Published October 29, 2014

Climatology & Water Management

Potato Gas Exchange Response to Drought Cycles

under Elevated Carbon Dioxide
David H. Fleisher,* Jinyoung Barnaby, Richard Sicher, Jonathan P. Resop, D. J. Timlin, and V. R. Reddy
ABSTRACT

Elevated carbon dioxide (CO2) influences photosynthesis (AN), transpiration (ET), and water use efficiency (WUE) for wellwatered potato (Solanum tuberosum L.). Little is known regarding effects of short-term drought and CO2 . Two experiments,
differing in the quantity of solar radiation, were conducted in soil-plant-atmosphere-research chambers. Plants were grown at
ambient (aCO2) or twice-ambient CO2 (eCO2) and received one of three irrigation treatments: no water stress (C), short-term
(1116 d) water-withholding during vegetative and post-tuber initiation stages (VR), or post-tuber initiation (R) only. Canopy
conductance to CO2 transfer () and water vapor (G v), light use efficiency (), daily AN, and ET decreased at the onset of each
drought and were correlated with volumetric water content. The rate of decrease was similar for R and VR. G v declined more
sharply than AN, resulting in higher WUE. Seasonal AN declined with the pattern of C > R > VR and was higher for eCO2 C
and R treatments. Seasonal WUE was higher for eCO2 at all irrigation treatments. Total dry matter, harvest index, and leaf area
were reduced (p < 0.05) for droughted treatments and total dry matter and harvest index were also higher for eCO2 VR pots.
Relative responses to drought and CO2 were similar among experiments, with greater magnitude of response under high solar radiation. Findings were similar to those reported under longer-term water-withholding studies, suggesting that interactions between CO2
and drought on carbon assimilation and water use are conserved across production zones with varying radiation and rainfall patterns.

Intergovernmental Panel on Climate Change

predictions (IPCC, 2007) include a higher atmospheric CO2

concentration, warmer growing seasons, and an increase in
extreme weather events, including altered rainfall patterns.
Shifts in rainfall intensity, duration, and timing during the
growing season may reduce water availability in many agricultural regions (CCSP, 2008). This is of particular concern
to potato, which is frequently rain-fed (Schafleitner, 2009).
Numerous experiments were conducted on potato agronomic
responses to long-term, seasonal drought under ambient CO2
(aCO2) (e.g., Jefferies, 1995; Onder et al., 2005; Walworth
and Carling, 2002), but few evaluated such responses under
elevated CO2 (eCO2) (Fleisher et al., 2008a, 2008b), and none
examined interactions between elevated CO2 (eCO2) and
short-term drought periods. Although potato is grown under
similar thermal regimes worldwide, average solar radiation
can vary considerably across geographic locations (Haverkort,
2007). Evaluation of potato responses during shorter-term
drought cycles at eCO2 , and the influence of solar radiation
D.H. Fleisher, J. Barnaby, R. Sicher, D.J. Timlin, and V.R. Reddy, USDA-ARS Crop
Systems and Global Change Laboratory, Beltsville, MD 20705; and J.P. Resop,
University of Maryland, Department of Geography, College Park, MD 20703.
Received 4 Apr. 2014. *Corresponding author (david.fleisher@ars.usda.gov).
Published in Agron. J. 106:20242034 (2014)
doi:10.2134/agronj14.0220
Copyright 2014 by the American Society of Agronomy, 5585 Guilford
Road, Madison, WI 53711. All rights reserved. No part of this periodical
may be reproduced or transmitted in any form or by any means, electronic or
mechanical, including photocopying, recording, or any information storage and
retrieval system, without permission in writing from the publisher.

2024

on these responses, is therefore needed to develop adaptation

strategies for projected climate change impacts.
Potato exhibits positive responses to CO2 enrichment (Finnan
et al., 2005) as consistent with the majority of plants with the
C3 biochemical pathway (Baker and Allen, 1994). Dry matter
production, yield, and WUE increased in well-watered plants at
eCO2 levels ranging from 20 to 100% higher than current aCO2
levels (Conn and Cochran, 2006; Fleisher et al., 2008a, 2008b;
Hogy and Fangmeier, 2009; Kaminski et al., 2014; Miglietta
et al., 1998; Schapendonk et al., 2000; Sicher and Bunce, 1999;
Vandermeiren et al., 2002; Wheeler et al., 1999). Leaf-level
responses include higher net photosynthetic rates, decreased stomatal conductance and transpiration rate, and higher leaf WUE
(Kaminski et al., 2014; Ku et al., 1977; Sicher and Bunce, 1999).
While some authors measured photosynthetic acclimation in
potato leaves during the season, the decline was not enough to
offset positive gains in biomass production and WUE (Sicher
and Bunce, 1999). Leaf level measurements provide insight into
physiology, but are often difficult to scale to the whole plant (van
Abbreviations: , canopy light utilization efficiency (mol CO2 mol1
PAR); , canopy conductance to carbon dioxide transfer (m s1); aCO2 ,
ambient carbon dioxide concentration of 400 L L 1; AG , gross canopy
photosynthetic rate (mol CO2 m2 s1); AN, net canopy photosynthetic
rate (mol CO2 m2 s1); C, non-droughted control pots; CO2 , atmospheric
carbon dioxide concentration; DAE, days after emergence; ET, canopy
evapotranspiration rate (mol H2O m2 s1); E1, experiment 1; E2, experiment
2; eCO2 , elevated carbon dioxide concentration of 800 L L 1; G v, canopy
conductance to water vapor (mol H2O m2 s1); HI, harvest index; PAR,
photosynthetically active radiation; R, single droughted pots at post-tuber
initiation; TDR, time-domain reflectometry; VR, pots droughted at both
vegetative growth and post-tuber initiation; VWC, volumetric water
contents; WUE, water use efficiency

A g ro n o my J o u r n a l Vo l u m e 10 6 , I s s u e 6 2 014

Iersel and Kang, 2002). Using whole canopy gas exchange measurements, based on averaged CO2 and water vapor exchange
rates across multiple plants in the same enclosure, Fleisher et
al. (2012; 2008a, 2008b) observed higher canopy net and gross
photosynthesis (AN and AG), reduced transpiration (ET), higher
radiation use efficiency and WUE, yet similar leaf area production, for eCO2 vs. aCO2 grown plants
Potato drought responses are influenced by the duration and
timing of the water with-holding event with respect to developmental stage (Dalla Costa et al., 1997; Iqbal et al., 1999;
Kang et al., 2004; Kashyap and Panda, 2003; Schafleitner,
2009). Few articles in the literature report the impact of eCO2
on potato production and drought; however, under aCO2
responses include reduced leaf area, canopy size and duration
(Jefferies, 1995; Fleisher et al., 2008a, 2008b; Lahlou et al.,
2003; van Loon, 1981), decreased dry matter production and
yield (Dalla Costa et al., 1997; Deblonde and Ledent, 2001;
Fleisher et al., 2008a, 2008b; Schittenhelm et al., 2006; van
Loon, 1981), with higher harvest index and WUE (Belanger et
al., 2001; Fleisher et al., 2008a; Trebejo and Midmore, 1990).
Under aCO2 in enclosure studies, Vos and Groenwold (1989)
measured a larger effect of drought on canopy stomatal conductance than AN, resulting in improved whole plant WUE over a
period of 33 d. Dalla Costa et al. (1997) found that AN of plant
canopies that were water-stressed during vegetative growth was
more sensitive, and less able to recover to re-watering events,
as compared to plants water-stressed following tuber maturity.
Only two studies on potato, eCO2 , and drought interactions
were reported (Fleisher et al., 2008a, 2008b), in which the
authors found droughted plants had similar total biomass, but
higher harvest index, radiation use efficiency, and WUE compared with aCO2 grown potato. It was unclear whether these
responses to long-term drought would manifest under the more
likely to occur short-term water with-holding periods.
Basu et al. (1999) indicated that tuber sink strength could
mediate drought-based photosynthetic feedback inhibition
under aCO2 . In addition to reduced stomatal conductance,
which has been identified as the primary mechanism for
improving WUE in C3 (Finnan et al., 2005) and C4 crops
in particular (Allen et al., 2011), growth at eCO2 results in a
larger plant carbon assimilate pool which has the potential to
form an even stronger tuber sink, potentially increasing the
capacity for reducing photosynthetic feedback inhibition as
compared to aCO2 . Since this drought tolerance mechanism
depends on the timing of tuber initiation and bulking stages,
interactions with periodic water-deficit, CO2 levels, and phenology need to be investigated. Research has also shown that
irradiance level influences the degree to which CO2 enrichment enhances leaf gas exchange in potato with a proportionately larger increase in these responses observed at lower light
levels (Ku et al., 1977; Wheeler et al., 1991). Based on these
observations, we speculate that eCO2 would reduce effects of
short-term drought on potato gas exchange and agronomic
response, that this moderating effect would be more pronounced during drought occurring post tuber-initiation stage
than at a prior vegetative event, and the relative degree of this
reduction would be greater under lower irradiance levels.
Sunlit enclosures were used to study effects of CO2 and shortterm droughts, when applied at different developmental stages,

on potato under contrasting light environments. Specifically, the

goals were to (i) quantify transient changes in canopy photosynthesis, transpiration, and associated gas exchange parameters during drought events, (ii) evaluate the extent to which
short-term drought cycles during pre- and post- tuber initiation
stages influence long-term seasonal gas exchange responses
under different CO2 concentrations, and (iii) assess the relationship between water-stressed canopy gas exchange response and
resulting dry matter production. Findings will help improve
water management strategies and provide critical data for testing
mathematical crop models and decision support tools.
MATERIALS AND METHODS
Design
Experiments E1 and E2 were conducted at different dates
in a set of six Daylit Soil-Plant-Atmosphere Research (SPAR)
chambers at United States Department of Agriculture- Agricultural Research Service (USDA-ARS) facilities in Beltsville,
MD, in 2011. SPAR chambers were composed of Plexiglas1
(Evonik Industries, Essen, Germany) walls and ceilings transparent to sunlight. Each chamber enclosed a 1 m2 production
area with an air volume of 3360 L, and provided control over
CO2 , air temperature, and relative humidity. Air, canopy, and
soil temperatures, relative humidity, CO2 , and photosynthetically active radiation (PAR) data were logged every 30 s and
stored as 5-min averages. Canopy surface air temperature was
measured using an infrared digital thermometer maintained 5
cm above canopy height (Model Envirotherm 4000L, Everest
Interscience Inc., Tucson, AZ). Infrared gas analyzers (LI6262, LI-COR Biosciences, Lincoln, NE) measured CO2 in
each chamber and the desired set-point was met using mass
flow controllers (Omega Engineering Inc., Stanford, CT) and
pure CO2 (bone dry 99.8%) from a compressed gas cylinder.
More details can be found in Fleisher et al. (2009).
Experimental dates were 28 May to 10 August for a total
74 d in E1 and 11 August to 20 October for a total of 71
d in E2. As chambers were transparent to sunlight and
located outdoors, solar radiation varied between experiments and averaged 41.7 10.3 mol PAR m2 d1 in E1 and
29.3 15.0 mol m2 d1 in E2 (Table 1). All other cultural,
management, and environmental factors were identical. Cut,
sprouted seed tubers (S. tuberosum L. Kennebec) were planted
at 10-cm depths in 16-L pots, 12 per chamber, in a medium of
3:1 volume ratio of washed construction sand and vermiculite
(Grace Construction Products, Cambridge, MA). Osmocote
(141414 Osmocote, Scotts Company LLC, OH) was added
(1.5 g pot1) at planting. Other nutrients were supplied via
an automated, micro-fertigation mineral solution (Robinson,
1984) at least twice per day except during water-withholding
periods. Two uniform main-stems were maintained per pot
following emergence. Three SPAR chambers were set to daytime concentrations of 400 L L1 (aCO2) and an additional
3 to 800 L L1 (eCO2). Night-time CO2 ranged from 645 to
1108 L L1 over the course of the season, the variation due
to respiration arising from differences in biomass and the lack
of a CO2 venting or scrubbing system. A 16-h thermoperiod
1 Mention of a trademark or proprietary product does not constitute a
guarantee or warranty of the product by the USDA and does not imply the
exclusion of other available products.

Agronomy Journal Volume 106, Issue 6 2014

2025

Table 1. Timing of drought cycles in days after emergence (DAE), average daily light integral (PAR), and averaged day (Tday) and night (Tnight) air temperatures, and 24 h relative humidity (RH) across all treatments for experiments E1 and E2.
Event
Drought 1
Drought 2
Season

Dates
DAE
1127
4559
171

PAR
mol m2 d1
41.7 10.3
45.5 8.7
43.9 10.1

E1
Tday
Tnight
C
22.0 0.17 17.0 0.16
21.9 0.47 17.5 0.61
22.0 0.21 17.3 0.36

RH
%
76.7 0.52
69.9 3.89
73.4 2.35

Dates
DAE
1329
4152
174

E2
PAR
Tday
Tnight
RH
mol m2 d1 C
%
29.3 15.0 22.1 0.12 17.1 0.04 78.9 0.06
15.7 5.9
22.0 0.17 17.0 0.18 79.9 0.83
24.7 12.4 22.0 0.08 17.1 0.10 79.0 0.11

Photoperiod averaged 13 h in E1 and 12.5 h in E2.

with a 22/17C day/night temperature was maintained

(0.3C accuracy across all chambers) and average 24-h relative
humidity ranged between 62 and 78%.
An initial drought cycle was applied on a single pair of aCO2
and eCO2 chambers during vegetative growth (Table 1). A
second drought cycle was applied to these same previously
droughted pots and an additional unstressed CO2 pairing
approximately 10 d post tuber initiation (Table 1). The final
pair of growth chambers were maintained as the control.
Drought cycles were held for a period of at least 11 d before
re-watering, the duration varying between E1 and E2 so as to
ensure a similar degree of water stress as monitored by mid-day
leaf water potential (LWP). The LWP was determined from
leaf discs excised from mature terminal leaflets at mid-day
(12001400 h) using dew point hygrometry with insulated
C-52 sample chambers and an HR-33T microvoltmeter
(Wescor, Inc., Logan, UT). Measurements were taken every
2 d on three plants per chamber, starting from the onset of
each drought cycle. Partial harvests were conducted following
each drought cycle, with pots thinned to a single main-stem
following the first drought, and six pots removed from the
chambers following the second drought. At harvest, leaf area
was recorded separately for each pot using a leaf area meter (LI3100, LI-COR Biosciences, Inc., Lincoln, NE) and all organs
(leaf, stem, tubers, roots, stolons) were separated and dried in
an air-forced oven at 70C until constant mass. The following abbreviations were adopted: CO2- refers to CO2 treatments, eCO2 or aCO2; H2O- refers to irrigation treatments,
C- control, R-pots droughted only at post-tuber initiation, and
VR-pots droughted at vegetative growth and a second time at
post-tuber initiation.
Hourly volumetric water contents (VWC) were measured in
seven pots per chamber with time-domain reflectometry (TDR),
using 20-cm waveguides and Campbell Scientific (Logan, Utah)
multiplexors (Campbell SDMX50), TDR100 Time-Domain
Reflectometer, and a CR1000 datalogger. Site-specific calibration for VWC and apparent permittivity was conducted using
the same soil mixture and water contents from air-dry to saturation (Timlin et al., 2007). Average hourly VWC were computed
during non-irrigation times as a five-pot average after discarding
the highest and lowest values in each 24-h period. Daily water
uptake rates were estimated by (i) multiplying hourly average
VWC by the soil volume (14.1 L), (ii) obtaining the difference
between pre-dawn (0600 h) and early evening (2100 h) values,
and (iii) accounting for irrigation water minus free drainage
from each pot. Free drainage was calculated each day based on
the period of time, if any, for which VWC exceeded 35%, a value
corresponding to saturation of the soil media.
2026

Canopy Gas Exchange

Each SPAR chamber formed a semi-closed system for
measurement of CO2 and water vapor fluxes produced by the
enclosed potato plants. Whole plant CO2 exchange rate (CER,
mol CO2 m2 s1) was calculated at 30-s intervals based
on the amount of CO2 injected, leaked from the chamber,
and injected but not used by the plants. Leakage rates were
estimated using an N2O tracer gas system (Baker et al., 2004).
During the daytime, CER values measured for each SPAR
chamber represented whole plant net photosynthesis, A N.
Mean values for dark respiration, R D, were estimated for each
24-h period. Night-time R D was estimated between 0100 to
0400 h. To avoid possible effects inaccuracies using the Q10
approach (Heskel et al., 2013), daytime R D was obtained by
averaging CER values between 2000 to 2200 h when PAR was
zero but chamber temperatures were still maintained at the
daytime set-point. Gross photosynthesis, AG, was computed as:
AG = A N + R D 

[1]

where AG is the gross instantaneous photosynthetic rate, (mol

CO2 m2 s1), AN = net instantaneous photosynthetic rate,
(mol CO2 m2 s1), and R D = dark respiration rate (mol
CO2 m2 s1). Gas exchange data were averaged at 15-min
intervals and a rectangular hyperbola (Eq. [2] 2, Pachepsky et
al., 1996) was fit to the relationship between AG and incident
PAR for each day using the NLIN procedure in SAS software
(SAS Institute, 2009):

AG =

a I tC

aI +tC

[2]

where is canopy light utilization efficiency

(mol CO2 mol1 PAR), I is incident irradiance above the
canopy (mol m2 s1), C is growth CO2 concentration
(mol CO2 m3), and is canopy conductance to CO2 transfer
(m s1). While the estimates for R D do not directly compensate
for possible light inhibition of foliar respiration (Heskel et al.,
2013), a comparison of the end of season percent error between
carbon content in the plant dry mass vs. total AG R D was conducted and averaged <5% across all treatments.
Total canopy conductance to water vapor (G v) (which
includes boundary and canopy surface conductances, mol
H2O m2 s1) was approximated as an average value during the
daylight hours by solving for G v in Eq. [3] (Campbell and Norman, 1998) using the measured canopy temperature for TC and
daily water uptake for canopy evapotranspiration, ET:
Agronomy Journal Volume 106, Issue 6 2014

 eC (TC ) - ea

lET = Gv
pa

[3]

where is the latent heat of vaporization (43,500 J mol1),

ec(Tc) and ea are the vapor pressures at the canopy surface and
in the air, and pa is atmospheric pressure.
Statistical Analysis
To test for differences due to solar radiation levels between
experiments, dry matter data were initially modeled as a twofactor factorial design with experiment as a random block. The
likelihood ratio statistic (Littell et al., 1996) was used to determine if this block effect was significant for each dry matter
response. The SAS MIXED procedure (SAS Institute, 2009)
was used, with chamber as a random effect, for analysis of variance of dry matter (n = 6) and time-averaged gas exchange data
(n 11, depending on experiment and drought cycle as in Table
1) during each drought. Mean separations were conducted with
Fishers protected LSD ( = 0.05). For dry matter analyses,
individual pots were used as pseudo-replicates as per Fleisher et
al. (2009) and Reddy and Zhao (2005). Covariance analyses,
using average PAR during the given harvest stage, were also
used to test for commonality of responses to CO2 and H2O
treatment factors between the two experiments for dry matter
responses. Linear regression and contrasts were conducted
using SAS Proc MIXED to compare differences in all other gas

exchange responses vs. VWC between H2O and CO2 factors

as indicated in respective figures and tables.
RESULTS
Transient Responses During Drought Cycles
There were no differences among VWC or LWP vs. time
due to growth CO2 during the first drought cycle (Fig. 1). The
VWC dropped to below 10% for both CO2 treatments (9.8
0.8 and 9.8 3.7 for aCO2 and eCO2 , respectively) in E1, and
mid-day LWP reached minimums of 1.04 0.04 and 1.10
0.09 MPa for aCO2 and eCO2 . In E2, these values were 7.9
0.8 and 7.5 0.4% VWC and LWP of 1.35 0.06 and
1.57 0.19 at aCO2 and eCO2 . A similar lack of response
for CO2 was also observed for the second drought cycle.
Minimum VWC of R-treated plants in E1 were 6.3 0.40
and 6.0 0.44% for aCO2 and eCO2 and LWP was 1.5
0.11 and 1.56 0.17MPa, respectively. For VR-treated plants
VWC was 7.9 0.31 and 7.1 1.5% and LWP was 1.5
0.1 and 1.65 0.29 for aCO2 and eCO2 . In E2, minimum
VWC of R plants were 7.8 0.94 and 10.16 1.1% and LWP
was 1.3 0.19 and 1.46 0.21MPa. For VR-treated plants,
VWC were 11.1% for both CO2 treatments, and LWP 1.61
0.11 and 1.57 0.19 MPa for aCO2 and eCO2 . Thus, minimum LWP for both experiments during either drought cycle
was not influenced by CO2 or either H2O treatment; however,
VWC were slightly higher for VR as compared to R treatments
during this second drought.

Fig. 1. Average daily volumetric water contents (VWC, n = 7) and mid-day leaf water potentials (LWP, n = 3) vs. day after emergence during two
drought cycles for experiments (a, b) E1 and (c, d) E2 at (a, c) ambient CO2 (aCO2) and (b, d) elevated CO2 (eCO2). H2O symbols: circle-C (control),
inverted triangle-R (drought applied at post tuber-initiation stage), square-VR (drought applied at vegetative and post tuber-initiation stages). Open
symbols for VWC and closed symbols for LWP. Standard errors indicated.

Agronomy Journal Volume 106, Issue 6 2014

2027

Table 2. Decline in gas exchange parameters (canopy light use efficiency, canopy conductance to carbon dioxide transfer, Gv canopy conductance to water vapor), normalized with respect to ambient (aCO2) or elevated (eCO2) CO2 control chamber, vs. decreasing volumetric water content
(VWC) during drought cycles (DC) in experiment E1 and E2 for H2O treatments VR (droughted at vegetative and post tuber-initiation stages) and R
(droughted at post tuber-initiation stage). Slopes and standard error of the estimate are shown. Letters indicate significant differences within a given
CO2 treatment. Slopes that were significantly different between CO2 treatments indicated by * ( = 0.5) or ( = 0.1).

Experiment

DC

E1

1
2

E2

1
2

* Significant at = 0.05.
Significant at = 0.1.

H2O
treatment
VR
VR
R
VR
VR
R

aCO2

eCO2

aCO2

eCO2

aCO2

eCO2

%1
0.024 (0.005)* 0.045 (0.003)*
0.03 (0.008)*
0.055 (0.005)*
0.037 (0.005)*
0.058 (0.01)*
0.031 (0.007) 0.020 (0.003)
0.052 (0.009)*
0.030 (0.006)a*
0.021 (0.002)*
0.043 (0.007)*
0.035 (0.007)
0.022 (0.004)
0.047 (0.005)*
0.079 (0.006)b*
0.023 (0.002)*
0.056 (0.007)*
0.027 (0.006)
0.026 (0.004)
0.056 (0.02)
0.042 (0.005)
0.037 (0.005)
0.036 (0.003)
0.03 (0.008)
0.02 (0.002)
0.083 (0.03)
0.094 (0.02)a
0.047 (0.009)a
0.043 (0.003)
0.023 (0.005)
0.022 (0.002)
0.045 (0.013)
0.027 (0.004)b
0.026 (0.004)b* 0.044 (0.007)*

Fig. 2. Declines in (a) light use efficiency , (b) canopy conductance

to CO2 transfer , and (c) canopy conductance to water vapor Gv for
ambient CO2 (aCO2) treatments vs. volumetric water content (VWC)
during droughts 1 and 2. Responses were normalized with respect to
control (C) values on each measurement date before plotting. Absolute
values for C chambers during each drought indicated as circles
(standard errors are indicated). Experiment E2 results not shown for
conciseness (regression results summarized in Table 2).

2028

Gv

Relative decline VWC1

Fig. 3. Declines in (a) light use efficiency , (b) canopy conductance

to CO2 transfer , and (c) canopy conductance to water vapor Gv for
elevated CO2 (eCO2) treatments vs. volumetric water content (VWC)
during droughts 1 and 2. Responses were normalized with respect to
control (C) values on each measurement date before plotting. Absolute
values for C chambers during each drought indicated as circles
(standard errors are indicated). Experiment E2 results not shown for
conciseness (regression results summarized in Table 2).

Agronomy Journal Volume 106, Issue 6 2014

Table 3. Averaged gas exchange values (ANcanopy net photosynthesis; ETcanopy evapotranspiration rate; WUEcanopy water use efficiency;
canopy light use efficiency; canopy conductance to carbon dioxide transfer; Gv canopy conductance to water vapor) for drought cycles (DC) 1 and
2 for E1 (n = 15 and 13, respectively) and E2 (n = 15 and 10, respectively). H2O symbols: Cnon-water stressed control; Rtreatments droughted at
post tuber-initiation stage only; VRtreatments droughted at post tuber-initiation and vegetative growth. Least square differences (LSD) within each
CO2 grouping are provided. Letters indicate significant differences within a given CO2 treatment ( = 0.05) and * indicates differences across CO2
treatments for a given H2O grouping ( = 0.05).
Experiment DC
E1

H2O
treatment

E2

C
VR
LSD
C
R
VR
LSD
C
VR
LSD
C
R
VR
LSD

AN
aCO2

ET
eCO2

aCO2

WUE
eCO2

mol m2 d1
0.85a
0.85a
319a* 261a*
0.49b
0.46b
167b* 104b*
0.14
0.19
25
32
1.25a* 1.58a*
453a* 336a*
0.52b
0.73b
107b
81b
0.53b
0.66b
101b
69b
0.16
0.16
28
25
0.55a
0.76
480a* 410a*
0.27b* 0.54*
125b
106b
0.14
0.25
55
40
0.38
0.48a
312a* 335a*
0.29
0.20b
117b
118b
0.36
0.33a
121b
104b
0.14
0.15
33
28

aCO2

eCO2

mmol mol1
2.7*
3.6a*
2.9*
5.7b*
0.6
1.4
2.5a*
5.1a*
6.0b*
9.2b*
5.2b*
9.6b*
1.0
1.5
1.1a*
1.9a*
4.6b
7.2b
2.3
1.7
1.4a*
2.0a*
4.2b
3.5a
3.5b
6.4b
1.0
1.5

aCO2

eCO2

mol mol1 ( 10)

0.72a
0.71a
0.53b
0.46b
0.01
0.08
0.91a*
1.03a*
0.59b
0.56b
0.56b
0.57b
0.07
0.06
0.64*
0.93a*
0.57
0.62b
0.11
0.10
1.32a*
1.22a*
1.04b
0.96b
1.08b*
0.84b*
0.09
0.09

aCO2

Gv
eCO2

mm s1
4.29a* 2.84a*
2.21b* 1.12b*
0.50
0.60
5.41a* 4.45a*
2.42b
1.75b
2.22b
1.52b
0.64
0.47
4.43a
3.43a
2.58b
2.04b
1.3
0.90
7.55a* 5.01a*
4.85b* 2.45b*
5.33b* 2.56b*
1.06
0.63

aCO2

eCO2

mmol m2 s1
679a*
460a*
356b*
203b*
86
72
525a
471a
120b
125b
147b
121b
54
49
1203a* 717a*
300b
257b
234
109
1079a* 680a*
235b
305b
337b
231b
111
74

* Significant at = 0.05.

Canopy gas exchange responses for light use efficiency ()

and conductances for CO2 transfer () and water vapor (G v)
were normalized with respect to the C chambers during each
drought. Rates of decline with respect to VWC were summarized in Table 2 and Fig. 2 and 3. All eCO2 treatment responses
showed a sharper decline than aCO2 during the first drought
(responses were not significant in E2) (Table 2). During the
second drought, eCO2 treated plants showed higher rates of
decline in G v by a factor of at least two as compared to aCO2;
as with the first drought, these responses were not consistently
significant for E2. Trends in were opposite for VR and R pots
in E1 at the different CO2 levels but were not repeated in E2.
In general, there was no consistent effect of H2O treatment on
the rates of decline within a given CO2 treatment; however,
for eCO2 , appeared to decline differently with respect to the
H2O treatment in the two experiments.
Average Gas Exchange Values
during Drought Cycles
In both droughts and experiments, average AN was the same
or higher ET generally the same or lower, and thus, WUE statistically the same or higher for eCO2 grown pots across a given
H2O treatment (Table 3). This pattern was consistent with the
transient conductance responses (Table 2) in which (a) declines
in G v were generally higher for eCO2 pots and (b) declines
in were more rapid than Gv for aCO2 pots, but not eCO2 .
Average G v and were also consistently lower for eCO2 pots at
a given H2O level. Absolute differences among parameters were
not always significant across CO2 levels however, differences in
WUE for eCO2 vs. aCO2 were. As with the transient responses,
no consistent pattern for between CO2 levels was observed.
Values for H2O treatments R and VR declined with respect
to the control chamber C during each drought (Table 3).
The WUE increased between C and VR or R pots in both
experiments and droughts and this was largely due to a sharper
decline in G v than , leading to stronger suppression of ET

than AN. For example, averaged across CO2 and H2O, G v was
reduced 51 to 74% as a result of the droughts while declined
40 to 60%. Light use efficiency was negatively impacted by the
droughts, particularly in E1. In nearly all cases there was no
evidence to suggest that the gas exchange responses of twicedroughted VR pots were more or less sensitive to a second
drought post tuber-initiation period than the single-droughted
R pots. Thus, previously droughted plants did not exhibit any
additional drought tolerance mechanisms to the additional
drought cycle, at least when assessed at the canopy level during
the drought itself.
Seasonal Gas Exchange and
Dry Matter Production
These transient gas exchange responses were reflected in the
whole season responses (Table 4). Cumulative AN decreased
with increasing drought frequency with the pattern of C >
R > VR, although such differences were more substantial in E1
than E2. Similar to responses during the water withholding
periods, seasonal ET of droughted pots generally declined to
a greater extent than AN as compared to the C values, resulting in higher WUE over the course of the season (Table 4).
Some variation existed with VR WUE responses, likely due
to higher soil evaporation as a result of sparser canopy growth.
Treatments with eCO2 showed consistently higher AN than
aCO2 across both experiments with either lower, or similar E
values, thus resulting in higher WUE regardless of H2O treatment. Less than 14% error between end-of-season dry matter
and cumulative AN was observed in all treatments (Table 4,
Error column). These C balance results are typical in canopy
gas exchange studies (Van Iersel and Kang, 2002) and indicate
the observations of seasonal AN were compatible with total dry
matter production. Slopes from the regression of cumulative
AN on time served as an analogue for plant growth rate (Fig. 4),
and confirmed that decreased AN in the VR and R treatments
was due to the drought cycles (Table 5). For example, growth

Agronomy Journal Volume 106, Issue 6 2014

2029

Table 4. End-of-season (cumulative) canopy net photosynthesis (AN), evapotranspiration (ET), water use efficiency (WUE), dry matter, and percent
difference (error) between end-of-season dry matter production and AN. H2O symbols as defined in Table 3.
Experiment E1
CO2
aCO2

eCO2

Experiment E2

ET

WUE

Dry mass

Error

ET

WUE

Dry mass

mol CO2 m2

mol H2O m2

mmol mol1

mol CO2 m2

mol CO2 m2

mol H2O m2

mmol mol1

mol CO2 m2

64.9

24,348

2.67

75.4

13.9

41.4

20,971

1.97

40.4

2.6

R
VR

54.4
44.7

18,284
15,339

2.98
2.91

63.2
45.5

13.9
1.9

40.5
35.9

18,031
12,259

2.25
2.93

38.4
38.6

5.3
6.9

C
R
VR

90.4
77.5
40.9

20,580
16,825
11,762

4.39
4.61
3.48

92.2
82.1
46.4

2.1
5.6
11.8

53.6
57.6
35.0

22,028
18,457
11,019

2.43
3.12
3.18

55.4
52.8
39.6

3.2
9.0
11.7

H2O

AN

AN

Error
%

Includes all dry matter from partial and final harvests. Dry matter was converted to mol CO2 basis based on average tissue carbon content of 40% for purposes of C
balance comparison.

Table 5. The rate of increase in canopy AN (mol CO2 m 2 d 1) during drought cycles 1 and 2 as obtained from Fig. 3 (r 2 = 0.95 or higher for all regressions). H2O symbols as defined in Table 3. Standard errors of the estimate indicated in parentheses. Letters indicate significant differences ( = 0.05)
within a given CO2 treatment and * indicates differences across CO2 treatments for a given H2O grouping ( = 0.05).
Experiment E1
Cycle

Experiment E2

H 2O

aCO2

eCO2

aCO2

eCO2

Drought 1

C
VR

0.86 (0.04)a
0.58 (0.02)b*

0.79 (0.07)a
0.44 (0.03)b*

0.72 (0.07)a*
0.45 (0.03)b*

1.01 (0.09)a*
0.64 (0.04)b*

Drought 2

C
R
VR

1.19 (0.08)a*
0.59 (0.05)b*
0.69 (0.04)b*

1.78 (0.09)a*
0.71 (0.06)c*
0.88 (0.04)b*

0.58 (0.05)a*
0.60 (0.03)a
0.62 (0.02)a*

0.85 (0.07)a*
0.55 (0.04)b
0.54 (0.03)b*

* Significant at = 0.05.

Fig. 4. Cumulative canopy net assimilation (AN) for all H2O treatments vs. days after emergence for experiments (a, b) E1 and (c, d) E2 at (a, c) ambient
CO2 (aCO2) and (b, d) elevated CO2 (eCO2). Drought cycle timing and durations are indicated with shaded lines.

2030

Agronomy Journal Volume 106, Issue 6 2014

Table 6. Total and leaf dry matter, leaf area, and harvest index (HI) at final harvest for experiments E1 and E2 expressed on a per pot basis (n = 6).
Analysis of variance and least square differences (LSD) indicated. Symbols as defined in Table 3.
Experiment E1
CO2

H2O

aCO2

C
R
VR

LSD
C
R
VR

eCO2

LSD
CO2
H2O
CO2 H2O

Total

Leaf

g pot1
232a*
46.7
167b
46.2
126c
42.3*
28.3
19.4
273a*
194b
136c
42
*
***

63a
47a
27b*
11.7
ns
**
*

Area

Experiment E2
HI

Total

cm2 pot1
10,123a
7,163b
8,353a*
1,574

0.43a
0.39b
0.32b*
0.08

12,647a
8,063b
6,029b*
2,309
ns
***
*

0.47b
0.47b
0.60a*
0.13
**
ns
*

Leaf

g pot1
122*
33.1a
96*
22.1b*
101
29.4a*
25.5
7.3
143a*
152a*
105b
46.2
*
ns

34.2b
46.9a*
19.4c*
8.8
*
*
***

Area

HI

cm2 pot1
9,857a
6,417b*
9,127a*
1,429

0.20a
0.39b
0.51c
0.19

10,277a
10,666a*
4,599b*
2,822
ns
**
***

0.43a
0.50ab
0.61b
0.11
**
**
ns

* Significant at 5%.
** Significant at 1%.
*** Significant at 0.1%.
ns, nonsignificant.
Significant at 10%.

rates computed in this fashion ranged between 56 and 67% of

the corresponding C value of VR treatments during the first
drought cycle. For the second drought, VR pots which had
already been droughted during the first cycle exhibited higher
growth rates than those receiving their first drought period (R)
at either CO2 level. However, this pattern was only exhibited
in E1; in E2, rates were identical among VR or R treatments.
Growth rates during the droughts were generally higher in
eCO2 than aCO2 C chambers, but varied with VR and R treatments depending on experiment. Ultimately, as seasonal AN
was typically higher for eCO2 vs. aCO2 treatments at a given
C and R H2O levels, the growth rate responses during drought
cycles did not necessarily correlate with season long production.
On an individual pot basis (Table 6), total dry mass was larger
in E1 than E2, and significantly different for each H2O level
within a given CO2 level. In E2, such differences were smaller
and only growth at eCO2 exhibited clear differences between C
and R vs. VR means. Total dry matter production was significantly higher for eCO2 than aCO2 for C and R treatments, but
not VR (p < 0.05). However, harvest indices (HI) were higher
for VR eCO2 plants than aCO2 despite the similarity in total
dry matter produced, indicating that a higher proportion of
photosynthate was allocated to tuber organs than haulm. Leaf
dry matter and leaf area patterns were more inconsistent and
included a significant CO2 H2O interaction. Ambient CO2
VR treatments produced a higher amount of leaf area than their
eCO2 counterpart, a result suggesting that potato determinacy is
strongly influenced by both CO2 and plant water status, at least
for the variety evaluated in this study.
Effect of Radiative Environment
on Drought Response
During the second drought, average gas exchange parameters , , and G v were higher in E2 than E1 for most CO2 and
H2O treatments (Table 3). This pattern was consistent during
non-drought periods (not shown). A more efficient photosynthetic response to light as illustrated in Fig. 5 was the result
of the larger values of and Similar responses were observed

for other H2O treatments at either CO2 level each day of the
respective experiments. Comparison on a given day between
experiments is strongly influenced by differences in canopy
development (a result of the radiation differences in E1 and
E2), however leaf area, while generally smaller in E2 than E1,
was not proportionately reduced in response to the drought
treatments to the same extent as AN, total or leaf dry matter
production (Table 6). This was largely a result of differences in
specific leaf area for the plant canopies which averaged 17.9
1.63 m2 kg1 in E1 and 27.9 3.35 m2 kg1 in E2, indicating
leaves were substantially thinner in E2 as a result of acclimation
to the lower light environment. It should be further emphasized that such values are instantaneous rates. When photosynthetic data are integrated over the course of the day or season
(such as the data in Tables 3 and 4), substantial differences were
observed between E1 and E2 due to reduced daily and seasonal
radiation levels (Table 1). Changes in C allocation and leaf
thickness as a result of the different radiative environments
between E1 and E2 impacted the degree to which drought
results were manifested, particularly in terms of the extent to
which dry matter and seasonal AN were reduced with respect
to the control treatments (Table 4).
Although the per-pot dry matter data was evaluated separately in each experiment (Table 6), an analysis of covariance
was conducted separately using the pooled data set across E1
and E2, with mean daily PAR during each H2O treatment
period (Table 1) used as the concomitant variable. With the
exception of harvest index, PAR was found to have a significant
influence on all dry matter and leaf area responses (data not
shown). Analyzed in this way, total dry matter and tuber production were significantly impacted by H2O and CO2, while leaf
and leaf area production showed by H2O and interactive effects.
DISCUSSION
The effects of the short-term water-withholding cycles on dry
matter production, HI, AN, ET, and WUE at the two different
CO2 levels were analogous to those reported from a long-term
water-withholding study (Fleisher et al., 2008a). In that study,

Agronomy Journal Volume 106, Issue 6 2014

2031

Fig. 5. Comparison of light response curves for gross photosynthetic

rate for ambient CO2 (aCO2) treatments in experiments E1 and E2
from 8 d after onset of the second drought (DAE 54 in E1 and 51 in E2).
Lines show fit of Eq. [2] to measured PAR data with 95% confidence
limits indicated at an irradiance of 1300 mol m 2 s 1. Fluctuations are
a result of variations in CO2 concentration within each chamber. Note
the cut-off on the x axis for E2 reflects the maximum irradiance level
for that particular day as a result of cloud cover.

AN and WUE were consistently higher, and ET generally lower,

for eCO2 vs. aCO2 at all levels of water stress. At the more severe
levels of drought, differences in cumulative AN due to CO2 treatment were minimal; however, HI increased for eCO2 chambers,
similar in response to what was observed for the VR treatment in
the present study. In both studies, the most water-stressed plants
grown at eCO2 had less leaf area, but still maintained similar
AN rates, on a production area basis, as the corresponding aCO2
grown plants. The additional dry matter production for eCO2
treatments in both Fleisher et al. (2008a) and the present study
was allocated to tubers, rather than to aboveground biomass,
as observed by higher harvest indices (Table 6). Such results
suggest that similar findings from prior research conducted on
long-term water-stress responses may be applicable to the more
likely-to-occur short-term drought periods studied in the current
manuscript. Since these patterns were maintained in the different radiation environments between E1 and E2, it is likely that
the observed potato responses to eCO2 and water stress will be
transferable to different microclimates and types of water stress
during the growth season.
End-of-season cumulative AN patterns (Table 2), where C >
R > VR, indicated that even a single short-term exposure to
drought for 10 to 11 d was significant enough to reduce growth
of a 70 d potato crop. Because VR pots were water-stressed
at both vegetative and post tuber-initiation stages, definitive
conclusions regarding the degree of growth stage sensitivity
to drought cannot be reached via direct comparison with R
responses. However, analyses of transient response of , , and Gv
parameters (Table 2) and averaged gas exchange values (Table 3)
during the second drought suggest a lack of consistent difference between VR and R treatments. Most canopy gas exchange
values were statistically similar for VR and R chambers regardless of CO2 level or experiment. Thus, pots previously exposed
to drought at vegetative stage did not exhibit more tolerance to a
future drought cycle. Similarly, R treatments were not observed
to show higher tolerance, suggesting there was apparently no difference of drought timing on potato post-water stress recovery.
2032

The WUE increased during drought as a consequence of

conductances for H2O transfer being more strongly reduced
than . Such results were similar to other enclosure studies
reported by Vos and Groenwold (1989) and Dalla Costa et
al. (1997), but at aCO2 levels. In general, the rate of decline
in conductances with respect to control values was higher for
eCO2 during the drought, and average values were also consistently lower at each H2O treatment for eCO2 vs. aCO2 . Thus,
CO2 plays a role in drought tolerance via an increase in WUE;
however, in the current study, differences due to R or VR treatments within a CO2 grouping were not consistent.
Potato reportedly has a lower ability to maintain large differences between leaf and soil water potential as compared with
other agronomically important crops (Dalla Costa et al., 1997),
the result being reduced stomatal conductance, transpiration,
and photosynthesis at relatively high leaf water potentials (Vos
and Groenwold, 1989). It is likely that responses among AN,
G v, and other gas exchange properties will be strongly influenced by soil media composition and volume which influences
buffering capacity. This is an important consideration given
that the current study used 16-L pots with sandvermiculite
media that had small water holding capacity compared with
typical soils, and thus little buffering capacity to drought
(leaves were visually wilted within first day of water withholding). Drought reduced both conductances as well as , suggesting that the water-withholding cycles presented severe enough
water stress to influence both supply of substrate for photosynthesis as well as any underlying metabolic processes. Whether
photosynthetic rate during water withholding is decreased
solely as a result of conductance or non-stomatal effects appears
to be species dependent (e.g., Hsiao and Acevedo, 1974; Martin
and Ruiz-Torres, 1992). However, the degree of water-stress
may influence such results. In the present case, mid-day leaf
water potentials ranged from 1.5 to 1.65 MPa in VR and R
pots across both experiments and CO2 levels. These values were
larger in magnitude than those reported by other studies (a
range from 0.94 to 1.1 MPa) (Gandar and Tanner, 1976; Liu et
al., 2005; Moorby et al., 1975; Vos and Groenwold, 1988), indicating a high degree of water stress before re-watering occurred.
Increased specific leaf area was observed in shading and
low-light studies with potato (Bodlaender, 1963; Sale, 1973)
and is typically associated with higher light-use efficiency than
thicker leaves (Bodlaender, 1963). Evans and Poorter (2001)
indicated this is a property most likely related to variations in N
distribution in shaded leaves towards light capture as opposed
to maximizing photosynthetic production. If compared on an
equivalent light intensity basis, as in Fig. 4, the photosynthetic
rates of plants grown under lower irradiance did appear to be
more strongly influenced by eCO2 as reported by Ku et al.
(1977) and Wheeler et al. (1991) and less influenced by drought
stress. The reduced dry matter production was then directly
related to smaller daily light integrals in E2, despite higher
instantaneous rates (Fig. 4). Averaged volumetric water contents
during the droughts also varied among E1 and E2. For example,
during the second drought, across CO2 levels, water contents
averaged 11.7% 0.1 for R and 12.4% 0.9 for VR pots in E1
vs. 14.7 1.3 and 18.3 1.6% in E2 (well-watered VWC of pots
in E2 were approximately 4% higher than in E1). While general
responses to drought were similar between E1 and E2, more
Agronomy Journal Volume 106, Issue 6 2014

differentiation among H2O treatments may have been observed

in E2 had these average VWC values been more similar.
Results from these experiments indicated that the number of
water-withholding cycles has a larger effect on canopy photosynthetic rate and gas exchange properties than the timing of
such events during the season. Even short-term water withholding cycles, when experienced pre- or post-tuber initiation rate,
resulted in significant loss of carbon for both eCO2 and aCO2
grown potato. The decline in carbon assimilation was attributed to both reduction in and G v, but also , which indicates
an effect not just on photosynthetic substrate availability due
to stomatal closure, but on photosynthetic metabolism. Transient reductions in gas exchange data during drought suggest
that conductance values decline more rapidly than AN at either
CO2 level, resulting in higher WUE. Seasonal and diurnal
rates of AN were higher and ET generally lower for eCO2 pots.
Twice-droughted VR treatments exhibited similar growth rates
regardless of CO2 concentration; however, HI increased for
eCO2 . While absolute values in response to the droughts were
different in E2 than in E1 as a result of the radiative environment, similar relative responses were reported. We expect that
the reported results in the present manuscript are likely to be
conserved among future drought studies of varying length with
potato under eCO2, as the short-term results for seasonal and
daily gas exchange values were similar to those reported for
potato grown under eCO2 with long-term water withholding
studies. It is difficult to extrapolate results from the present
study to all future climatic scenarios as the present data was
obtained from chambers in which air temperatures were maintained at optimal levels for potato growth. However, the data
demonstrates that future atmospheric CO2 concentrations will
help mediate effects of limited water availability on potato as
compared with production under historical CO2 levels.
CONCLUSIONS
Potato plants were grown under elevated (eCO2) or ambient
(aCO2) carbon dioxide levels and exposed to three different
short-term drought treatments: no-stress, drought stress at post
tuber-initiation stage, and drought at both vegetative and post
tuber-initiation stages. Two experiments were conducted at
low and high solar radiation and measurements of canopy net
photosynthesis (AN), transpiration rates (ET), conductance to
CO2 and water vapor, and light use efficiency were used, along
with dry matter data, to assess the combination of eCO2 and
short-term drought. As has been observed for season-long water
withholding studies, growth under eCO2 generally resulted in
higher AN, decreased ET, higher water use efficiency, and higher
harvest index. There were no consistent differences in the degree
of canopy gas exchange responses during the droughts at either
CO2 level with respect to the timing of the drought and potato
developmental stage. Results were consistent between the low
vs. high solar radiation environment; however, significance of
responses was greater under the more intense radiation condition. These findings suggest interactions between CO2 and
drought on potato water use and C assimilation rate are likely to
be conserved across different radiation and rainfall production
zones. The data also indicate, if all other factors were to be held
equal, that future atmospheric CO2 concentrations are likely to
help reduce the severity of water deficits on potato production.

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Agronomy Journal Volume 106, Issue 6 2014