooting zone...

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Flora 202 (2007) 624–636

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General relations of stomatal responses to xylem sap abscisic acid under

stress in the rooting zone – A global perspective

Hermann Heilmeiera,�, Ernst-Detlef Schulzeb, Jiang Fanc, Wolfram Hartungc

aInterdisziplinares Okologisches Zentrum, TU Bergakademie Freiberg, Leipziger Str. 29, D-09599 Freiberg, GermanybMax-Planck-Institut fur Biogeochemie, POB 100164, D-07701 Jena, GermanycJulius-von-Sachs-Institut der Universitat Wurzburg, Lehrstuhl Botanik I, Julius-von-Sachs-Platz 2, D-97082 Wurzburg, Germany

Received 7 June 2007; accepted 7 June 2007

Dedicated to Prof. Dr. Dr. h.c. mult. Otto Ludwig Lange on the occasion of his 80th birthday

Abstract

A sensitivity factor that quantifies the responsiveness of stomata to xylem sap abscisic acid concentration ([ABA]xyl)is described, using the relation between [ABA]xyl and maximum leaf conductance (gmax). Plotting gmax against thisfactor results in a common linear relationship for woody and herbaceous species from boreal to (semi-) arid climates.The global distribution of the sensitivity factor reveals an unexpected pattern which is inverse to rainfall, i.e., plants inhumid climates respond more sensitively to ABA than plants in arid areas. The implications for the response of naturalvegetation and consequences for agriculture are discussed.r 2007 Elsevier GmbH. All rights reserved.

Keywords: ABA; Irrigation; Leaf conductance; Plant functional types; Plant life forms; Stomatal sensitivity

Introduction

The role of abscisic acid (ABA) as a plant stresshormone is well established. Under a range of stressconditions ABA biosynthesis is initiated in differentplant organs. After transport to target cells, such asstomata, plant water relations can be maintained oreven improved by reduction of stomatal transpirationavoiding damage by desiccation (Davies and Zhang,1991; Hartung and Davies, 1991; Schulze, 1993).

Under mild stress conditions whenever the soil startsto dry, ABA is being transported from the root to theshoot and it thus acts as a long distance stress signal.

e front matter r 2007 Elsevier GmbH. All rights reserved.

ra.2007.06.002

ing author. Tel.: +49 3731 39 3208;

9 3012.

ess: [email protected] (H. Heilmeier).

Zhang and Davies (1987) were the first to describe therelation between ABA concentration in the xylem sap([ABA]xyl) and leaf conductance (g). For field-grownplants, the first relation between [ABA]xyl and maximumleaf conductance (gmax) was shown by Wartinger et al.(1990) in desert grown almond trees. They found abiphasic relation between [ABA]xyl and gmax withconcentration ranges of [ABA]xyl for both highly andless sensitively responding stomata.

The relation between [ABA]xyl and gmax has beeninvestigated since then for a large range of plants, bothherbaceous and woody, originating from moderate andextreme habitats (for references see Table 1). It turnedout that in many cases the relationship between [ABA]xyland gmax was very similar – indicating a general principlefor the stress physiological role of ABA within terrestrialplants.

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Table

1.

Listofplants

includingtheirreferenceswhichwereusedto

establish

therelationofFig.3

Species

Life

form

PFT

Location

ofgrowth

Rooting

condition

Drivingfactor

Sampling

ofxylem

sapat

gmax

Methodof

xylem

sap

sampling

gmax

Sensitivity

factor

Reference

Aca

cia

con

fusa

WT

GP

Soildrought,split

root

No

PP

0.14

�0.0835

LiangandZhang(1999)

Aca

cia

con

fusa

WT

GP

Soilcompaction,soil

drought

No

PP

0.08

�0.8618

Lianget

al.(1996)

Aca

cia

con

fusa

WT

GP

Splitroot

No

PP

0.09

�0.0470

Lianget

al.(1997)

Ace

rp

seu

do

pla

tan

us

WN

GP

Splitroot

Yes

PS

0.10

�0.1993

KhalilandGrace

(1993)

Ace

rru

bru

mW

NF

SSoildrought

No

PS

0.16

�0.1115

Augeet

al.(2000)

Ace

rsa

cch

aru

mW

NG

PSoildrought

No

PS

0.14

�0.0420

Loew

ensteinandPallardy

(1998)

Bet

ula

pen

du

laW

NG

PSplitroot

No

PS

0.38

�0.2592

Fort

etal.(1998)

Bu

xu

sm

icro

ph

yll

aW

SF

PSoildrought

Yes

PS

0.09

�0.0374

AbrilandHanano(1998)

Ca

psi

cum

an

nu

um

HL

GP

Rootrestriction,soil

drought

Yes

PS

0.60

�0.4378

IsmailandDavies(1998)

Ca

psi

cum

an

nu

um

HL

GP

Soildrought

Yes

PS

0.50

�0.3968

Ismailet

al.(2002)

Ca

psi

cum

an

nu

um

HL

GP

Soildrought

Yes

PS

0.40

�0.3205

Ismailet

al.(2002)

Ca

sta

nea

sati

vaW

WG

PSplitroot

Yes

PS

0.50

�0.4522

Maurelet

al.(2004)

Cea

no

thu

sth

yrs

iflo

rus

WS

FP

Soildrought

No

PS

0.10

�0.0545

Tenhunen

etal.(1994)

Cea

no

thu

sth

yrs

iflo

rus

WS

FP

Soildrought

Yes

PS

0.15

�0.0508

AbrilandHanano(1998)

Co

rnu

sfl

ori

da

WN

FS

Soildrought

No

PS

0.16

�0.1150

Augeet

al.(2000)

Gly

cin

em

ax

HL

GP

Soildrought

No

PP

0.54

�0.2468

Liu

etal.(2003)

Gly

cin

em

ax

HL

GP

Soildrought

No

PP

0.56

�0.2100

Liu

etal.(2005a)

Hel

ian

thu

sa

nn

uu

sH

LG

PPressurizedpot

No

PC

0.65

�0.3673

Schurr

etal.(1992)

Hel

ian

thu

sa

nn

uu

sH

LG

PSoildrought

No

PS

2.25

�1.4382

TardieuandSim

onneau

(1998)

Hel

ian

thu

sa

nn

uu

sH

LF

PSoildrought

No

PS

2.25

�1.6579

TardieuandSim

onneau

(1998)

Ho

rdeu

mvu

lga

reH

3G

PSoildrought

No

PS

0.55

�0.3673

Borelet

al.(1997)

Ho

rdeu

mvu

lga

reH

3G

PSoildrought

No

PS

0.55

�0.3976

Borelet

al.(1997)

Ju

gla

ns

nig

raW

NG

PSoildrought

No

PS

0.04

�0.0255

Loew

ensteinandPallardy

(1998)

Leu

caen

ale

uco

cep

ha

laW

TG

PSplitroot,soil

drought

No

PP

0.21

�0.1420

LiangandZhang(1999)

Leu

caen

ale

uco

cep

ha

laW

TG

PSplitroot,soil

drought

No

PP

0.21

�0.2284

LiangandZhang(1999)

H. Heilmeier et al. / Flora 202 (2007) 624–636 625

ARTICLE IN PRESS

Table

1.(c

on

tin

ued

)

Species

Life

form

PFT

Location

ofgrowth

Rooting

condition

Drivingfactor

Sampling

ofxylem

sapat

gmax

Methodof

xylem

sap

sampling

gmax

Sensitivity

factor

Reference

Leu

caen

ale

uco

cep

ha

laW

TG

PSplitroot

No

PP

0.18

�0.0953

Lianget

al.(1997)

Liq

uid

am

ba

rst

yra

cifl

ua

WN

FS

Soildrought

No

PS

0.50

�0.1676

Augeet

al.(2000)

Lit

sea

glu

tin

osa

WT

GP

Soilcompaction,soil

drought

No

PP

0.10

�0.0787

Lianget

al.(1996)

Lu

pin

us

alb

us

HL

GP

Soildrought

Yes

PS

0.80

�0.4210

CorreiaandPereira

(1995)

Nic

oti

an

a

plu

mb

ag

inif

oli

a

HL

GP

Soildrought

No

PS

1.50

�0.7314

Borelet

al.(2001)

Pic

easi

tch

ensi

sW

EF

PSoildrought

No

PS

0.15

�0.1959

Jacksonet

al.(1995)

Pin

us

sylv

estr

isW

EF

PSoildrought

No

PS

0.80

�0.4521

Jacksonet

al.(1995)

Pin

us

sylv

estr

isW

EF

SSoildrought

No

PS

0.26

�0.2100

Sturm

etal.(1998)

Po

pu

lus

trem

ula

WN

FS

Soildrought

Yes

PS

0.28

�0.0663

Aasamaaet

al.(2004)

Po

pu

lusspec.

Wn.d.

Fn.d.

Soildrought

Yes

n.d.

0.40

�0.2351

TardieuandSim

onneau

(1998)

Pru

nu

sa

viu

mW

NF

SSoildrought

No

PS

0.50

�0.1701

HartungandHeilm

eier

(1993)

Pru

nu

sd

ulc

isW

WF

SSoildrought

Yes

PS

0.40

�0.2948

Wartinger

etal.(1990)

Pru

nu

sp

ersi

caW

WF

SSoildrought

Yes

PS

0.20

�0.2513

Correiaet

al.(1997)

Qu

ercu

sa

lba

WN

GS

Soildrought

No

PS

0.60

�0.2976

Augeet

al.(2000)

Qu

ercu

sp

rin

us

WN

FS

Soildrought

No

PS

0.50

�0.3667

Augeet

al.(2000)

Sa

lix

nig

raW

NG

PSoildrought

No

PS

1.12

�0.5352

Loew

ensteinandPallardy

(1998)

So

lan

um

tub

ero

sum

HL

GP

Soildrought

No

PP

0.75

�0.6102

Liu

etal.(2005b)

Til

iaco

rda

taW

NF

SSoildrought

No

PS

0.05

�0.0607

Niinem

etset

al.(1999)

Tri

foli

um

sub

terr

an

eum

HL

FS

Soildrought

No

PS

1.00

�0.6096

Sociaset

al.(1997)

Vig

na

un

gu

icu

lata

HL

GP

Soildrought

Yes

PS

0.34

�0.1631

Duanet

al.(1996)

Vig

na

un

gu

icu

lata

HL

GP

Soildrought

No

PS

0.22

�0.0922

Ebel

etal.(1997)

Vit

isvi

nif

era

WW

FS

Soildrought

Yes

PS

0.46

�0.5804

Correiaet

al.(1995)

Zea

ma

ys

H4

GP

Osm

oticstress

Yes

PP

0.08

�0.7474

Stikic

andDavies(2000)

Zea

ma

ys

H4

GP

Osm

oticstress

Yes

PP

0.07

�0.0544

Stikic

andDavies(2000)

Zea

ma

ys

H4

GS

Soilcompaction,soil

drought

Yes

PS

0.24

�0.1163

TardieuandDavies(1992)

Zea

ma

ys

H4

FS

Soilcompaction,soil

drought

No

PS

0.27

�0.1740

Tardieuet

al.(1992)

Zea

ma

ys

H4

FS

Soildrought,ABA

feeding

Yes

PS

0.28

�0.1396

Tardieuet

al.(1993)

Zea

ma

ys

H4

FP

ABA

feeding

No

Exudate

0.13

�0.0429

ZhangandDavies(1990)

Additionally,life

form

(herbaceous,H,andwoody,W)andplantfunctionaltype(PFT;3:cultivatedC3grasses,4:cultivatedC4grasses,L:broad-leaved

crops,N:temperate

deciduousbroad-leaved

trees,W:warm

deciduousbroad-leaved

trees,S:sclerophyllousscrub,E:evergreen

coniferoustrees,T:tropicaltrees),locationofgrowth

(greenhouse,G,vs.field,F),rootingconditions(pots,P,or

unrestricted

naturalsoil,S),drivingfactorforthevariationin

xylem

sapABA

concentrationandleafconductance,coincidence

ofxylem

sapsamplingandmaxim

um

leafconductance

(gmax)and

methodofxylem

sapsampling(PC:balancingpressure

inPassioura-typepressure

chamber,PP:pressurizingdetopped

potted

plantin

pressure

chamber,PS:pressurizingexcisedshootorleafwith

pressure

chamber)are

given

(n.d.:nodata).

H. Heilmeier et al. / Flora 202 (2007) 624–636626

ARTICLE IN PRESSH. Heilmeier et al. / Flora 202 (2007) 624–636 627

In the following paper, (1) it will be tested whethersuch a general relation exists, (2) such a relationship willbe quantified for individual species on the basis of anewly defined stomatal sensitivity factor, and (3) thehypothesis will be tested that the stomatal sensitivityfactor is related to physiological performance of theplants as indicated by maximum leaf conductance. Inaddition the relationship between the stomatal sensitiv-ity factor and global vegetation patterns will beinvestigated, and practical agricultural implications ofsuch a sensitivity factor will be discussed.

The importance of stomatal sensitivity to

[ABA]xyl

Already in 1975, Raschke pointed out that stomataresponded to ABA when intercellular CO2 was increasedalthough bulk ABA content of the leaves remainedunchanged (Raschke, 1975). He explained this phenom-enon by a significantly increased stomatal sensitivity toABA. Later, Burschka et al. (1983) confirmed theimportance of changing sensitivity of stomata forArbutus unedo plants growing in a natural macchia.Despite the high amounts of leaf ABA which againshowed small diurnal fluctuations only, the injection oftiny amounts of ABA only to the petiole resulted indrastic responses to the applied ABA. This responsediffered during the course of the day pointing to achange of sensitivity. Diurnal variation in the sensitivityof stomata to xylem sap ABA under field conditions hasalso been found by Tardieu and Davies (1992) andCorreia et al. (1995, 1997). The more pronouncedstomatal response to [ABA]xyl in the afternoon in maizeplants in the experiments of Tardieu and Davies (1992)was attributed to sensitising of stomata by lowepidermal water potentials. In contrast, in field-grownalmond trees leaf conductance was suppressed by high[ABA]xyl during daily courses at leaf water potentials(cl) below �3.2MPa only, whereas for a less critical leafwater status stomatal response to diurnal changes in[ABA]xyl was independent of cl (Hartung and Heilmeier,1993). This agrees with a unique relationship betweenleaf conductance and [ABA]xyl regardless of cl in therange from 0 to �3MPa for sunflower plants subjectedto a variety of treatments (Tardieu et al., 1996). On theother hand, for the same species Schurr et al. (1992)found contrasting sensitivities of stomatal opening to[ABA]xyl as dependent on xylem sap pH, nitrate orcalcium concentration. Alkalinisation of xylem sap is acommon effect of various environmental stressors(Hartung and Radin, 1989; Wilkinson et al., 1998);however, stomatal response to elevated xylem pH isvariable (Dodd, 2005). Bahrun et al. (2002) propose asequence of events for maize plants responding to

progressive soil moisture deficit, starting with a decreasein xylem nitrate concentration and a corresponding shiftin xylem pH, which initiate de novo ABA synthesis inroots and ABA release into the xylem, causing stomatalconductance to decrease before a fall in leaf waterpotential. Also environmental conditions such astemperature and vapour pressure deficit can influencethe apparent stomatal sensitivity to ABA. These andother examples are cited and discussed by Trejo et al.(1993, 1995), Dodd et al. (1996) and Dodd (2003, 2005).

As for diurnal courses, a number of studies shows aclose relationship between xylem sap ABA concentra-tion and leaf conductance for an extended period, e.g.,during soil drying for several days to weeks. Periods ofhigh maximum leaf conductances (gmax) and low[ABA]xyl during early stages of soil drying followed bylow gmax and high [ABA]xyl during periods with waterdeficits have been documented both for woody (Augeet al., 2000; Jackson et al., 1995; Khalil and Grace, 1993;Liang and Zhang, 1999; Liang et al., 1996, 1997; Sturmet al., 1998; Wartinger et al., 1990) and herbaceousspecies (Correia and Pereira, 1995; Ismail and Davies,1998; Ismail et al., 2002; Liu et al., 2003, 2005a; Sociaset al., 1997). In these cases, it is essential to excludeshort-term sources of environmental variability like thetremendous effect of humidity on stomata first docu-mented by the group of Otto L. Lange (e.g., Lange et al.,1971). However, using a standardized protocol in long-term experiments, e.g., measurement of g at saturatinglight intensity, but non-limiting VPD, should allow toreveal a possible general relationship between gmax and[ABA]xyl. Dodd (2005) concludes that ‘‘in a givenspecies, this relationship is commonly unified acrossdifferent growing conditions, from leaf to leaf onindividual plants, and from day to day as the plantdevelops’’. In the following these individual responsepatterns for a number of plant species from theliterature will be synthesised into a general stresssensitivity framework.

Processing the data

A literature study was performed to select experi-ments in which plants subjected to different stresstreatments (e.g., drought, soil compaction, split-rootsystems, osmotic stress, feeding of ABA) were assayedfor both leaf conductance and xylem sap ABAconcentration during the whole treatment period. Table1 gives the references of those data analysed in thisstudy. Three case studies only did not show a relation-ship between g and [ABA]xyl (Triboulot et al., 1996:Quercus spec.; Niinemets et al., 1999: Populus tremula;Sobeih et al., 2004: Lycopersicon esculentum). Because asensitivity factor could not be calculated, these studies

ARTICLE IN PRESSH. Heilmeier et al. / Flora 202 (2007) 624–636628

were not included. At present we have no explanationfor these missing relation, special experimental condi-tions may be the reason. When there were several datasets available from any one publication (Correia et al.,1995, 1997; Tardieu and Simonneau, 1998; Tardieuet al., 1992, 1993), e.g., for diurnal courses, data fromthe morning were selected when minimum influence ofVPD or cl was assumed.

Experiments were classified into the driving factor forvariation in g and [ABA]xyl, location of growth (green-house or field), rooting conditions (grown in pots withsoil or in unrestricted soil at the natural site). In additionplants were separated into herbaceous or woody growthforms, and into eight plant functional types (cultivatedC3 and C4 grasses, broad-leaved crops, temperatedeciduous broad-leaved trees, warm deciduous broad-leaved trees, tropical trees, sclerophyllous scrub, ever-green coniferous trees). Thus plant species in this studycover a wide range of life forms from annual crop plantsto long-living trees, and they grow from humid to semi-arid climates (Table 1). Nevertheless, among herbaceousplants the database shows a bias towards agriculturalspecies, especially broadleaved crops. For trees, broad-leaved deciduous species predominate.

In order to reduce the amount of data handling,paired data for leaf conductance and [ABA]xyl werefitted by eye and some 4–6 data pairs taken from eachcurve. These data pairs were plotted for each plantspecies, yielding a rather homogeneous pattern for allplants (Fig. 1 for both woody and herbaceous plants).

0

1

2

3

0

0

g (

mol m

-2 s

-1) g (

mol m

-2 s

-1)

[ABA]xyl (µ

40002000

Herbaceous species

Woody species

0.8

0.6

0.4

0.2

0.0

Fig. 1. Relation between xylem sap abscisic acid concentration ([A

species. Data are from a literature survey (cf. Table 1).

When plotting the data for individual species, therelation between g and [ABA]xyl was exponential inmost cases (Fig. 2a). Using a logarithmic scale for[ABA]xyl, these curves could be linearised (Fig. 2b). Forabout 10% of all studies not the whole data range wastaken, but only those data points at the lower end of[ABA]xyl which yielded a linear relationship (e.g.,Trifolium subterraneum and Zea mays (Tardieu et al.,1992) in Fig. 2b).

The slope dg/dlog[ABA]xyl, i.e., the response of leafconductance to an increase in ABA concentration of thexylem sap, was interpreted as stomatal sensitivity to achange in xylem sap composition in response to externalstress. The sensitivity factor was plotted against max-imum leaf conductance (gmax) in order to test thehypothesis that stomatal sensitivity is related to thephysiological performance of the plants. Maximum leafconductance was assumed to indicate a plant’s physio-logical performance due to the close relationshipbetween gmax and maximum rate of photosynthesis(Korner, 1994) or leaf nitrogen concentration (Schulzeet al., 1994). The relationship between stomatal sensi-tivity factor and gmax was tested via linear regressionanalysis. Following this procedure, several linear regres-sion models were established.

First, the regression model was established for thecomplete data set (radj

2¼ 0.883, po0.001; Table 2).

Residuals were homogenous for the complete datarange. Next the reliability of the data set was assessedby several tests by analysis of covariance, with stomatal

mol m-3)

[ABA]xyl (µmol m-3)

1000080006000

16001200800400

BA]xyl) and leaf conductance (g) for woody and herbaceous

ARTICLE IN PRESS

3

2

1

00 100 200 300 400 500 600 700 800 900

g (

mol m

-2 s

-1)

3

2

1

00 1 2 3 4

g (

mol m

-2 s

-1)

Helianthus annuus (Tardieu and Simonneau, 1998)

Trifolium subterraneum (Socias et al., 1997)

Zea mays (Tardieu and Davies, 1992)

Zea mays (Tardieu et al., 1992)


Helianthus annuus (Tardieu and Simonneau, 1998)

Trifolium subterraneum (Socias et al., 1997)

Zea mays (Tardieu and Davies, 1992)

Zea mays (Tardieu et al.,1992)


ABAxyl (µmol m-3)

log (ABAxyl (µmol m-3))

Fig. 2. Relation between xylem sap abscisic acid concentration ([ABA]xyl) and leaf conductance (g) for single-herbaceous species

grown in the field (a) on a linear scale, (b) on a logarithmic scale for [ABA]xyl.

Table 2. Linear regression model for stomatal sensitivity as

dependent on maximum leaf conductance (gmax)

Effect Coefficient Std error t P

Constant 0.000 0.020 �0.015 0.988

gmax �0.624 0.031 �19.846 o0.001

Dependent variable: stomatal sensitivity, N: 54, adjusted R2: 0.883.


sensitivity as the dependent factor, different experimen-tal procedures or plant types as grouping factor andgmax as covariate.

Goodger et al. (2005) had pointed out that differenttechniques of xylem sap sampling may yield contrastingconcentrations e.g., of ABA for both well-watered andwater-stressed plants. Therefore, first the effect of xylemsap sampling on stomatal sensitivity was tested.Although the main effect of sampling technique wasnot significant, there was a significant interactionbetween sampling method and gmax (Table 3a), due toa relatively low sensitivity for Helianthus annuus xylemsap recovered under balancing pressure in a Passioura-type pressure chamber (Schurr et al., 1992).

Second, in view of contrasting patterns of diurnalcourses for both g and [ABA]xyl documented in theliterature it was necessary to test whether the time ofsampling xylem sap and measuring g was of relevance.For example, Tardieu et al. (1991), Tenhunen et al.(1994) and Jackson et al. (1995) showed an increasingtrend for [ABA]xyl during a daily course with g

decreasing in the afternoon, whereas Correia et al.(1997) found a steady decrease in g with constant[ABA]xyl during the day. Therefore, the complete dataset was divided into experiments in which, according tothe long-term pattern between [ABA]xyl and gmax firstestablished by Wartinger et al. (1990), both variableswere measured at the time of gmax on the one handand the rest on the other hand (see Table 1). Therewas no significant effect of the experimental protocol(Table 3b). Therefore, we conclude for our data set thatboth long-term experiments in which there was a clearrelationship between gmax and [ABA]xyl and experimentsin which there was an impact of environmental factorsvarying on a short time scale like VPD or plant-internalfactors like leaf water potential do not differ withrespect to their effect on stomatal sensitivity.

ARTICLE IN PRESS

Table 3. Analysis of covariance for the effect of method of xylem sap sampling, time of xylem sap sampling, driving factor for

variation in gmax and xylem sap ABA concentration, growth conditions, plant growth form and plant functional type (grouping

factors) on stomatal sensitivity as dependent on maximum leaf conductance (covariate)

Source Sum-of-squares df Mean-square F-ratio P

(a) Effect of method of xylem sap sampling: pressurizing leaf (n ¼ 16) or shoot (n ¼ 23), pressurizing detopped plants (n ¼ 12),

Passioura-type pressure chamber (n ¼ 1), root exudate (n ¼ 1)

Sampling method 0.004 2 0.002 0.199 0.820

gmax (covariate) 0.035 1 0.035 3.731 0.060

Sampling method� gmax 0.171 4 0.043 4.612 0.003

Error 0.416 45 0.009

Dependent variable: stomatal sensitivity, N: 53, squared multiple R: 0.918

(b) Effect of time of xylem sap sampling: coincidence with maximum leaf conductance (n ¼ 18) or not (n ¼ 32)

Sampling time 0.004 1 0.004 0.448 0.507

gmax (covariate) 1.097 1 1.097 118.5 o0.001

Sampling time� gmax 0.001 1 0.001 0.073 0.789

Error 0.426 46 0.009


(c) Effect of driving factor: soil drought (n ¼ 37), split-root system+soil drought (n ¼ 8), soil compaction (n ¼ 4), pressurized pot

(n ¼ 1), osmotic stress (n ¼ 2), ABA feeding (n ¼ 2)

Driving factor 0.003 3 0.001 0.074 0.990

gmax (covariate) 0.001 1 0.001 0.132 0.718

Driving factor� gmax 0.036 5 0.007 0.743 0.596

Error 0.423 44 0.010


(d) Effect of location of growth: greenhouse (n ¼ 31) vs. field (n ¼ 23)

Location of growth 0.009 1 0.009 0.872 0.355

gmax (covariate) 4.488 1 4.488 422.4 o0.001

Growth location� gmax 0.051 1 0.051 4.799 0.033

Error 0.531 50 0.011


(e) Effect of rooting conditions: pots (n ¼ 37) vs. unrestricted soil (n ¼ 16)

Rooting conditions 0.011 1 0.011 1.067 0.307

gmax (covariate) 4.349 1 4.349 407.8 o0.001

Rooting� gmax 0.059 1 0.059 5.546 0.023

Error 0.523 49 0.011


(f) Effect of plant growth form: woody (n ¼ 32) vs. herbaceous (n ¼ 22)

Growth form 0.041 1 0.041 3.736 0.059

gmax (covariate) 2.064 1 2.064 189.5 o0.001

Growth form� gmax 0.034 1 0.034 3.132 0.083

Error 0.544 50 0.011


(g) Effect of plant functional type PFT: cultivated C3 (n ¼ 2) and C4 (n ¼ 6) grasses, broad-leaved crops (n ¼ 14), temperate

deciduous broad-leaved trees (n ¼ 14), warm deciduous broad-leaved trees (n ¼ 4), tropical trees (n ¼ 7), sclerophyllous scrub

(n ¼ 3), evergreen coniferous trees (n ¼ 3)

Plant functional type 0.056 6 0.009 0.922 0.490

gmax (covariate) 0.035 1 0.035 3.467 0.070

PFT� gmax 0.084 7 0.012 1.188 0.333

Error 0.384 38 0.010


H. Heilmeier et al. / Flora 202 (2007) 624–636630

ARTICLE IN PRESS

0

y (

dg d

(logA

BA

)-1)


Third, the driving factor that caused variation in g

and [ABA]xyl was categorised into the six groups soildrying, split-root experiments with soil drought, soilcompaction, Passioura-type pressurized pot, osmoticstress and ABA feeding (Table 1). There was nosignificant effect of the driving factor on stomatalsensitivity nor a significant interaction between drivingfactor and gmax (Table 3c).

Fourth, it was tested whether stomatal sensitivity ofplants grown in the greenhouse differed from thosegrown under field conditions, using maximum leafconductance as a covariate. There was no significantmain effect; however a significant interaction betweengrowth location and gmax (Table 3d). Plants grown inthe field (n ¼ 23) had a higher stomatal sensitivity factor(�0.705, s.e. ¼ 0.047) compared to greenhouse-grownplants (�0.569, s.e. ¼ 0.040; n ¼ 31).

Fifth, when plants grown in pots were compared tothose grown in unrestricted soil at the natural site, therewas no significant main effect (Table 3e). However, againthe interaction between rooting medium and gmax wassignificant, with plants grown in unrestricted soil (n ¼ 16)responding more sensitive (�0.719, s.e. ¼ 0.058) thanplants grown in pots (�0.569, s.e. ¼ 0.036; n ¼ 37).

Finally, the effect of plant growth form and func-tional type (PFT) on stomatal sensitivity was tested.There was no difference in stomatal sensitivity betweenherbaceous and woody plants (Table 3f) nor betweendifferent PFT (Table 3g).

Thus, we could not find a main effect of experimentalprocedure nor plant type on stomatal sensitivity inour data set. Since interaction effects, when present,were of minor significance in most cases (p40.01),we conclude that for the complete data set sensitivityto ABA did not change dramatically with environmentalor experimental conditions nor depend on speciesidentity.

-2

-1

0 1 2 3

Sto

mata

l se

nsitiv

it

Maximum leaf conductance (mol m-2 s-1)

cultivated C3 grasses

warm deciduous

cultivated C4 grasses

broadleaved trees

evergreen coniferous

trees tropical trees

sclerophyllous scrub

broadleaved treestemperate deciduous

broadleaved crops

Fig. 3. Relation between maximum leaf conductance (gmax)

and stomatal sensitivity (dg/d log[ABA]xyl) for different plant

functional types (PFT). The effect of PFT was statistically not

significant (cf. Table 3g).

Responsiveness of stomata to stress in the

rooting zone: stomatal sensitivity

Examples of the relation between g and [ABA]xylshow the similarity between plants (Fig. 1). For bothherbaceous and woody plants, leaf conductance de-creases dramatically at xylem sap ABA concentrationsabove 1mmolm�3. However, herbaceous plants reachhigher maximum leaf conductances, and they respondearlier to an increase in xylem sap ABA as shown by thesteeper decline. Woody species, on the other hand,maintain higher leaf conductance at [ABA]xyl between0.5 and 4mmolm�3.

Linearisation of these curves (cf. Fig. 2 for herbaceousplants grown in the field) reveals a distinct pattern: InH. annuus, the species with the highest maximum leaf

conductance (2.25molm�2 s�1) leaf conductance de-creases much steeper with increasing [ABA]xyl than inother species with lower gmax. The three experimentswith Z. mays yielded similar gmax and slopes for g versuslog[ABA]xyl (Fig. 2b).

As may be inferred from Fig. 1, the relationshipbetween g and log[ABA]xyl showed similar patternsfor all species studied: for species with higher gmax, theslope (dg/d log[ABA]xyl) was steeper and vice versa ascan be concluded from Fig. 2. Plotting dg/d log[ABA]xylas a function of gmax for all data available from theliterature survey resulted in a common linear relation-ship for all plant functional types (Fig. 3). The slopedg/d log[ABA]xyl describes the responsiveness of thestomata to various external stresses that affect the waterrelations of the plant (drought, salt, heat, coldness, etc.).It indicates whether plants would respond with high(more negative slope) or low sensitivity (less negativeslope) to stress. It is called ‘‘sensitivity factor’’.

The significance of stomatal sensitivity to ABA hasalready been discussed by Trejo et al. (1993, 1995)without showing a general relationship. In the presentstudy, the relationship between plant physiologicalperformance and stomatal sensitivity seems to beindependent of genetic or environmental influences(see Table 3). Rather it may be general for a wide rangeof plant and vegetation types.


Ecological relevance of stomatal sensitivity

The general relationship between gmax as an indicatorof plant physiological performance and stomatal sensi-tivity as shown in Fig. 3 evokes a number of ecologicalimplications. Schulze et al. (1994) have presented a closelinear relationship between gmax and leaf nitrogen (N)concentration for a broad range of vegetation types withdifferent leaf longevities. Based on the global distribu-tion of leaf N concentration, they produced a globalmap for gmax. Because of the linear relationship betweengmax and the sensitivity factor the latter can betransferred to the global map of gmax by Schulze et al.(1994) as shown in Fig. 4. Regions with the mostsensitive stomata are those dominated by intensiveagricultural land use in the mid latitudes of NorthAmerica, Europe, Western and Eastern Asia, andsubtropical Southern Asia (India). Furthermore, thetropical deciduous forests in Central and South Americaand Africa show high stomatal sensitivity. Cold-temperate grasslands in Central Asia are major ecosys-tems with medium stomatal sensitivity. For major partsof tropical rainforests, boreal deciduous and evergreenforests, semiarid and arid savannahs and deserts andalpine ecosystems stomatal sensitivity is low. Theseareas are characterized by various stress factors in therooting zone, e.g., low nutrient availability, soil droughtand low temperatures.

In the case of plants growing in dry or extremely dryhabitats, no direct relationships between gmax and[ABA]xyl have been published, mainly because theharvest of xylem sap from these plants is not possibleor extremely difficult. This is (1) because of the anatomyof the plants and (2) because of the extremely low xylemwater potential that makes the harvest of xylem sap bypressurising such plants a serious problem. We areaware of only one experiment in which leaf conductancewas recorded after feeding three different concentrationsof ABA to the xylem sap of a desert plant (Anastatica

hierochuntica, Hartung et al., 1990). However, since thein planta [ABA]xyl is not known in this case, data werenot included in the present study.

It is known that in plants from arid habitatsABA concentrations in the xylem sap often areextremely high with small fluctuations only (ownunpublished data for Hammada scoparia: 670 mmolm�3,Pulicaria crispa: 700 mmolm�3, Reaumuria negevensis:1400 mmolm�3, Zygophyllum dumosum: 1400 mmolm�3,Atriplex halinus: 1000–2000 mmolm�3, Artemisia herba-

alba: 1800–2000 mmolm�3). For these desert plantsgrowing in the Negev (Israel) extremely high leafdiffusion resistances have been measured by Schulzeet al. (1972, 1973). Similar relations also have beendetected with poikilohydric angiosperms from SouthernAfrica and Western Australia (Schiller et al., 1997). Toour surprise, it emerges that the ABA root signal may

not be very effective in desert plants as can be inferredfrom their low sensitivity factor. Under severe stressconditions, as they are typical for deserts, ABA mayplay a more important role for acquiring or maintaininga high desiccation tolerance by formation of dehydrinsor other protective compounds rather than in regulatingleaf conductance (Hartung et al., 1998; Heilmeier andHartung, 2001). A significant part of this ABA may besynthesised in the leaves.

If in agricultural areas gmax of crop plants would bemeasured with a porometer on a sunny day duringthe late morning hours, the linear relation of Fig. 3could be taken as a calibration line to estimate thesensitivity coefficient. In the range of gmax from 0.8 to1.8molm�2 s�1, the sensitivity would be sufficiently highto indicate further stomatal closure. Thus, a moderateirrigation would be sufficient to prevent negativeconsequences for productivity. Consequently, gmax

values below 1molm�2 s�1 could be avoided where thesmall sensitivity of the stomatal system would requiremuch higher irrigation to reverse the response. Thiswould be relatively ineffective. The sunflower plantswithin the gmax range above 1.8molm�2 s�1 originatefrom a greenhouse and a field study on sufficientlyirrigated plots where drought stress does not haveserious negative effects on crop production. Since therelation of Fig. 3 seems to be valid for nearly all climatesand plant functional types, the calibration line could beused for terrestrial plants nearly worldwide and could behelpful for farmers especially in semiarid and aridclimates. Thus besides modern irrigation techniquessuch as partial root zone drying (PRD, Davies et al.,2005) the use of the sensitivity factor could play a partfor performing a sustainable agriculture.

From an ecosystem point of view, it would beinteresting whether a general relationship exists betweensoil water content and stomatal response to xylem sapABA. However, only few data have been publishedshowing the relation between the soil water content (y)and [ABA]xyl. The five data sets evaluated yielded ahyperbolic shape which could be linearised by plottinglog[ABA]xyl against log(y). Although these data trans-formation resulted in straight lines with different slopes,no pattern related to plant life form or experimentalconditions emerged. In greenhouse experiments withplants grown in pots Vigna unguiculata (Duan et al.,1996; Ebel et al., 1997) reacted more sensitively thanHordeum vulgare (Borel et al., 1997) and sycamoreseedlings (Acer pseudoplatanus, Khalil and Grace, 1993).An intermediate response was found for Scots pine(Pinus sylvestris) growing at its natural site (Sturm et al.,1998). Because of the very small number of data, it is notpossible to perform a similar analysis as in the case of g

vs. [ABA]xyl, where a large body of data is available.However, taking in mind that soil water status and g areclosely related (Schulze, 1986) one also may expect

ARTICLE IN PRESS

Fig.4.Theglobaldistributionofthesensitivityfactord

g/d

log[A

BA] xyl.Productionofthemapwasbasedontheglobaldistributionmapfor

gmaxbySchulzeet

al.(1994)and

applyingalinearregressionto

thedata

from

Fig.3yieldingthemodel

dg

/dlog[A

BA] xyl¼

0.000–0.624

gmax(cf.Table

2).



a similarly close relation between y and [ABA]xyl.Consequently, the global distribution of the sensitivity[ABA]xyl (d log[ABA]xyl/d log y) versus log(ymax) shouldresemble that of dg/d log[ABA]xyl vs. gmax as shown inFig. 3.

Following this analysis, it emerges that the ABA rootsignal is mainly important for fast-growing herbaceousspecies from mesic environments with high rates ofwater flow and a fast root-to-shoot communication. Incontrast, if the relationship depicted in Fig. 3 is furthersubstantiated with experimental data and proves to bewidely applicable one may conclude that for plants frommore stressful habitats with low water flow and aconservative water use, just as much as for very tallspecies (e.g., Sequoiadendron) the ABA root signal maynot be very effective. In these cases, other factors, suchas ABA production or release within the leaf, may bemore important.

Acknowledgement

We thank Kerstin Sickel, MPI for Biogeochemistry,for help to prepare the global ABA-sensitivity map.

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General relations of stomatal responses to xylem sap abscisic acid under stress in the rooting zone...

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