Download Effect of soil drying on growth, biomass allocation and leaf gas

,
Plant and Soil 185: 137-149, 1996.
137
@ 1996Kluwer Academic Publishers. Printed in the Netherlands.
Effect of soil drying on growth, biomassallocation and leaf gas exchangeof
two annual grass species
Tibor Kalapos2,Riki van denBoogaard1andHansLambersl
I Department of Plant Ecology and Evolutionary Biology Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht,
The Netherlands. 2Present address and addressfor correspondence: Department of Plant Taxonomy and Ecology,
L. Eötvös University, Ludovika tér 2, H-1083 Budapest, Hungary*
1
I
Received
30November1995.Accepted
in revisedform23April1996
-1
~
Key words: C3, C4, relative growth rate, Tragus racemosus, Triticum aestivum, water stress
,
Abstract
i
-.
~
Influence of short-term water stress on plant growth and leaf gas exchange was studied simultaneously in a growth
chamber experiment using two annual grass species differing in photosynthetic pathway type, plant architecture
and phenology: Triticum aestivum L. cv. Katya-A-I (C3, a drought resistant wheat cultivar of erect growth) and
Tragus racemosus (L.) AlI. (C4, a prostrate weed of warm semiarid areas). At the leaf level, gas exchange rates
declined with decreasing soil water potential for both speciesin such a way that instantaneous photosynthetic water
use efficiency (PWUE, mmol CO2 assimilated per mol H20 transpired) increased. At adequate water supply, the
C4 grass showed much lower stomatal conductance and higher PWUE than the C3 species, but this difference
disappeared at severe water stress when leaf gas exchange rates were similarly reduced for both species. However,
by using soil water more sparingly, the C4 species was able to assimilate under non-stressful conditions for a
longer time than the C3 wheat did. At the whole-plant level( decreasing water availability substantially reduced the
relative growth rate (RGR) of I: aestivum, while biomass partitioning changed in favour of root growth, so that
the plant could exploit the limiting water resource more efficiently. The change in partitioning preceded the overall
reduction of RGR and it was associated with increased biomass allocation to roots and less to leaves, as weIl as with
a decrease in specific leaf area. Water saving by I: racemosus sufficiently postponed water stress effects on plant
growth occurring only as a moderate reduction in leaf area enlargement. For unstressed vegetative plants, relative
growth rate of the C4 I: racemosus was only slightly higher than that of the C3 I: aestivum, though it was achieved
at a much lower water cost. The lack of difference in RGR was probably due to growth conditions being relatively
suboptimal for the C4 plant and also to a relatively large investment in stem tissues by the C4 I: racemosus. Only
10% of the plant biomass was allocated to roots in the C4 species while this was more than 30% for the C3 wheat
cultivar. Theseresultsemphasizethe importanceof watersavingandhigh WUE of C4plantsin maintaininggrowth
undermoderate
waterstressin comparison
with C3species.
Abbreviations: A-photosynt!teticrate,Ela-waterlasson leaf areabasis,gs-stomatalconductancefor watervapour,
IWR-inflorescence weight ratio, LA-total leaf area, LAR-Ieaf area ratio, LWR-Ieaf weight ratio, NAR-net
assimilationrate, Pi/Pa:'-ratio
of intercellular and atmosphericCO2partial pressure,PPFD-photosyntheticphoton
flux density, PWUE-photosyntheticwater use efficiency (A/gs), RGR-relative growth rate, RW-total root dry
weight, RWR-root weight ratio, SLA-specific leaf area,SWR-stemweight ratio, WUEB-water useefficiency of
biomassproduction,~ leaf-Ieafwaterpotential,~ soil-soilwaterpotential.
.
FAX No: +3613338764
138
Introduction
pathwaytype (C3 vs. C4), plant architecture(erectvs.
prostrate)andphenology(spring vs. summerannual).
A short-termsoil-drying treatrnentwas applied to the
two annualgrassspeciesin a growth chamberexperiment,andchangesin leaf gasexchangeratesandplant
growth parameterswerefollowed simultaneously.
Plant growth is limited by water shortageover large
areasof the world, both in naturalcommunitiesandin
agriculturalsystems.To copewith this limitation variousplantadaptationshaveevolvedatdifferentlevelsof
organizationfrom moleculesto the wholeplant (Smith
andGriffiths, 1993;TurnerandKramer,1980).In addition to these, various acclimation mechanismsmay
be activatedin plants in responseto moderatewater
stressto compensatefor the effects of reducedwater
availability (Bradford and Hsiao, 1982; Pereira and
Chaves,1993;Taiz andZeiger, 1991).Stressresponse
or any other plant function operatingat a certainlevel of biological organizationcan be greatlyinfiuenced
by changesat other levels as weIl. For example,the
leaf photosyntheticrate is usually higher in C4 than
in C3 plants, yet the plant or crop growth ratesmight
be similar for these,if differencesin totalleaf areaor
reproductiveallocationcancelout the leaf level advantage(Bazzazet al., 1989; Gifford, 197'4;Hofstra and
Stiénstra, 1977; Slatyer, 1971). Plants utilizing the
C4 pathway of photosynthesisusually occur in open
habitatsof high temperatureand irradiance.In many
of these biotopes, water shortageis responsiblefor
the incompleteplant cover. Despitethis habitat preférenceby C4 plants, the C4 pathwayis not known to
confergre!ltertoleranceof water stressin itself if compared with the C3 metabolism(Osmondet al., 1982;
pearcyandEhleringer,1984).Underappropriateenvironmentalconditions, however,the higher photosynthetic capacityand higher water- and nitrogen- use
efficienciesof photosynthesisof C4leavesmay leadto
a higherplant growth rate andproductivity thanthat of
C3 plants, althoughthis is not invariably the case(see
Poorter, 1989a;and Snaydon,1991for literature surveys).Under waterstress,the net assimilationrateand
relative g'rowthrate may be equally low in C3 and C4
Growthof plants
.
Two annual grassspecieswere used for this study:
Triticum aestivumL. CV.Katya-A-1 (C3), a relatively drought-resistantwinter wheat variety (Van den
Bogaard,1995)cultivated in South East Europe,and
Tragusracemosus(L.) AlI. (C4). The latter speciesis
a cosmopolitanweedwith warm African origin which
regularly occurson wasteground or in early successional communitieswith coarsetextured soil (Hitchcock, 1950; Soó, 1973). 7: racemosusreachesthe
Northern limit of its distribution under the semiarid
continentalclimateof East-CentralEurope(Meuseiet
al., 1965),whereit growsduring the hot anddry summ6r months.
.
Seedsof 7: racemosuswerecollectedin a disturbed
sandgrasslandstandin Hungary,while thoseof 7: aestivum were obtainedfrom the InternationalCenterfor
Agricultural Researchin Dry Areas(ICARDA, Aleppo, Syria). After a few daysof dry cool storage(at 5
OC),seedsweregerminatedon wet filter paperin Petri
dishes.Whentheyreachedan appropriatesize(after 23 days)seedlingswereplantedinto 2.4 dm3pots filled
with loamy sandysoil (this day was the first day of
the experiment).Plantsweregrown in a growth chamber underthe following conditions:20 oC air temperature,70%relativehumidity,550ILmolm-2 s-1 photon
fiux density(PPFD)at pot height provided by Philips
.
species(Hofstra and Stienstra,1977; Ludlow, 1976).
Infiuence of water shortageon leaf gas exchangeis
reasonablywell-understoodby now for both C3 and
C4 plants (Bradford and Hsiao, 1982;Osmondet al.,
1982;PearcyandEhleringer 1984),but muchremains
to be explored about simultaneouschangesin plant
growth rate and biomassallocation, and the variation
of thesetraits amongplants.
To graspasmuchof this variationaspossiblewithin a small experiment, we comparedtwo markedly
different species.Theseweretwo annualgrassspecies
fromtemporallywaterstressedseasonalenvironments
in South East Europe, which differ in photosynthetic
HPIff-400Wlamps, 40PaCO2partialpressureand 14
h light 110 h dark period. Potswere rotatedregularly
on the benchto minimize effectsof possibleheterogeneouslight distribution within the growth room. The
soil surfacein the pots wascoveredwith plastic granules to minimize evaporation,and two pots per treatment without plantswere usedto measurethis. Plants
were wateredevery 2-3days to bring the pots to the
samesoil watercontent.Beforethe startof the experiment, dissolvednutrientswere given to the soil in the
following quantities:6 mmol Ca(NO3)2.4H20,8 mmol
KNO3, 2 mmol KH2PO4,2.75 mmol MgSO4.7H20,
4 ILmol MnSO4'H20, 1.7 ILmol ZnSO4'7H20, 0.3
Materials and methods
139
,umol CuSO4.5H20, 40 ,umol H3BO3, 0.5 ,umol
Na2MnO4.H20,81 ,umol FeSO4.7H20and 80 ,umol
NaEDTA. Additional nutrients were supplied three
daysprior to and at the start of the droughttreatment,
containing 1/3 of the abovequantitiesof the first four
compoundsin thelist before.Atday 19(1: aestivum)or
20 (1: racemosus),waterwaswithheld from half of the
plants (drought treatrnent),while the other half was
watered regularly (control). With 2-5 day intervals,
gas exchangeand leaf water potential measurements
weremadeon 3 plantsper speciesand treatrnent,then
plants were harvestedand measurementswere made
for a limited growth analysis.The experimentlasted
36daysfor 1:aestivumand44 daysfor 1: racemosus.
Six harvestswere madefor both species.
Measurements
,
Leaf gas exchangeparameterswere measuredwithin the growth room betweenthree and six hours after
the beginning of the light period on the'5th leaf for
1: aestivum, and on the 3rd leaf for 1: racemosus,
using an ADC LCA-2 Portable Infrared Gas Analyzer with a PLC-2N grassleaf chamber(ADC Ltd.,
Hoddesdon,UK). The PPFD on the cuvettewas 550
,umolm-2 S-l on average.Leafwater potential('I11eaf)
was determinedon the sameleaf, right after the gas
exchangemeasurement,
by apressurechamber(TFDL,
Wageningen,The Netherlands)using compressedair
aspressurizinggas.Theleaf waswrappedin plasticfoil
prior to excision and during the measurementwithin
the pressurechamberto prevent water loss from it.
Plantswere then harvested,separatedinto leaves(leaf
blades),stems(culms andleaf sheaths),inflorescences
(only for 1: racemosus)androots. Leaf areaand fresh
and dry weights of leaves,stems,inflorescencesand
roots were determined.Leaf areawas measuredusing
anLI-31 00 areameter(LI-COR Inc., Lincoln, Nebraska, USA). Plant material was dried at 70 oC for 1-2
days. Whole plant water loss was also measuredby
the weight loss of pots. A correctionwasmadefor the
evaporationfrom the soil surfaceby using pots without plantsmaintainedat the samewatercontentasthat
of treatmentand control pots, respectively.Soil water
potential('ll soiUwascalculatedfrom soil watercontent
data measuredfor eachpot, using an experimentally
determinedrelationshipbetweenthesetwo soil properties.
Data analysis
Leaf gasexchangeparameterswerecalculatedaccording to von CaemmererandFarquhar(1981).The ratio
of photosynthesis(A) and stomatalconductancefor
water vapour(gs)wasusedto measurephotosynthetic
wateruseefficiency(PWUE).The relativegrowth rate
(RGR) of plantswas determinedfollowing the procedure of Poorter (1989b). In this method, the RGR is
first calculatedaccordingto the classicalapproach,by
skipping one harvesteachtime, ratherthan using valuesfrom successiveharvests.Then,the RGR on every
harvesttime can be calculatedas the averageof two
or threevaluesobtainedin this way. Net assimilation
rate (NAR, net dry weight gain per unit leaf area)was
determinedin a similar manner.Leaf arearatio (LAR)
was calculatedas the ratio of leaf areaand plant dry
weight. Specificleaf area(SLA) was obtainedas the
ratio of leaf areato leaf dry weight. Leaf weight ratio
(LWR), stemweightratio (SWR),inflorescenceweight
ratio (IWR) and root weight ratio (RWR) was calculated as the ratio of leaf, stem,inflorescenceand root
dry w~ght to total plant dry weight,respectively.Leaf
areaper unit root weight (LA/RW),was calculatedas
the ratio of totalleaf areaandroot dry weight.
Whole plant water loss data were obtainedafter a
correctionfor evaporationfrom the soil surface.Transpirationper unit leaf area(Ela)was calculatedas the
ratio of mean daily plant water use betweencurrent
and previous harvestsand total leaf area at the day
of harvest.Wateruseefficiencyof biomassproduction
(WUEB)wascomputedastheratioofdryweightincrementandwaterconsumptionby the plant betweentwo
successiveharvests.
For eachparameter,two-way analysisof variance
with least significant difference (LSD) test for comparisonof means(SokalandRohlf, 1981)was usedto
analyzespeciesandtreatrnenteffectsat referencedays
(day 33 for 1: aestivumand day 41 for 1: racemosus).
For the full length of the experiment,differencesin
RGR betweenspeciesand treatrnentswere testedby
three-wayanalysisof varianceof the ln-transformed
plantdry weightdata(PoorterandLewis, 1986).A significant interactionbetweenspeciesor treatrnentand
time indicatesa differencein RGR. (In this analysis,
time wasmeasuredinthe numberofharvestsinsteadof
days,becausetime coursesdifferedfor thetwospecies,
but equal number of harvestswere performed.) AlI
statistical comparisonswere consideredsignificantly
different at p<0.05.
1.40
Results
After withholding water from the plants, soil water
content declined from 20 to 4% (data not shown) and
'lIsoil dropped from -0.06 to -0.4 MPa (Figures lAB). The time course of the drought treatment experiment was different for the two species, because J:
racemosus depleted soil water content of pots much
more slowly than J: aestivum did (Figures lA-B). For
this reason, not only the time courses (Figures 1 and
2) were analyzed, but instantaneous species performances were also compared by using data collected on
days with similarly low (-0.27 MPa, drought treatment) 'lIsoil values (that occured on day 33 for J: aestivum, and on day 41 for J: racemosus, Table 1 and 2).
Because of the different time courses, our experimental design was appropriate to study drought effects on
leaf gas exchange and plant growth simultaneously for
J: aestivum, but not for J: racemosus. In this rapidly
developing species water stress did not occur until the
plants were no longer producing new 1eaves,as by that
time they had already reached the reproductive phase.
Consequently, water shortage had a pronounced effect
on leaf gas exchange, but not on growth parameters of
J: racemosus, except for a moderate reduction in leaf
area enlargement. J: aestivum remained in the vegetative growth phase throughout the experiment.
In the case of J: aestivum, control plants also experienced a slight water stress towards the end of experiment, as it is shown by 'll soil and gas exchange rate
values (Figures lA, E, G). This was because the older and larger plants exploited soil water inpots more
rapidly than the smaller and younger ones at the same
watering frequency. However, this minor deviation did
not alter the overall outcome of the experiment.
Lea! gas exchange
When grown at adequate water supply, most of the
leaf gas exchange parameters were significantly different for the two species (Figs. lE-N, Table 1, controls).
Stomatal conductance (gs) and intercellular C02 partial pressure (Pi/Pa) were lower, instantaneous photosynthetic water use efficiency (PWUE) was higher for
the C4 J: racemosus than for the C3 J: aestivum. Considering the full length of the experiment, there was no
consistent difference in the photosynthetic rate (A) of
the two species, although it tended to be higher for J:
racemosus at the first two samplings (Figures lE-F).
After water was withheld from plants, J: racemosus showed a much slower rate of water stressdevelop-
ment than J: aestivum (Figures lA-D); thus the farmer
was able to maintain a relatively unlimited assimilation
rate much longer (Figures lE-F). However, at similarly severe water stress ('lIsoil ~ -0.27 MPa), leaf
water potential ('lIleaf), instantaneous assimilation rate
(A) and stomatal conductance (gs) values were equally reduced in both species (Table 1, treatment). In J:
aestivum Pi/Pa decreased, PWUE increased with soil
drying, while in J: racemosus the change was less clear
(Figures ll-N). In J: aestivum a decrease in 'lIsoil led
to a more rapid decline of leaf gas exchange rates than
.
that of 'lIleaf; A, gs and Pi/Pa in water-stressed plants
were significantly below those of controls by day 31
(Figures lA, E, G, K), while the difference in 'lIleaf
between treatment and control occurred at day 33 at
the earliest (Figure IC). Similarly, in control plants
a moderate decline of 'lIsoil at the end of the experiment caused no change in 'lIleaf (Figures lA, C), but
decreased leaf gas exchange parameters appreciably
(Figures IE, G, K). In drought-affected plants, gs was
highly correlated with 'll soil(r2=0.66, p<0.001), but less
so with 'lIleaf (r2=0.34, p<0.01): Stomatal conductance
~creased more rapidly with soil drying than did A,
and variation in Aduring treatment was explained by
that of gs (r2=0.87, p<O.OO1). PWUE steadily increased
with decreasing 'll soil,but suddenly dropped at day 36,
when 'lIleaf reached -3.0 MPa (Figure 11). Similarly, after a steady decline, Pi/Paapproximately doubled
by the same day (Figure 1K). Though these abrupt
changesmay suggest non-stomatallimitation of A, we
will notdiscuss it any further, becausemeasured values
of gas exchange were rather small at that time.
Plant water lass
Gravimetric water lass of well-watered J: racemosus
plants was about half of that of J: aestivum controls,
when expressedon a leaf area basis Ela (Figures lM-N,
Table 1). Droughtreduced Ela markedly in J: aestivum,
while in J: racemosus the change occured at the last
harvest only (Figures lM-N). Water use efficiency of
biomass production (WUEB) was higher in the C4 J:
racemosus than in the C3 J: aestivum (Figures 10-P,
Table 1). Both species showed increasing WUEB with
the drought treatment, except for a sharp decline at
the last harvest (Figure 20) paralleling simultaneous
changes in PWUE and Pi/Pa.
.
141
Triticum aestivum
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Tragus racemosus
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Figure
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On
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25 27 29 31 33 35 37 39 41 43 45
Day of experiment
on Triticum
axis,
time
aestivum
is
plotted
cv. Katya-A-l
in
days
elapsed
(C3)
after
the
and
start
Tragus
of
racemosus
the
withheld from the "drought" seriesplantsat day 19for 7: aestivumandat day 20 for Tracemosus.Averagevalues:i:SE
experiment.
(n=3).
(C4). J. Leaf
Water
was
142
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Triticum aestivum
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Figure 1. Cont.
Table 1. Influence of short-tenn drought treatrnent on leaf gas exchange and plant water use
parameters of one C3 and one C4 annual gr:assspecies. Values measured on days with similar soil
water potentia! for the two species are compared (mean values:i:SE, n=3), days after the start
of the experiment are shown in brackets. For each parameter, means with the game superscript
are not significantly different (p<O.O5). Abbreviations and units: A-photosynthetic rate (p,mol
CO2 m-2 s-I), Ela-water lass on leaf area basis (kg H20 m-2 leaf day-l), gs-stornatal
conductance (mmol H20 m-2 s-I), PWUE-photosynthetic water use efficiency (Ngs, mmol
CO2 mol-:1 H20), Pi/Pa-ratio ofintercellular.md atrnospheric CO2 partial pressure (Pa Pa-I),
WUEB-water use effciency of biomass production (mgbiomass g-1 H20), IlIleaf-Ieaf water
potential (MPa), IIIsoil-soilwater potetitial (MPa)
Parameter
7: aestivum(C3)
Control (33)
Treatrnent(33)
,-
7: racemosus(C4)
- --Control (41)
Treatrnent(41)
IlIsoil
-O.09:i:O.O1B
-0.27:i:O.04b
~Ieaf
-:-1.24:i:O.02B
-1."~~:i:O.21b
20.2:i:1.21B
10.6:i:2.2b
28.4:i:3.77B
387:i:28B
56:i:11b
212:i:47c
98:i:25b
O.14:i:O.O1c
. O.45:i:O.O3c
O.16:i:O.02bc
O.39:i:O.O7c
A
,
gs
PWUE
Pi/p~
Ela
WUEB
-O.09:i:
O.OOO3B
-1.20:i:O.04B
-"O.26:i:O.07b
-1.94:i:O.37b
15.5:i:4.11b
O.O5:i:O.OO2B
O.70:i:O.O3B
O.19:i:O.OO4b
O.24:i:O.O1b
1.10:i:O.O3B
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O.58:i:O.O3b
O.55:i:O.04b
18.7:i:3.ib'
18.4:i:1.3b
254:i:4.1b
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.
143
§
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Triticum aestivum
10
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. . o- . .Control
--- Drought
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Day of experiment
Figure 2. Time coursesof a short-termdroughttreatmenteffectson Triticum aestivum cv. Katya-A-1 (C3) and Tragus racemosus (C4). II. P1ant
growth response. On the horizontal axis, time is p1otted in days e1apsedafter the start of the experiment. Water was withhe1d from the "drought"
seriesp1antsat day 19 for 7: aestivumandat day 20 for 7: racemosus.Averagevalues:l:SE(n=3).
144
Triticum aestivum
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.:-- 40
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22 24 26 28 30 32 34 36
Day of experiment
"E.
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0.3
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Day of experiment
Figure 2. Cont.
O
145
Growthparameters
.
.
,
At favourable water supply the relative growth rate
(RGR) of plants was about 100-200mg g-l day-l,
andtherewaslittie differencebetweenthe two species
(Figures 2E-F and Table 2, control). During the early days of experiment, RGR was slightly higher for
the C4 7: racemosus,but steadily declined as plants
enteredthe reproductivephaseand allocatedprogres-
RWR) <;:hanged
5 daysearlier(Figures2A, C, 1,M, Q).
The three-wayanalysisof varianceof ln-transformed
plant weight yielded a significantspeciesx time interaction, while the treatrnentxtimeinteraction was not
significant. Total leaf area of droughtedplants was
abouthalf of that of controlsby the end of the experiment (Figure2C).
sively more biomass into inflorescence (Figures 2E-F,
Discussion
S). Comparing the C3 and C4 species,there was no
differencein the Detassimilationrate (NAR) of wellwateredplants(Figures2G-H, Table2, control). HoweveT,there were conspicuousinterspecificdifferences
in biomasspartitioning. Only 10% of plant biomass
was allocatedto roots in 7: racemosus,while it was
about30%in 7: aestivum,asshownby their root weight
ratios (RWR, Figures 2Q-R, Table 2). Stem weight
ratio (SWR) was almost 0.5 in 7: racemosuswhile it
wasonly 0.25 for 7: aestivum(Figures20-P, Table2).
In control plants, both RWR and SWR remainedfairly constantduring the courseof the experiment.Leaf
weight ratio (LWR), specificl~af area(SLA) and leaf
arearatio (LAR) declinedmarkedly with ontogenetic
plant developmentin 7: racemosus,while showedno
particular changein 7: aestivum(Figures21-N).In its
vegetativephase, 7: racemosushad higher SLA and
LAR than 7: aestivumdid, while LWR values were
similar (Figures21-N,days23-27).
Soil drying wasmuch slowerfor 7: racemosusthan
for 7: aestivum(Figures lA-B), so this speciescould
maintain a relatively high RGR during most part of
the treatment (Figure 2F, drought treatment). Water
stress- developingonly towardsthe end of the experi-
Short-term soil drying influenced pl ant functioning
at both leaf and whole-plantlevels in the two annual speciesstudied. Soil water stressdevelopedmuch
more slowly for the C4 Tragusracemosusthan for the
C3 Triticum aestivum.This differenéewas primarily
due to the substantiallylower rate of water consumption by 7: racemosus(measuredejtheTby leaf stomatal
conductance/gs/ or by gravimetric plant water loss
expressedon a leaf areabasis /Ela/, Table 1, Figure
1). A somewhatsmallersize of 7: racemosusindividuals at the beginning of the drought treatrnentprobably also contributedto this difference. As a consequence,the C4 specieswas ableto maintainrelatively
high leaf assimilation (A) and plant growth (RGR)
rates during most part of the treatmentcomparedto
the markedly reduced values of the water stressed
wheat.(The gradualdeclineof RGR for 7: racemosus
that occuredthroughoutthe experimentwas because
the rapidly developingplantsenteredthe reproductive
phasesoon). Comparing non-stressedcontrol plants
(in the vegetativegrowth phasefor 7: racemosus),the
A did not differ considerably,while RGR was only
slightly higher for the C4 7: racemosusthan that for
ment - caused no perceivable change in the growth of
the C3 wheat (Figure 2, days 23-27). This was most
reproducing7: racemosusplants, except for a slight
decreasein leaf areaenlargement(Figures2D, J). In
contrast, soil drying started much earlier in 7: aestivum (Figure lA), and reducedboth RGR and NAR
of plants substantially(Figures2E, G). Biomasspartitioning also changedmarkedly.With declining 'I!soil
theLAR decreased,
dueto areductionin bothLWR and
SLA (Figures 21, K, M). Root weight ratio increased
with droughttreatrnent(Figure2Q). As a consequence
of a reducedLAR and an increasedRWR, a unit of
root dry weight supplieda smallerleaf areawith water
in droughtedplants than in control plants (Table 2,
LA/RW). Concerningthetreatrnenttime course,a considerablereductionin total plant weight in stressed7:
aestivumplants occurredonly by day 36, while total
leaf area and allocation parameters(LAR, LWR and
probablybecausegrowthconditions(PPFD<600Jl,mol
m-2 s-l, air T=20 OC)wererelatively suboptimalfor
the C4 pathwayof carbonfixation, but less so for the
C3metabolism,consideringthe generallight- andtemperatureresponsecurvesof photosynthesis(Pearcyand
Ehleringer,1984).Thus,the higher wateruseefficiency of leaf photosynthesis(PWUE) and plant biomass
production (WUEB) observedin 7: racemosuswas
mainly due to its lower rate of water consumption,as
theA andRGRvaluesdid not differ markedlybetween
the two species.
At the leaf level, instantaneousrate of leaf gas
exchangedeclinedwith decreasingsoil wateravailability (Figure 1, Table 1), due to a reductionin stomatal
conductance.Stomatareactedto waterstressin sucha
way that photosyntheticwateruseefficiencyincreased
146
Table 2. Inftuence of short-term drought treatment on plant growth parameters of one C3 and
one C4 annual grass species. Values measured on days with similar soil water potential for
the two species are compared (mean values:i:SE, n=3), days after the start of the experiment
are shown in brackets. For RGR and NAR, treatrnent averages are also given in parenthesis.
For each parameter, means with the same superscript are not significantly different (p<0.05).
Abbreviations and units: IWR-inftorescence weight ratio (g inft. g-l plant), LAR-leaf area
ratio (m2 leaf kg-l plant, LA/RW-leaf area/root weight (m2 leaf kg-l), LWR-leaf weight
ratio (g leaf g-l plant), NAR-net assimilation rate (mg biomass m-2 day-l), RGR-relative
growth rate (mg g-l day-l), RWR-root weight ratio (g root g-l plant), SLA-specific leaf
area (m2 leaf kg-l leaf), SWR-stem weight ratio (g stem g-l plant), NA-not applicable
7: aestivum (C3)
Parameter
Control (33)
Treatrnent (33)
T racemosus (C4)
Control (41)
Treatment (411)
RGR
171 (149a)
89 (l06b)
112 (148a)
107 (143a)
NAR
12.0 (10.7a)
9.9 (8.5b)
10.5 (ll.oa)
14.0 (10.9a)
:,.
LAR
'j(
LWR
14.3:i:0.8a
0.43:i:0.02a
9.0:i:l.28bc
0.34:i:0.OO7b
10.6:i:0.15b
0.30:i:0.OO4c
:-
7.6:i:0.92c
;
0.24:i:0..013d
SLA
33.5:i:0.4a
26.2:i:3.3b
35.8:i:0.66a
31.7:i:3.1ab
RWR
0.34:i:0.02a
O.44:i:O.Olb
0.10:i:0.OO5c
0.095:i:0.Olc
LA/RW
/
42.7:i:4.5a
20.4:1::2.9b
104.8:i:6.12c
83.4:i:16.6c
SWR
0.23:i:0.OO4a
0.22:1::0.01a
O.46:i:O.Olb
0.45:1::0.01b
IWR
NA
NA
0.14:i:0.Qla
O.21:i:0.03b
at the leaf level. In 7::aestivum,changesin leaf gas
exchangeparameterswere much more closely related
However, theseefficiency parameterscan be greatly
modified under natural conditions, as the phenology
to those in IlIsoil than in bulk leaf water status (llIleaf,
of C3 and C4 species is usually
Figures lA-D). This phenomenon- also encountered
in water stressedZea mays(Zhangand Davies, 1990)
and in Lupinus albus (Quick et al., 1992) - must be
the result of the root-to-shootchemicalsignalling,that.
occursduring soil drying (BlackmanandDavies,1985;
Gollanetal., 1986;Schulze,1986;TardieuandDavies,
1993; Zhang and Davies, 1990).When wateredadequately, the C4 7::racemosusshowedslightly higher
instantaneousrate of photosynthesisand twice higher
PWUE than the C3 grass(Figures IE-F, I-J, days2327). However,at severewater stressby the end of the
droughttreatment,interspecificdifferencesin leaf gas
exchangeparametershad disappeared(Figures lE-J,
Table 1). This confirms that the higher WUE of the
C4 photosyntheticpathway is not invariably associated with a greater water loss toleranceof the leaf
(Osmondet al., 1982;PearcyandEhleringer,1984).In
7::racemosus,the higher PWUE of the C4pathway led
to higher WUE for biomassproductionat the wholeplant level asweIl, comparedto that of the C3 species.
Under the growth conditionsusedin this experiment,
this differencewasmostly dueto differencesin aplant
water use. Although it should be kept in mind, that
thesedifferencesin PWUE and WUEB were obtained
under identical aerial conditions (resemblingspring
weather when 7:: aestivum grows) for both species.
- displacedunder seasonaltemperateclimate (Boutton et al., 1980; Kalapos, 1991;Kemp and Williams,
1980; Monson and Williams, 1982). Thus, most of
the growth of the C3 7::aestivumoccursduring spring,
when the vapour pressuredeficit of the air is much
lower thanit is in summer,when the C4 7::racemosus
grows. Differencesbetweenthesetwo photosynthetic pathwaysin stomatalefficiency to conservewater
underboth steadystateand nonsteadystatelight conditions werefound to play a major füle in the observed
phenologicalgrowth patterns(Knapp, 1993).
In this experiment, neither RGR nOTNAR was
markedly different betweenthe C3 and C4 species.
When interpreting this, it should be consideredthat
growthconditionswererelatively unfavourablefor the
C4plant,but not really for the C3.In comparisonsof C3
andC4species,growthtemperaturewasfound to greatly influencethe RGR of plants (Kemp and Williams,
1980;Pearcyet al., 1981). Although there is increasing evidencethat the high photosyntheticcapacityof
C4 leavesdoes not invariably translateiota a higher
RGR or crop growthrate(Bazzazet al., 1989;Gifford,
1974;Hofstra andStienstra,1977;Slatyer,1971).In a
critical review of the literature Snaydon(1991) found
no consistentdifferencein productivity of C3 and C4
plants that could be attributedparticularly to the dif-
- partIyor
completely
"
147
lessrootsthanC3plantsdo.Plantspecies
witha higher
0.6
- 0.5
i
"g:0.4
i
03
O~.
_!.-~
r-=~;:':::==':
:.:--
.
;-_!
~.
-~ 02
NAR tendto havegreaterallocationto root biomass
(Konings,1989),buttherelationshipmightnotbeuni-
~~~I
c._SWR plants,
C4plants
were
found
to have1980;
a lower
(Gebauer
et al., 1987;
Kemp
and
Williams,
Saxena
and
..
g 0.1
.
Ramakrishnan,1983; Wong and Osmond, 1991), a
higher(Caldwellet al., 1977;HofstraandStienstra,
0.0
o
1977;Roushand Radosevich,1985;Sageand Pearcy,
-0.1
-0.2
-0.3
1987a)or a similar(Bazzazet al., 1989;Forsethet al.,
-0.4
'!'.,,(MPa)
.
.
form acrossphotosyntheticpathways,becauseof differential resourceuseefficiencies.Comparedwith C3
1984)proportionof their biomassinvestedin roots.In
Fig-
the C4Echinochloapolystachiagrowing on the Ama-
ure3. Changes
of biomasspartitioningwith decliningsoil water
potentia!
in droughtaffectedr aestivum
plants.Abbreviations
asin
Table2
zon ftoodplains, root system accounted for less than
5% of total pl ant biomass, while monotypic stands
f h. 1
. d th h. h
.
ferentpathwayof CO2fixation,but muchmore to various environmentalconditions(e.g. the usuallylonger
growth seasonin the habitatsofC4 species).
WaterstresssubstantiaIlydecreasedthe RGR of 1:
aestivum,while NAR alsotendedto decrease.
Biomass
partitioning also changed with decreasing'Il soil in
such a way that the proportion of water-absorbing
biomass increased, while the proportion of waterloosing biomassdecreased(Table 2, Figure 2). This
was achievedby greaterallocationto roots andlessto
leaves(Figure 3), with a simultaneousdeclineof specific leaf area.By thesechangesthe plant can exploit
the limiting waterresourcein a moreeffectiveway, In
1: aestivum,biomasspartitioning changedmorerapidly than the overall decreaseof growth rate. Increased
biomasspartitioning to roots and less to leavesis a
frequentlyobservedresponseto moderatewaterstress
in most plants (Bradford and Hsiao, 1982; Konings,
1989;Mooney and Winner, 1991; Sharpand Davies,
1979;Simaneet al., 1993;Van den Boogard,1995).
Whenunstressedvegetativeplantsacecompared,1:
racemosusshowsa patternofbiomasspartitioningdistinctly different from 1: aestivum(Figures21-R,days
23-27,control). Only 10% of its total dry weight is in
roots, while for 1: aestivumthis figure is around30%.
We have two possible explanationsfor that: 1) We
observedroots of 1: racemosusto be much finer than
thoseof 1: aestivum(althoughno quantitativemeasurementswere made);bence,a unit root weight might be
more efficient in capturingwaterandnutrientsby having a larger surface-to-volumeratio. 2) Due to their
higher water- and nitrogen use efficiencies(Osmond
et al., 1982;Sageand Pearcy,1987b),C4plantsmight
be able to producethe gameamountof biomasswith
o t ISP ant attaIne e 19 est Detpnmary production evecrecordedfor terrestrial vegetation(Piedade
et al., 1991).To draw any firm conclusions,whether
C4 plantscan potentiaIlyfunction with relatively less
root biomassthan C3 plants do, a wider comparison
of closely related C3 and C4 speciesunder identical
environmentalconditionsis needed.
Assimilatessavedon roots can be spent on other plant structures/processes
in C4 species, which
increaseplant fitnessin their naturalhabitat.In 1: racemosusthis was investedinto stemsleading to nearly
half of the plant dry weight allocatedto them,while in
1: aestivumit was around20%. Saxenaand Ramakrishnan(1983)found two perennialC4 weedspeciesto
partition a large proportionof their biomassto undergrouridrhizomes,while their RGR wassimilar to sympatricC3species.Thehighstemweightratioin 1: racemosusis explainedby its particular modular growth
form. Youngplantsmakea smallrosette,but soonproduceseveralprostratestemsgrowing aut radially with
long internodes.Newramets(withleavesandroots)are
formed at the new nodes,which in tum produceadditional modules.After a seriesof two or three ramets
on one stem,inftorescencesaceformed at stemapices
and plant growth comesto an end. This growth form
is likely to confer severaladvantagesfor the plant in
its naturalenvironmentusuallycharacterizedby sparse
plant cover due to water limitation. The most important of thesemay be that the plant can exploit a larger
volume of soil for water and nutrients by additional
roots formedat the new nodes.
In conclusion,althoughgrowth conditions in this
experimentprobably did not allow to fully utilize the
greaterphotosyntheticand growth capacityof the C4
speciescomparedto the C3 one,its sparingwater consumptionandgreaterwateruseefficiencyconsiderably
148
postponed the development of plant water stress.If this
is coupled with arapid plant ontogenesis, the C4 annu.
al will be able to produce seeds at lower water supply
than a C:1 one. At severe water stress, however, leaf
gas exchange rates were similarly reduced in our C:1
an
dC
.
4 grass speCIes.
Acknowledgements
..
ThIJs
We thank
Pons
and
Hendnk
.
Poorter
for
. .
cntt-
cai comments on an earlier version of this manuscript,
and Rob
.
Welschen
expenment.
for technical
Th
supported
Hungarian
Research
bank
Rt
by the Utrecht
Fund
Tudomanyért
(Hungary).
Boogaard
during
the
.b .
f T .b K 1
e contrI utton O 1 or a ap.os was
financially
the Magyar
assistance
The
(OTKA
Alapitvány
researc?
was part of a collaborattve
UniversIty,
2049,
F6434)
the
and water supply. Acta Bot. Neerl. 26, 63-72.
Kalapos T 1991 C3 and C4 grasses of Hungary: their environmental
requirements, phenology and role in the vegetation. Abstr. Bot.
15, 83-88.
Kemp P R 1983 Phenological patterns of Chihuahuan Desert plants
in relations to the timing of water availability. J. Ecol. 71, 427-
cilis (C4).Ecology61,846-858.
Knapp AK
74,113-123...
..
Konings H 1989 Physlologlcal and morphologlcal dlfferences
between plants with a high NAR and a high LAR as related
project
between
of Development
Coopera-
-
.
1993 Gas exchange dynamics in C3 and C4 grasses:
/ Magyar
Hitel. .
~kI
van den
of
:-
436.
Kemp P R and Williams G J 1111980 Physiological basis for niche
separation between Agropyron smithii (C3) and Bouteloua gra-
consequences of differences in stomatal conductance. Ecology
to environmental conditions. In Causes and Consequences of
Variation in Growth Rate and Productivity. Eds. H Lambers,
M L C~bridg~, ~ Konings and T L Pansopp 101-123. SPB
Academlc Publlshing, The Hague, the Netherlands.
Ludlow M M 1976 Ecophysiology of C4 grasses. In Water and Plant
Life. Problems and Modern Approaches. Ecological Studies 19.
Eds, O L Lange, L Kappen and E-D Schulze. pp 364-386.
Springer-Verlag,
Meusei
H, Jtiger E andBerlin,
WeinertGermany.
E 1965 Vergleichende Chorologie der
Re f,erences
Bazzaz F A, Garbutt
Hofstra J J and Stienstra A W 1977 Growth and photosynthesis of
closely related C3 and C4 grasses, as m
. fl uencedb y 1.Ig ht mtenslty
.
.
and
the Utrecht University and the ICARDA, financed by
the Netherlands'
Ministry
.
.
tton, project SY /90/950.
GollanT, Passioura
J B andMunnsR 1986Soilwaterstatusaffects
stomatal
conductan~e
offully turgidwheatandsunflower
leaves.
Aust.J. PlantPhystol.13,459-464.
HitchcockAS 1950Manualof thegrasses
of theUnitedStates.
2nd
ed.U.S.Department
of AgricultureMiscellaneous
Publication
No.200.USDA,Washington,
USA.1051p.
K, Reekie E G and Williams
WE
1989 Using
Zentraleuroptiischen
Flom. Band 1. VEB Gustav Fischer
Jena, Germany. 583 p.
Verlag,
growth analysis to interpret competition between a C3 and C4
annual under ambient and elevated COl. Oecologia (Beri.) 79,
223-235.
. .
Blackrnan P G and Davies W J 1985 Ro?t to ~hoot communication
in maize plants of the effects of soll drymg. J. Exp. Bot. 36,
39-48.
..
. .
Boutton T W, Harrison A T and Srmth B N 1?80 Distribution of
biomass of species differing in photosynthetlc pathway along an
aridity gradient in. Southeastern Wyoming grassland. Oecologla
45, 287-298.
Bradford K J and Hsiao TC 1982 Physiological responses to mode:ate water stress. In Physiological Plant Ecology.lI. Encyclopedia
of Plant Physiology, New Series,. Vol 12B. Eds. O L L~ge, P
S Nobel, CB Osmond and H Zlegler. pp 263-324. Spnnger-
Monson R K and Williams G J III 1982 A correlation between
photosynthetic temperature adaptation and seasonal phenology
patterns in the shortgrass prairie. Oecologia (Beri.) 54, 58-62.
Mooney H A and Winner WE I 991 Partitioning response of plants
to stress. In Response of Plants to multiple Stresses. Eds. H
A Mooney, WE Winner andE J Pell. pp 129-141. Academic
Press, San Diego, USA.
Osmond C B, Winter K and Ziegler H 1982 Functional significance
of different pathways ofCOz fixation in photosynthesis. In Physiological Plant Ecology. II. Encyclopedia of Plant Physiology,
New Series, Vo112B. Eds. O L Lange, PS Nobel, C B Osmond
and H Ziegler. pp 480-547. Springer-Verlag, Berlin, Germany.
Pearcy R W and Ehleringer J R 1984 Comparative ecophysiology of
C3 and C4 plants. Plant Cell Environ. 7, 1-13.
:
Verlag, Berlin, Germany.
Caldwell MM, White R S, Moore R T and Camp ~ B 1977 Carbon
balance, productivity, and water use of col~-wmter des~rt shrub
communities dominated by C3 and C4 species. Oecologla (Beri.)
pearcy R W, Tumosa N and Williams K 1981 Relationship between
growth, photosynthesis and competitive interactions for a C3
and a C4 plant. Oecologia (Beri.) 48, 371-376.
Pereira J S and Chaves M M 1993 Plant water deficits in Mediter-
,
29,275-300.
.
Forseth IN,Ehleringer JR, WerkKS andCookCS 1984Fleld water
relations of Sonoran Desert annuals. Ecology 65, 1436-1444.
GebauerG, SchuhmacherM 1, KrsticB, Reh~erH and~iegler H 1987
Biomass production and nitrate metabolism ofAtrlplex hortensls
L. (C3 plant) and Amaranthus retroftexus L. (C4 plant) in cultures
at different levels ofnitrogen supply. Oecologia (Beri.) 72, 303314.
..
.
Gifford ~ ~ 1974.A companson o! pot~ntl~ p~otosynthesls, pr?dUCtlVlty and Yield of plant species Wlth dlffenng photosynthetlc
carbon metabolism. Aust. J. Plant Physiol. 1,107-117.
ranean ecosystems. In Water Deficits. Plant Responses from cell
to Community. Eds. J A C Smith and H Griffiths. pp 237-251.
BIOS Sci. Publ., Oxford, UK.
Piedade MT F, Junk W J and Long SPI 991 The productivity of the
C4 grass Echinochloa polystachya on the Amazon floodplain.
Ecology 72, 1456-1463.
Poorter H 1989a Interspecific variation in relative growth rate: on
ecological causes and physiological consequences. In Causes
and Consequences ofVariation in Growth Rate and Productivity.
Eds. H Lambers, M L Cambridge, H Konings and T L Pansopp
45-68. SPB Academic Publishing, The Hague, the Netherlands.
149
PoorterH
1989b Growth
and functional
Poorter
analysis:
approach.
H and Lewis
towards a synthesis oftheclassical
Physiol.
C 1986 Testing
rate: a method avoiding
Smith
Plant. 75, 237-244.
differences
curve-fitting
in relative
and pairing.
growth
Physiol.
Quick W P, Chaves M M, Wendler R, David M, Rodrigues M L,
Passaharinho J A, Pereira J S, Adcock M D, Leegood R C and
Stitt M 1992 The effect of water stress on photosynthetic
in four species grown
Cell Environ.15,
-
and Radosevich
SRI985
Relationships
of four annual
between growth
weeds. J. Appl.
Ecol.
1. Leaf
nitrogen,
in Chenopodium
use efficiency
growth,
and biomass
album (L.) and Amaranthus
(L.). Plant Physiol. 84,954-958.
Sage R F and Pearcy R W 1987b The nitrogen
and C4 species.
characteristics
retrlljlexus
Saxena
II. Leaf
nitrogen
of Chenonlldium
(L.) Plant Physiol.
Physiol.
Responses
and Amaranthu.\"
India.
responses to drought.
and shoots
of water-stressed
regulation
maize
and growth
plants.
Planta
by
147,
43-49.
plasticity
and growth
PC 1993 Differences
rate among drought-resistant
susceptible cultivars of durum wheat (Triticum
durum). Plant and Soil157,
155-166.
Slatyer
R O 1971 Relationship
tosynthesis
Slatyer.
between
pp 76-81.
Eds. M D Hatch,
J Wiley
turgidum
plant growth
in C3 and C4 species of Atriplex.
and Photorespiration,
in develop-
CB
and
L. var.
and leaf pho-
Utrecht
Von
-
Eds. J A C Smith
and H
exchange
among
use and growth
University,
Caemmerer
Utrecht,
S and
UK.
the biochemistry
ofleaves.
G
D
cultivars
Ph.D.
Some
of photosynthesis
relation-
and the gas
Planta 153,376-387.
C B 1991 Elevated
atmospheric
III. Interactions
with emphasis
partjai pres-
between
CO2, N nutrition
and irradiance
responses estimat-
Aust. J. Plant Physiol.
18, 137-152.
Zhang J and Davies W J 1990 Changes in the concentration
sap as a function
In Photosynthesis
account for changes in.leaf
Envirolj.
13,277-285.
and Sons, New York, USA.
GR Stewart
of changing
conductance
Triticum
(C4) during growth
on below-ground
ed using the 13ÓC value of root biomass.
in xylem
in
Thesis.
155 p.
1981
aestivum (C3) and Echinochloafrumentacea
treatments,
wheat
parameters.
the Netherlands.
Farquhar
sure of CO2 and plant growth.
Section editor:
.
Plant
P J 1980 Adaptation
of Plants to Water
Stress. pp 7-353. J Wiley and Sons, New
Osmond
and R O
and
Deficits.
Sci. Publ., Oxford,
in mixed culture under different
Simane B, Peacock J M and Struik
mental
BCOS
communication
flux. In Water
R 1995 Variation
of water
Wong S C and Osmond
W J 1979 Solute
of water
York, USA.
Van den Boogaard
ships between
Aust. J. Plant
The Benjamin/Cummings
Cell to Community.
Turoer N C and Kramer
and high Temperature
and allocation
Can. J. Bot. 61, 1300-1306.
from
Budapest,
City, USA. pp 346-356.
W J 1993 Root-shoot
regulation
pp 147-162.
efficiency
weeds of slash and hum agriculture
1986 Whole-plant
Griffths.
on the gas exchange
(L.)
13, 127-141.
Sharp R E and Davies
roots
effects
album
parti-
FIorae Vege-
Kiad6,
432-433.
1991 Plant Physiogy.
F and Davies
and Co.,
- növényföldrajzi
- Geobotanica
Tomus V. Akadémiai
Co., Inc., Redwood
whole-plant
of C3
UK. 345 p.
2nd ed. Freeman
rendszertani
Systematico
pp 268-269,
of C3
retro.flexus
use efficiency
P S 1983 Growth
of some perennial
in northeastem
Schulze E-D
Hungariae.)
Publishing
84,959-963.
K G and Ramakrishnan
strategies
(Jhum)
tationisque
Tardieu
and C4 species.
tioning
(Synopsis
Taiz L and ZeigerE
22,
896-905.
P1ant responses
of C3 and C4 plants: a reassess-
J 1981 Biometry.
kézikönyve.
Hungary.
Sage R F and Pearcy R W 1987a The nitrogen
.
Plant
25-35.
and competitiveness
Deficits.
Sci. Publ., Oxford,
New York, USA. pp 208-270.
S06 1973 A magyar fl6ra és vegetáci6
carbon
under field conditions.
BIOS
ment. Funct. Eco1. 5,321-330.
Sokal R R and RohlfF
metabolism
H 1993 Water
Snaydon R W 1991 The productivity
Plant.
67,223-226.
RoushML
J A C and Griffihs
from Cell to Community.
of ABA
soil water
status can
and growth.
Plant Cell