Nocturnal and daytime stomatal conductance respond to root-zone temperature in 'Shiraz' grapevines.

1.3 MB·English

by  Rogiers, Suzy Y.

Annalsof Botany111:433–444, 2013
doi:10.1093/aob/mcs298,availableonlineatwww.aob.oxfordjournals.org
Nocturnal and daytime stomatal conductance respond to root-zone
temperature in ‘Shiraz’ grapevines
Suzy Y. Rogiers1,2,* and Simon J. Clarke1,3
1National Wine and Grape Industry Centre, Wagga Wagga, NSW, Australia, 2NSW Department of Primary Industries,
Wagga Wagga, NSW, Australia and 3School of Agriculture and Wine Science, Faculty of Science, Charles Sturt University,
Wagga Wagga, NSW, Australia
*For correspondence. E-mail [email protected]
Received:30August2012 Revisionrequested:8November2012 Accepted:3December2012 Publishedelectronically:4January2013
†BackgroundandAimsDaytimeroot-zonetemperaturemaybeasignificantfactorregulatingwaterfluxthrough
plants.Waterfluxcanalsooccurduringthenightbutnocturnalstomatalresponsetoenvironmentaldriverssuch
as root-zone temperature remains largely unknown.
†Methods Here nocturnal and daytime leaf gas exchangewas quantified in ‘Shiraz’ grapevines (Vitis vinifera)
exposed tothree root-zone temperatures frombudburstto fruit-set, foratotalof8weeksin spring.
†Key Results Despite lower stomatal density, night-time stomatal conductance and transpiration rates were
greaterforplantsgrowninwarmroot-zones.Elevatedroot-zonetemperatureresultedinhigherdaytimestomatal
conductance, transpiration and net assimilation rates across a range of leaf-to-air vapour pressure deficits, air
temperatures and light levels. Intrinsic water-use efficiency was, however, lowest in those plants with warm
root-zones. CO response curves of foliar gas exchange indicated that the maximum rate of electron transport
2
and the maximum rate of Rubisco activity did not differ between the root-zone treatments, and therefore it
waslikelythatthelowerphotosynthesisincoolroot-zoneswaspredominantlytheresultofastomatallimitation.
One week after discontinuation of the temperature treatments, gas exchange was similar between the plants,
indicating a reversible physiologicalresponseto soiltemperature.
†Conclusions In this anisohydric grapevine variety both night-time and daytime stomatal conductance were
responsive to root-zone temperature. Because nocturnal transpiration has implications for overall plant water
status,predictiveclimatechangemodelsusingstomatalconductancewillneedtofactorinthisroot-zonevariable.
Keywords: Water-use efficiency, leaf gas exchange, CO assimilation, grapevine, Vitis vinifera, stomatal
2
conductance,root-zone temperature, ‘Shiraz’,grapevine, soiltemperature.
INTRODUCTION characterizing the consequences of soil moisture on leaf
gas exchange, soil temperature has also been found to
Rising global temperatures can be accompanied by smaller, affectstomatalconductance andphotosynthesis inperennials
but significant, changes in soil surface temperatures (van (CaiandDang,2002;Wanetal.,2004; Wuet al.,2012) and
Gestel et al., 2011) and this has the potential to affect root annuals (He and Lee, 2001; He et al., 2001; Zhang et al.,
physiology and root activity. In particular, a gradual rise in 2008). Root-zone temperature can restrict photosynthesis
night-time air temperature over the past few decades (Vose through alterations in photosynthetic reactions (Cai and
et al., 2005) has probably resulted in an increase in soil tem- Dang, 2002; Zhou et al., 2004; Erice et al., 2006) or
perature during the night and early morning, depending on changes in stomatal conductance (Wan et al., 2004). For in-
soil depth. Root growth (Larson, 1970; Kasper and Bland, stance,borealandalpine plants areoftenexposed tolow soil
1992), water uptake (Wan et al., 1999), nutrient uptake and temperature stress and in conifer species the maximum rate
availability (MacDonald et al., 1995; BassiriRad, 2000; of carboxylation (V ) and the maximum rate of electron
c,max
Melillo et al., 2002; Pregitzer and King, 2005) and signal transport (J ) increased with soil temperature up to an
max
transduction (Zhang et al., 2008; Field et al., 2009) are all optimum and then declined (Cai and Dang, 2002).
influenced by the temperature of the soil. These processes Conversely, it was found that when Populus tremuloides
affect above-ground growth (Lopushinsky and Kaufmann, was exposed to low temperatures soil net assimilation was
1984; Dawes et al., 2011; Rogiers et al., 2011b) and product- limited by stomatal conductance (Wan et al., 1999). As a
ivity (He et al., 2001). As a result, analogous to air tempera- consequence, it was suggested that similar root-to-shoot sig-
ture, soil temperature can limit the geographical distribution nalling pathways may operate in plants subjected to drought
of plants and crops (Fosaa et al., 2004). and low root temperature (Wan et al., 2004). As such, it was
Leaf gas exchange is particularly responsive to the found that roots of Cucurbitaceae species can regulate
root-zone environment. While there are many studies stomatal behaviour in response to root-zone temperature by
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434 Rogiers & Clarke — Soil temperature and gas exchange in grapevines
modifying delivery of abscisic acid (ABA) to shoots and water at controlled temperatures through a 1.1-m long coil of
leaves (Zhang et al., 2008). 13-mm polyethylene irrigation tubing inserted within the pot
Those environmental parameters regulating stomatal con- and embedded through the root-zone to a depth of 30cm. This
ductance (g) and transpiration (E) during the day may also tubingwasattachedto50-mmDWVpipeconnectedtoarecircu-
exert some control during the night. Stomata can remain par- lating water system (UPS 32-80 N 180; Grundfos, Bjerringbro,
tially open during the night and, although the function of Denmark) and one of three temperature-controlled 1200-litre
night-time transpiration is yet to be resolved, this can result water tanks. The sides and bottom of the pots were insulated
in substantial night-time transpiration if the vapour pressure with blue 10-mm dense foam to minimize heat exchange
difference between the leaf and air (VPD) is high. In some between the soil and air or ground. At the time of re-potting, a
species and varieties, nocturnal transpiration can even cause soil temperature probe (DS18B20; Maxim Integrated Products,
disequilibrium in plant water status (Caird et al., 2007; Sunnyvale, CA, USA) was inserted into the centre of the root
Dawson et al., 2007; Fisher et al., 2007; Kavanagh et al., mass of every vine. A TDR soil moisture probe (Trace; Soil
2007). For instance, Vitis vinifera ‘Grenache’, an isohydric Moisture Equipment Corp., Santa Barbara, CA, USA) was also
grapevine variety, has low g both during the day and night. inserted in the same location in nine pots per treatment. Both
This is in contrast to ‘Semillon’, an anisohydric variety, with these probes were logged at 30-min intervals (Mini Trase data
comparatively high g throughout the diurnal cycle and as a logger; Soil Moisture Equipment Corp.). A weather station,
result incomplete plant rehydration prior to dawn especially equipped with an air temperature probe (Intercap HMP50;
during warm, windy nights (Rogiers et al., 2009). Aside Vaisala, Hawthorn, VIC, Australia) and a quantum sensor
from inherent genetic factors, nocturnal g appears to be influ- (Apogee,SQ-110;LoganUT,USA)loggingathalfhourlyinter-
enced byabioticfactorssuchasVPD,wind,atmosphericCO vals,wasplacedatcanopyheightwithinthetrial.Tenweeksprior
2
concentration and soil moisture (Ludwig et al., 2006; Howard tobud-burst,theplantswereprunedtotwospurs,eachcarrying
and Donovan, 2007; Zeppel et al., 2010, 2012). Another key two buds. After bud-burst the plants were irrigated daily and
environmental factor which may regulate nocturnal g is root- excess water was allowed to drain from the bottom of the pot.
zonetemperature.Todate,theconsequencesofroot-zonetem- Beginning 25 d after bud-burst plants were fertilized with
peratureonnocturnalstomatalconductance,toourknowledge, 200mL tap water containing 1mL nutrient concentrate
are unknown. It is therefore difficult to incorporate soil tem- (Megamix Plus, equivalent to N/P/K 130:100:150mg per
peratureintocropproductionmodelsbecausethereislittlein- plant)every5duntilveraison,thenevery10dthereafter.
formation available on how soil temperature affects daytime
and especially night-time foliar gas exchange.
Root-zone temperature treatments
Weassessedthefoliargasexchangeresponseof‘Shiraz’,an
anisohydricgrapevinevariety(Schultz,2003)originatingfrom Threeroot-zonetemperaturetreatmentswereinitiatedatthe
temperate Bordeaux, France, and grown widely in warm cli- onset of budburst (E-L Stage 4) and terminated at fruit-set
mates across southern Australia and Argentina. ‘Shiraz’ is (E-L stages 27–29). The root-zone temperatures were
grown across a broad range of latitudes, elevations and topo- allowed to fluctuate diurnally, with the ambient treatment
graphic conditions that expose this variety to a wide range in mimicking the nearby vineyard under-vine soil at a depth of
root-zone temperatures. Slope orientation and the extent of 15cm. Maximum root-zone temperatures over the 63-d treat-
ground cover in the inter-row area by cover crops or weeds ment period averaged 16.9+0.38C for the cool, 22.6+
will also affect the temperature of the soil. Other factors 0.58C for the ambient and 24.8+0.48C for the warm treat-
such as rain patterns, irrigation and soil type influence ment, while minimum root-zone temperatures averaged
rooting depth, and therefore root-zone temperature, and this 13.3+0.3, 17.8+0.58C and 22.6+0.28C, respectively.
will also affect plant response. The objective of this work Air temperature at the canopy level (approx. 1m above the
wastoclarifytheroleofroot-zonetemperatureonbothnoctur- soil surface) was not altered by the treatments and ranged
nal and daytime g in ‘Shiraz’. Using well-watered grapevines between an average minimum of 10.38C and maximum of
grown in three different root-zone temperatures for 2 months 28.58C. VPD ranged between 1.97 and 0.17kPa while daily
we assessed the response of g to this below-ground parameter maximum photosynthetically active radiation (PAR) averaged
during both the day and the night. The three root-zone tem- 1200mmolm22 s21. Soil moisture over the 63-d treatment
peratures consisted of ambient, 58C below or 58C above period averaged 21.9+1.3% for the cool, 21.5+1.4% for
ambient levels to encompass the natural variation that can the ambient and 21.1+1.4% for the warm treatment.
occur across a vineyard site in spring.
Plant measurements
MATERIALS AND METHODS Instantaneous net assimilation, stomatal conductance, tran-
spiration and leaf intercellular CO concentrations were mea-
Plant material 2
sured using a portable photosynthesis system (LI-6400;
Six-year-old‘Shiraz’grapevines(n¼60)ontheirownroots(Vitis LI-COR Biosciences Inc., Lincoln NE, USA). Midday mea-
vinifera L., clone 1654) were re-potted during dormancy into surementswerecarriedoutweeklyfrombud-bursttofruit-set.
40-litre pots containing a well-draining potting mix. The plants An artificial red–blue light source attached to the chamber
were placedoutdoors ina bird-proof enclosure in a randomized head was used to illuminate the leaf at 1500mmolm22 s21
blockdesignsurroundedonallsidesbybufferplants.Theroot- PAR. The CO concentration of the incoming air was main-
2
zone temperature treatments were administered by circulating tained at 400mmolmol21 and the block temperature was set
Rogiers & Clarke — Soil temperature and gas exchange in grapevines 435
at 258C. On each shoot (18 plants per treatment with four J , the maximum rate of electron transport, V , the in
max c,max
shoots per plant), the leaf opposite the basal inflorescence vivo maximum rates of Rubisco activity, and R , the day res-
d
(most often located at the fourth or fifth node from the base) piration, according to the method of Greer and Weedon
wasmeasured.Nocturnalmeasurements(nineplantspertreat- (2012) using SAS 9.1 (SAS Institute Inc., Cary, NC, USA).
ment)werecarriedoutevery2weeksonthesameleavesprior
todawnwiththechamberlightturnedoff,incomingCO con-
2
centration set at 400mmolmol21 and the block temperature Statistical analysis
set to 188C. Time-integrated values of transpiration were cal- SigmaPlot graphing and statistics software (version 12.3;
culated based on a normal distribution of leaf stomatal tran- SPSS Inc., Chicago, IL, USA) was used to fit linear or non-
spiration (Rogiers et al., 2009), over a 15-h light period and linear regressions of gas exchange parameters with soil tem-
constant E during the 9-h dark period. Light, temperature perature, air temperature, VPD and PAR. The three-
and VPD response curves were carried out at midday, 43–50 dimensionalmeshplotsofnocturnalleafstomatalconductance
d after the onset of the root-zone temperature treatments, on (g ) and nocturnal leaf stomatal conductance (E ) with soil
n n
four to six plants per treatment. VPD was not controlled in moisture and root-zone temperature were created with
the temperature or light response curves. smoothed data calculated from running averages using
Leaf chlorophyll was assessed non-destructively with a SigmaPlot. An analysis of variance (GenStat release 15.0;
chlorophyll meter (SPAD-502; Minolta Co., Ltd, Tokyo, VSN, Hertfordshire, UK) was used for comparison of treat-
Japan) twice weekly from 30 d after bud-burst to fruit-set. ment effects during the root-zone temperature treatments and
The meter readings were converted to chlorophyll content least significant differences were calculated at 5% signifi-
using a calibration curve derived from paired meter and spec- cance. Results of the statistical analyses are presented in
trophotometer readings. The spectrophotometer readings were the tables and figures. Values presented in the text are
converted to an estimate of chlorophyll content following the means+s.e.
method of Steele et al. (2008). Measurements were carried
out on the leaf opposite the basal inflorescence and all
leaves opposite the basal tendril in the three-node repeating RESULTS
metamer pattern that occurs along V. vinifera shoots.
Nocturnal gas exchange
Stomatal density was assessed on these same leaves on six
plants per treatment according to the method of Rogiers Nocturnalleafstomatalconductance,gn,(P,0.001)andtran-
et al. (2011a). spiration, En, (P,0.001) responded to root-zone temperature
(Table1).Inthecoolroot-zonetreatment,g was14.5%lower
n
thanintheambienttreatmentand20.7%lessthaninthewarm
treatment. Similarly, compared with the ambient and warm
A/C responses to root-zone temperatures
i root-zone treatments, E was 13.8 and 19.8% lower, respect-
n
Measurements of photosynthetic responses to cool and ively, in the cool treatment. This decline was apparent
warm root-zone temperatures were carried out 50 d after without any treatment differences in soil moisture (P¼
onset of treatments on four plants per treatment, targeting 0.105) which averaged at 20.9% at the time of measurement.
fully expanded leaves opposite the basal inflorescence. The A linear regression of g with soil moisture at the time of the
n
leaf respiration/internal CO concentration (A/C) response gasexchangemeasurements(P,0.01)explainedonly4%of
2 i
was measured according to Ainsworth et al. (2002). the variance in the data while a regression of this parameter
Photosynthesis was initially measured at 400mmolmol21 with root-zone temperature (P,0.002) accounted for 3% of
CO under saturating light (1500mmolmol21 s21) and a the variance. Further detailed examination of these two envir-
2
block temperature of 258C, until A was steady-state. The onmental parameters, however, showed that vines exposed to
CO concentration surrounding the leaf (C ) was then high root-zone temperatures combined with high soil moist-
2 a
reduced to 50mmolmol21 over nine steps with A and C ures had highest g and E values while those exposed to
i n n
recorded as soon as C was stable. C was then returned to low temperatures and low moisture responded with low g
a a n
400mmolmol21 and increased over eight steps to and E (Fig. 1). The combined factors of leaf age, leaf
n
2000mmolmol21. Each A/C curve was processed to obtain temperature, soil moisture and soil temperature accounted
i
TABLE 1. NocturnalleafA,gn,EnandCiofgrapevinesundercool,ambientorwarmroot-zoneconditions
Root-zone Soilmoisture A g E C
n n i
Treatment temperature(8C) (%) (mmolCO m22s21) (molHOm22s21) (mmolHOm22s21) (mmolmol21)
2 2 2
Cool 14.8a 21.2a –0.53a 0.0314a 0.275a 455.2a
Ambient 20.8b 20.9a –0.45a 0.0367b 0.319b 437.8b
Warm 24.2c 19.7a –0.48a 0.0396b 0.343b 435.5b
LSD 0.2 1.8 0.11 0.0034 0.025 11
F-test,P, 0.001 0.179 0.199 0.001 0.001 0.001
Valuesaremeansofthreesamplingdatesovera60-dtreatmentperiod(n¼9oneachsamplingdate).Root-zonetemperaturesandsoilmoisturesrepresent
themeansatthetimethegasexchangemeasurementsweremade.MeansfollowedbydifferentlettersaresignificantlydifferentatP,0.05.
436 Rogiers & Clarke — Soil temperature and gas exchange in grapevines
A
0·06
0·01
0·05
0·02
1–) 0·03
s
2 0·04
–
m 0·04 0·05
O
2
H
lom 0·03
( n
g 26
0·022 2244
2222
%%)
2200 ee ((
0·011 1188 uurr
sstt
2244 16 oii
22 m
Soil te2m0pera1t8ure (°1C6) 14 12 1214 Soil
B
0·40
0·10
0·35 0·15
0·20
1–) 0·25
s
2 0·30 0·30
–
m 0·35
O 0·40
H2 0·25
lo
m
m 0·200
( n 226
E
2244
0·155
2222
%%)
2200 ee ((
0·100 1188 uurr
sstt
2244 1166 ooii
2222 mm
Soil te2m0pera1tu8re (°1C6) 14 12 1214 Soil
FIG. 1. Nocturnalleaf(A)gnand(B)Enasafunctionofroot-zonetemperatureandsoilmoisture.‘Shiraz’plantsweretreatedwithcool,ambientorwarm
root-zoneconditionsovera60-dperiodfrombud-bursttofruit-set.Smootheddatarepresentthreesamplingdates(n¼9oneachsamplingdate).
for 31% of the variance in g (P,0.001) and 58% of the Midday gas exchange
n
variance in E (P,0.002).
n Asleavesmaturedovera20-dperiodofrapidshootgrowth,
Leaf respiration (–A) was not affected (P¼0.20) by root-
midday stomatal conductance (g ) increased (P,0.001) and
zone temperatures and averaged 0.49mmol CO m22 s21 d
2 had doubled by the time full lamina expansion had taken
(Table 1). Internal CO concentrations (C), were higher by
2 i place. This occurred in all three treatments within 1 month
about 20mmolmol21 in cool root-zone temperatures com-
after bud-burst (Fig. 2). On each measuring date, g was sub-
pared with the other treatments (P,0.001), although this d
stantially less in the cool root-zone as compared with the two
was apparently not linked to g because a linear regression
n other treatments. As the season progressed, air temperatures
of C with g was not significant (P¼0.15).
i n
Rogiers & Clarke — Soil temperature and gas exchange in grapevines 437
rose, the soil temperatures of the ambient and thewarm treat- This was not the result of earlier bud-burst in the warm or
ments converged, and so did leaf g of plants grown in those later bud-burst in the cool treatment because bud-burst oc-
d
treatments. curred at roughly the same time for all the treatments (P¼
RatesofCO assimilation(A)werehighestinthewarmand 0.37). Leaf development after bud-burst may have proceeded
2
lowestinthecoolroot-zonetemperatures(P,0.001),eachdi- at a greater rate in the warm root-zone treatment, but even
verging by about 5% from the ambient treatment (Table 2). though leaves of plants grown in this treatment were larger
(Table 4), lamina length and A were not correlated (P¼
0.822). Higher A was also not due to higher chlorophyll
levels in warm plants because chlorophyll levels in the
35 leaves from nodes 2 to 6 over this period were not different
A
from each other in the cool and warm treatments (Table 3).
30 Soil moisture can also not explain these differences because,
at the time gas exchange was measured, this parameter
°C) 25 varied only slightly between the treatments with lower levels
e ( in the warm treatment (22.8+0.5% for cool, 22.6+0.5%
eratur 20 finorstaommbaiteanltcalonsdur2e0.a6n+d d0e.c5li%nefionrAwarramth)erwthhiacnhawnoiunlcdreraesseu.lt
p
m Despitenodifferencesinsoilmoisturebetweenthecooland
e
oil t 15 the ambient treatments, midday gd (P,0.001) and Ed (P,
S 0.001) were lower by 22 and 17%, respectively, in the cool
10 Cool treatment (Table 2). While there were no differences in g or
Ambient d
E between the ambient and warm treatments, regressions of
Warm d
5 gd and Ed with root-zone temperature were highly (P,
0.001) significant (Fig. 3). During a 9-h period of darkness,
0·35
B total E amounted to 160mL H O m22 leaf area in the cool,
n 2
186mL H O m22 in the ambient and 200mL H O m22 in
0·30 2 2
the warm treatment. During the 15-h light period, total E
d
–1) amounted to 1312mL H2O m22 in the cool, 1584mL H2O
2 s 0·25 m22intheambientand1580mLH2Om22inthewarmtreat-
–
m ment. Daily E as a proportion of E varied by only 1%
O 2 0·20 between the trenatments (12.2% for thed cool treatment, 11.7
ol H % for the ambient treatment and 12.7% for the warm
m treatment).
(d 0·15 Plantsgrownwithcoolroot-zoneshad15%greatertranspir-
g
Cool ation efficiency (A/E) (P,0.001) and 23% greater intrinsic
0·10 Ambient transpiration efficiency (A/g) (P,0.001) than plants grown
Warm in ambient soil (Table 2). Those grown in the warm soil also
0·05 hadsomewhathigherA/g(6%)butthismayhavebeenanarte-
25 30 35 40 45 50 55
fact of the slightly reduced soil moistures in this treatment.
Day of soil temperature treatment
While there were no differences in A/E between the ambient
FIG. 2. (A) Average root-zone temperature of the cool, ambient and warm and warm treatments (Table 2), the regression of A/E with
treatments (n¼18), and (B) midday leaf stomatal conductance (gd) in re- soil temperature was significant due to the strong cool treat-
sponse to cool, ambient and warm root-zone temperatures applied over a
ment effect (Fig. 3). Similar to g , midday leaf C was some-
60-d period from bud-burst to fruit-set in ‘Shiraz’ vines. The first measure- d i
whatless(7%)inthecool treatment, indicatingdepleted CO
mentsweremadewhenleavesoppositethebasalinflorescencehadobtained 2
anapproximateareaof10cm2. concentrations and a stomatal limitation to photosynthesis.
TABLE 2. MiddayleafA,gd,Ed,A/g,A/EandCiofgrapevinesundercool,ambientorwarmroot-zoneconditions
Root-zone A(mmolCO g (molHO E (mmolHO A/g(mmolCO A/E(mmolCO C (mmolCO
2 d 2 d 2 2 2 i 2
Treatment temperature(8C) m22s21) m22s21) m22s21) mol21HO) mmol21HO) mol21air)
2 2
Cool 16.7a 8.83a 0.155a 2.70a 62.0a 3.74a 262.3a
Ambient 23.1b 9.17b 0.198b 3.26b 50.5b 3.24b 280.0b
Warm 26.5c 9.60c 0.201b 3.25b 53.8c 3.35b 275.4b
LSD 0.3 0.30 0.006 0.09 2.7 0.13 5.0
F-test,P, 0.001 0.001 0.001 0.001 0.001 0.001 0.001
Valuesaremeansofsevensamplingdatesovera60-dtreatmentperiod(n¼18oneachsamplingdate).Root-zonetemperaturesrepresentthemeansatthe
timethegasexchangemeasurementsweremade.MeansfollowedbydifferentlettersaresignificantlydifferentatP,0.05.
438 Rogiers & Clarke — Soil temperature and gas exchange in grapevines
TABLE 3. Leaf chlorophyll concentrations and leaf 0·40
photosynthetic characteristics derived from intercellular CO A
2
response curves of mature leaves that emerged during the cool
0·35 Cool
orwarmrootzonetreatments(n¼4) 1) Ambient
Treatment C(hmlogromp2h2y)ll (mmJso2ml1axm) 22 (mmVsco2,ml1am)x22 (mmsoR2ld1m) 22 –2–O m s200··3205 Warm
H
ol
Cool 424.4a 91.0a 34.8a 0.29a m 0·20
Warm 424.9a 97.1a 33.0a 0.58a (d
LSD 2.56 17.4 9.15 0.45 g
F-test,P, 0.756 0.442 0.655 0.18 0·15
Jmaxisthemaximumrateofelectrontransport,Vc,maxistheinvivo 0·10
maximumratesofRubiscoactivityandR isthedaytimerespirationrate.
d 6·0
Chlorophyllconcentrationsrepresentaveragesofnodes2–6ofweekly
B
measurementsduringthetemperaturetreatments(n¼18plants,fourshoots
5·5
perplant).Meansfollowedbydifferentlettersaresignificantlydifferentat
P,0.05.
1) 5·0
–
s
2
–m 4·5
Light, temperature and VPD response curves
O
24·0
Air temperature, light and VPD response curves (Figs 4–6) H
provide more extensive data of how leaf gas exchange was mol 3·5
affected by root-zone temperatures. In both cool and warm m
root-zones, stomata were progressively more closed across an E (d3·0
airtemperaturerangeof18–388C(Fig.4).VPDwasnotcon-
2·5
trolled over this temperature range and E increased linearly
d
(P,0.001)withairtemperatureinbothroot-zonetemperature 2·0
treatments.However,Adidnotchangewiththisenvironmental 90
parameterineitherthecool(P¼0.38)orthewarm(P¼0.73) C
root-zones. C followed similar trendsto that of g with lower 80
values in theicool root-zones. d O)
H270
ThereweresimilartrendsingdandEdwithincreasingVPD –1
(Fig. 5). While g declined, E increased linearly across the ol 60
d d m
wVePrDe draonugbeleof(s1lo–p4ek1P.9a.mInmcroelaHse2sOinmE2d2ins2th1ekwPaa2rm1)rtohoatt-iznonthees CO 250
cool root-zones (slope 0.86mmol H2O m22 s21kPa21) (P, mol 40
0.001). Despite stomatal closure, A increased slightly with µ
VPD in both root-zone treatments. C was lower in the cool g ( 30
i A/
root-zones and responded in a curvilinear manner to VPD,
20
unlike in the warm root-zone treatment.
Aswiththe airtemperatureandVPDcurves,light response 10
curves showed good separation between the root-zone treat-
5
ments with higher values in the warm treatment as compared D
with the cool treatment (Fig. 6). Both g and E increases
were curvilinear and did not plateau untidl the hidghest PAR O) 4
2
value tested (2000mmolm22 s21). A increased steeply in re- 1 H
–
sponse to rising PAR and leaves from the warm root-zone ol
m 3
reached a 15% higher plateau at 1000mmolm22 s21 than in 2
O
the cool root-zone. Conversely, Ci values declined with in- C
creasing PAR and above 1500mmolm22 s21 C settled at ol 2
i m
300mmolmol21 in the warm and 260mmolmol21 in the µ
cool root-zone treatment. E (
A/ 1
FIG. 3. Middayleafgd,Ed,A/gandA/Easafunctionofroot-zonetempera- 0
ture48daftertheonsetoftreatments.Soilmoisturewasnotdifferentbetween
10 12 14 16 18 20 22 24 26 28 30 32
the treatments (F-test, P¼0.72) and averaged 22.6+1.4% at the
time of measurement. F-test of linear regression for g¼0.001, E¼0.001, Soil temperature (°C)
A/g¼0.001andA/E¼0.001;varianceaccountedforing¼0.47,E¼0.49,
A/g¼0.34andA/E¼0.19.
Rogiers & Clarke — Soil temperature and gas exchange in grapevines 439
Leaf and photosynthetic characteristics 0·28
A
Cool
A/Ci curves in response to root-zone temperatures are pre- 0·26 Warm
sented in Fig. 7. Further analyses of these curves indicate
there were no differences in Jmax (P¼0.44) or Vc,max (P¼ –1s) 0·24
0.65) between the treatments and they averaged 94.1+7.5 –2 0·22
and 33.0+4.0mmolm22s21, respectively (Table 3). O m 0·20
Daytime dark respiration was also not different between the 2
H
treatments (P¼0.18) and averaged 0.4+0.2mmolm22 s21. ol 0·18
m
F(Pur¼the0r.m75o)rea,ndleaavfercahgloedro4p2h4y.l6l +co1n.c3enmtrgatmio2ns2.did not differ g (d 0·16
Oneleafcharacteristicthatdiddifferbetweenthetreatments 0·14
was stomatal density. Of those leavesthat emerged during the
0·12
treatments,stomataldensitywas10%(P,0.05)higherinthe
cooltreatmentascomparedwiththewarmtreatment(Table4). B
Despite 8% larger leaves in the warm treatment as compared 7
with the cool treatment (Table 4), therewas no significant re- –1)
lationship between stomatal densityand leaf area (F-test, P¼ 2 s 6
–
0.10 for a data set with combined treatments), and therefore m
O 5
other factors aside from leaf area appear to be involved. 2
H
There were no differences in stomatal density of those leaves ol 4
m
that emerged after the discontinuation of the treatments and m
they averaged 125.6+5 stomata mm22. Note, however, that (d 3
E
stomatal density of newly emerging leaves of plants grown
2
in the warm treatment increased by 11% after that treatment
had been removed. As averaged over 60 d following the ter- 1
mination of the treatments, leaf length remained 6% larger
13
in the warm treatment than the cool treatment (P,0.001). C
12
1)
Gas exchange after termination of the treatments –s
2
–
Afterdiscontinuationofthetreatmentsthemiddayroot-zone m 11
temperaturesaveragedat20.6+0.38Candvariedbylessthan O2
C
4% (Table 5). Despite equal amounts of water applied, soil ol 10
moisturewasslightly(3%)higherinthoseplantsthatreceived m
µ
thecooltreatment ascomparedwiththewarmtreatment. This A ( 9
is probably because the cool plants had less total leaf area
(Table 4) and therefore less whole plant transpiration and
lower rates of soil water utilization. Leaf A, g and E were 8
d d
nolongerdifferentbetweenplantsthathadpreviouslyreceived
D
the three treatments. 300
DISCUSSION 1) 280
–
ol
Nocturnal stomatal conductance m
ol
Our study confirms that daytime stomatal conductance of m 260
µ
grapevines, like many other species, responds to root-zone C (i
temperature. Our present findings extend this observation to
240
nocturnal stomatal conductance. There is very little experi-
mental work on the interaction of root-zone temperatures
with nocturnal gas exchange and we believe this is one of 220
15 20 25 30 35 40
the first reports to characterize this. Cool root-zones resulted
in a sustained suppression in g and E during both the day Air temperature (°C)
and the night and leaves transpired nearly 20% less than FIG.4. Middayleafgd,Ed,AandCiinresponsetoairtemperature(n¼4)of
thosegrowninwarmroot-zones.Asidefromthestomatallimi- vinesgrownineithercoolorwarmsoil.Atthetimeofmeasurement,root-zone
tationevidentinourdata,othershaveshownthatlowEcanbe temperatureofthewarmtreatmentwas26.9+1.38Candofthecooltreatment
was 15.0+1.08C (P,0.001). Soil moisture was not different between the
the result of reductions in both soil and plant hydraulic con-
treatments (F-test, P¼0.72) andaveraged 17.6+0.6%. The intercepts and
ductance (Kramer and Boyer, 1995; Fennel and Markhart,
slopes of the regressions for the cool and warm cohorts are different from
1998; Berndt et al., 1999) possibly through an increase in each other for g (P,0.001), E (P,0.001), A (P,0.001) and C (P,
d d i
water viscosity (Muhsin and Zwiazek, 2002). After 0.001).
440 Rogiers & Clarke — Soil temperature and gas exchange in grapevines
0·30 discontinuationofthetreatments,differencesinleafgdandEd
A
Cool werenolongerapparent.Thissignifiesthattheroot-zonetem-
Warm perature effect on gas exchange was not due to a permanent
0·25 anatomical change but rather a transient physiological effect,
–1s) perhaps relayed through signals targeted at the stomata.
–2m 0·20 Another study on aspen has demonstrated that low root-zone
O temperatures can reduce g through pH, ion and ABA signals
H2 transportedinthexylemsap(Wanetal.,2004).Itwouldthere-
ol 0·15 fore be expected that these signals persist throughout the
m
g (d diurnal cycle, including the night. The role of such signals
was not addressed in this study, however, and further work
0·10
is required to verify their contribution to g and g in
d n
grapevines.
0·05 The resultant reduction in g of plants growing in cool
n
root-zones may thus be an after-effect of daytime changes,
B
8 or it may offer a physiological advantage such as hastened
plant rehydration through concomitant decreases in E .
n
–2–1m s) 6 NsTphoricisntugir-sntiamsliemtriaclanorsnpdtioirtaitooinothsn,e,rwassaspseescsgieeedsnegirnarollwtyhnisabinsotuuwtdye1tt2eur%ndeenrovfimroEinldd-.
O
H2 ments (Caird et al., 2007; Dawson et al., 2007) and less
ol 4 than the 40–75% found in desert species (Ogle et al.,
m
2012). Substantial night-time transpiration as a consequence
m
(Ed 2 ocofmeplelevtaetepdlagnnt irnehwydarramtionnigphrti-otrimtoe droaowt-nzo(nKeasvamnaayghperetvaenl.t,
2007), resulting in greater water stress during the day as
evaporative demand increases. Because our plants were
0
well watered in all treatments with soil moistures not drop-
14 ping below 20%, soil moisture was not a stressor. In grape-
C vines, wilting tendrils at the shoot tips are the first signs of
13 water stress (Winkler et al., 1974) and we did not observe
this in any of our plants. In a field situation, however,
–1s) 12 under the absence of irrigation or under reduced water allo-
–2m cations, plants may experience daytime water stress due to
11
O 2 elevated night-time soil temperatures, especially in warm,
C dry climates. It follows then that daily minimum soil tem-
mol 10 perature may be just as critical as daily maximum or
A (µ 9 average soil temperature in determining plant water
relations.
8
7 Absence of acclimation
300
D One of most significant findings of this study was that sto-
280 matal conductance remained low in the cool root-zones
throughout the 2-month treatment period, with apparently no
260
temperature acclimation. Sustained reduction in g may be
–1ol) 240 requiredoverweeksifplantsaretopreventdehydration,espe-
m cially with rising middayand nocturnal VPD driving E asthe
ol 220 season progresses.
m
µ
C (i 200
180
FIG. 5. Midday leaf gd, Ed, A and Ci in responseto VPD (n¼4) of vines
grownineithercoolorwarmsoil.Atthetimeofmeasurement,root-zonetem-
160 perature of thewarmtreatmentwas 20.3+0.98C and of the cool treatment
was 13.3+0.78C (P,0.001). Soil moisture was not different between the
140
0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0 4·5 treatments(F-test, P¼0.50) and averaged 16.8+0.5%. The intercepts and
slopes of the regressions for the cool and warm cohorts are different from
VPD (kPa) eachotherforE (P,0.001),butonlytheinterceptforg (P,0.001)and
d d
A(P,0.001).Anon-linearcurvewasfittedtotheC dataofthecoolroot-
i
zonetemperaturetreatment (P,0.001).
Rogiers & Clarke — Soil temperature and gas exchange in grapevines 441
0·35 25
A
0·30 20
–2–1m s) 0·25 –2–1 s) 15
HO 2 0·20 O m210
mol 0·15 ol C
(d µm 5
g 0·10 Cool A (
Warm
0 Cool
0·05 Warm
–5
B 0 500 1000 1500
5
C (µmol mol–1)
i
1)
–
2 s FIG. 7. A/Cicurvesofgrapevinesgrowninwarmorcoolsoil(n¼4).Atthe
–m 4 time of measurement, root-zone temperature of the warm treatment was
O 25.9+0.88Candofthecooltreatmentwas15.1+1.38C(P,0.001).Soil
H2 moisturewasnotdifferentbetweenthetreatments(F-test,P¼0.12)andaver-
ol 3 aged18.0+0.5%.
m
m
(d
E 2 TABLE 4. Stomatal density of leaves that emerged during the
root-zone temperature treatments and of those leaves that
1 emergedafterthecessationofthetreatments
C Stomataldensity
12 (stomatamm22) Laminalength(mm)
–1) 10 During Following During Following
s
–2 8 Treatment treatments treatments treatments treatments
m
O 2 6 Cool 127.93a 127.04a 83.6a 77.2a
C Ambient 123.15ab 120.08a 87.0b 79.5b
ol 4 Warm 116.67b 129.70a 90.6c 81.8c
m
µ LSD 8.26 9.76 3.0 1.4
A ( 2 F-test,P, 0.018 0.127 0.001 0.001
0
Dataduringthetreatmentsarethemeansofleavesuptoandincluding
–2 node6,wheregasexchangemeasurementsweremade(n¼5plants,four
shootsperplant).Dataofleavesthatemergedafterthetreatmentswere
D discontinueduptonode27.Meansfollowedbydifferentlettersare
400
significantlydifferentatP,0.05.
380
1) 360
–
ol
m 340
ol Other factors controlling nocturnal stomatal conductance
m 320
µ Because nocturnal gas exchange has not yet received the
C (i300 same depth of attention as daytime gas exchange, far less is
280 known about the plasticity of g to environmental factors.
n
Wefoundthatasidefromroot-zonetemperature,soilmoisture
260
wasanothervariablethatimpingedonnocturnalstomatalcon-
240 ductance. Nocturnal stomatal conductance was found to
0 500 1000 1500 2000 2500
decline with drying soil (Cavender-Bares et al., 2007;
PAR (µmol m–2 s–1)
Howard and Donovan, 2007) and increasing VPD (Barbour
FIG. 6. Midday leaf gd, Ed, A and Ci in response to PAR (n¼6) of vines and Buckley, 2007) in other studies. VPD did not explain
grownineithercoolorwarmsoil.Atthetimeofmeasurement,root-zonetem- any of the variance in g in our ‘Shiraz’ plants but this may
perature of thewarmtreatmentwas 24.2+1.18C and of the cool treatment n
was 13.3+0.78C (P,0.001). Soil moisture was not different between the be because the leaf chamber temperature was held constant
treatments(F-test,P¼0.63)andaveraged17.6+0.9%. and the resultant VPD range was fairly narrow.
442 Rogiers & Clarke — Soil temperature and gas exchange in grapevines
TABLE 5. MiddayleafA,gd,EdandCiofgrapevinesafterroot-zonetemperaturetreatmentswerediscontinued
Root-zone A g E
d d
Treatment temperature(8C) Soilmoisture(%) (mmolCO m22s21) (molHOm22s21) (mmolHOm22s21) C (mmolmol21)
2 2 2 i
Cool 21.0a 23.6a 10.3a 0.223a 3.70a 286.2a
Ambient 20.2b 20.1b 10.2a 0.225a 3.74a 288.9ab
Warm 20.7a 20.0c 10.5a 0.218a 3.66a 283.0b
LSD 0.3 2.1 0.4 0.008 0.14 4.5
F-test,P, 0.007 0.001 0.314 0.703 0.573 0.038
Valuesaremeansofthreesamplingdatesovera54-dperiodafterthediscontinuationofthetreatments(n¼12oneachsamplingdate).Root-zone
temperaturesandsoilmoisturesrepresentthemeansatthetimethegasexchangemeasurementsweremade.Meansfollowedbydifferentlettersare
significantlydifferentatP,0.05.
In the first few weeks after bud-burst g increased with leaf overlooked in root-zone studies (Pregitzer et al., 2000), but
n
age, mimicking trends in g . Leaf maturity thus appears to be to mimic field conditions we allowed soil temperature to fluc-
d
anothervariablecontrollingg .Whenleavesfirstemergethere tuate diurnally by approximately 58C. Diurnal soil tempera-
n
is a progressive increase in g as stomata mature and the sto- ture fluctuations would also be relevant to newly established
d
matal apertures expand (England and Attiwill, 2011) and we seedlings with small root systems as well as shallow-rooted
reason that a similar developmental effect persists on g species growing on impenetrable soils.
n
during the night. We did not measure g during the latter
n
half of the season but ageing and senescing leaves often
Transpiration efficiency responds to root-zone temperature
have lower g and thus probably g as well, but this is yet to
d n
be verified. Other factors that might affect g and E include Despite greater A in warm root-zones, both A/g and A/E
n n
developmental stage of the plant and plant nutrient status were inversely proportional to root-zone temperature. In
(Ludwig et al., 2006). other words, leaves of plants grown in the warmer root-zones
lostgreateramountsofwaterperunitofcarbongained.Thisis
similartothedropintranspirationefficiencyofgrapevinevar-
Root-zone temperature regulates photosynthesis
ieties grown in high VPD (Du¨ring, 1987; Pou et al., 2008) or
Rates of CO assimilation were highest in the warm and ample soil moisture (Cuevas et al., 2006). There is wide var-
2
lowest in the cool root-zones, and this was apparent across a ietal diversity in transpiration efficiency of grapevines
wide range in PAR, VPD and air temperatures. The decline (Schultz, 1996; Bota et al., 2001; Gibberd et al., 2001;
inC valuesundercoolroot-zonetemperaturespointstoasto- Rogiersetal.,2009).Whiletheadoptionofirrigationtechnol-
i
matallimitationandthereforeacurtailedCO supplytophoto- ogy that confers water savings has improved water-use effi-
2
synthesis under these conditions. There were no apparent ciency at the vineyard level, further gains can be made by
limitations at the chloroplast level as chlorophyll content and planting inherently efficient varieties (Condon et al., 2004).
both J and V did not differ between the treatments. Varietal selection therefore must not only take into consider-
max c,max
This indicates that the low photosynthesis of the cool root- ation VPD and soil moisture responses but, as shown here,
zones was not due to Rubisco or RuBP limitations. Cai and soil temperature as well.
Dang (2002) found that root-zone temperature had an effect
on both J and V in conifer species, although a much
max c,max Stomatal density responds to root-zone temperature
widertemperaturerange(5–358C)wasemployed.Thesepara-
meters had a maximum at around 258C, declining at Stomatal density of concurrently formed leaves was lowest
supra-optimal temperatures. Similar to our grapevines, dark in the warm root-zone treatment and highest in the cool treat-
respiration was not affected by root-zone temperature in any ment. It would seem intuitive that the high stomatal densities
of the four species tested. of the cold treatment might lead to higher g and g , but as
d n
The key point is that soil temperature did influence A, and is apparent here, there was no such relationship. The low g
furthermore A was more sensitive to soil temperature than to characteristic of the cool root-zone treatment is therefore not
an air temperature range of 20–358C. Similarly, photosyn- due to low stomatal density and must be related to stomatal
thesis of red spruce saplings grown in a cold region was aperture only.
limited more by minimum soil temperature than minimum In a previous study on ‘Chardonnay’ grapevines it was
air temperature, especially in spring (Schwarz et al., 1997). found that root-zone temperature and atmospheric carbon
If this is the case for grapevines grown in cool regions, it dioxide both impinged on stomatal density (Rogiers et al.,
would be advantageous for the plant to direct root growth to 2011a).Becausethisleafparameterwascloselyandinversely
a depth where diurnal temperature fluctuations are dampened. correlated with starch concentration in roots and trunks we
Whenfieldgrapevinesaredripirrigated,however,mostofthe suggested that the carbohydrate reserve status of the plant
roots can be found in the top layers (Stevens and Douglas, may be an important endogenous determinant of stomatal
1994)andthereforetheyareexposedtosignificantfluctuations density. Depleted starch reserves, elicited by several weeks
in temperature. Natural daily cycling in temperature is often of high metabolism in the warm root-zones, would require