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Agriculture, Ecosystems and Environment 112 (2006) 4957

www.elsevier.com/locate/agee

Response of potato (Solanum tuberosum L.) to elevated


atmospheric CO2 in the North American Subarctic
Jeffery S. Conn *, Verlan L. Cochran
USDA-ARS, 360 ONeil Bldg., University of Alaska, Fairbanks, Alaska, 99775 and 501 L. West Road, Palouse, WA 99161, USA
Received 2 March 2004; received in revised form 14 July 2005; accepted 21 July 2005
Available online 19 September 2005

Abstract
The response of potato (Solanum tuberosum L., cv. Shepody) to elevated CO2 was studied in 1994 at Fairbanks, Alaska using open-top
chambers (OTC). Three CO2 exposure levels were used in OTC: ambient (A); A + 175 mmol mol1 CO2 (A + 175); A + 350 mmol mol1
CO2 (A + 350). Plots were also established outside chambers (ANC) to test chamber affects. Potato leaf appearance rate and canopy
development did not differ between CO2 treatments. Six plants in each plot were harvested in late July and August. At the first harvest, the
number of stems, total stem weight, number of flowers, and total flower dry weight decreased with increasing CO2. Biomass allocated to stems
and leaves declined while allocation to tubers increased with elevated CO2. Root:shoot ratio was larger and percent leaf nitrogen declined
12.6% with increased CO2. At the final harvest, total tuber dry weight in A + 350 chambers was 36% higher than in the A treatment, but yields
in open-top chamber plots were lower than the no-chamber plots possibly due to 714% less photosynthetic active radiation in chambers. Net
photosynthesis measurements made on July 13 showed no differences due to CO2 treatment; however, on August 5, net photosynthesis of
leaves grown at A + 350 was 53% greater than at ambient CO2. Tuber initiation and growth began between the two photosynthesis
measurements. Before tuber initiation, photosynthetic rates may have been down-regulated by insufficient carbon sink capacity.
# 2005 Elsevier B.V. All rights reserved.
Keywords: Carbon dioxide; Atmospheric CO2; Potato; Yield; Photosynthesis; Open-top chambers; Subarctic

1. Introduction
Kimball (1983) compiled data from 430 studies with
various crop species grown under ambient and 2X ambient
CO2 levels and found that yields at 2X CO2 were increased
on average by 32% over ambient. However, lack of response
to elevated atmospheric CO2 or apparent acclimation has
been noted in a number of studies. Such lack of response
may be an artifact of experimental design such as
insufficient rooting volume in pots, which may restrict
the carbon storage capacity of roots (Berntson et al., 1993;
Conn et al., 1994). In addition, low nutrient availability may
decrease the capacity to accumulate additional carbon
under elevated CO2 conditions (Goudriaan and Ajtay, 1979;
Jarvis, 1989; Kramer, 1981; Oechel and Strain, 1985;
* Corresponding author. Tel.: +1 907 474 7652; fax: +1 907 474 6521.
E-mail address: ffjsc1@uaf.edu (J.S. Conn).
0167-8809/$ see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.agee.2005.07.010

Shaver et al., 1992; Stitt and Krapp, 1999). Several


mechanisms have been proposed to account for true
physiological adjustment to elevated CO2 (Drake et al.,
1997) including: (1) end product inhibition (Madsen, 1968);
(2) reduced nutrient acquisition relative to CO2-stimulated
growth (Herold, 1980; Adamsen et al., 2005); and (3)
reduced RUBP activity, regeneration, or concentration in
elevated CO2 environments (Wong, 1979).
Temperature is another important factor influencing plant
response to CO2. The response of photosynthesis is
temperature dependent (Pearcy and Bjorkman, 1983) largely
due to the temperature dependent specificity of Rubisco for
CO2 (Jordan and Ogren, 1984). Cure (1985) reviewed
studies of CO2 response in crops at various temperatures and
found that under elevated atmospheric CO2, growth
increased more at high than at low temperatures. Idso
et al. (1987) studied CO2 response in several crops at
different mean daily temperatures and showed that below

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J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

18.5 8C, increased CO2 decreased crop yields. Morison and


Lawlor (1999) reviewed CO2 X temperature interactions for
106 experiments and could find no clear pattern of how
plants respond to CO2 at low temperatures. Some species
were able to respond to increased CO2 at temperatures below
18 8C and some were not.
The potato (Solanum tuberosum L.) is well adapted to the
cool growing season of Alaska and is the most economically
important field crop (Benz et al., 2002). Potatoes have a large
carbohydrate sink in the form of tubers and exhibit apoplastic
phloem loading of sucrose which predisposes the species to
large increases in yield with elevated CO2 (Farrar and
Williams, 1991; Miglietta et al., 1998; Schapendonk et al.,
2000; De Temmerman et al., 2002a). Experiments performed
in growth chambers (Goudriaan and de Ruiter, 1983; Wheeler
et al., 1991; Stutte et al., 1996) and in the field (Miglietta et al.,
1998; Sicher and Bunce, 1999; Schapendonk et al., 2000;
Craigon et al., 2002) have generally shown that potato tuber
yields increase with elevated CO2. At ambient CO2 levels,
marketable tuber yields increased at higher latitudes in
association with lower temperatures and longer day-lengths
(De Temmerman et al., 2002b).
The objective of this research was to determine the
pattern of response of potato to increased atmospheric CO2
under the cool air temperatures and long day length typical
of summer at Fairbanks, Alaska (latitude 648490 N) at the
northern limit of commercial agriculture in North America.
Specific objectives were to determine: (1) if potato would
exhibit signs of CO2 acclimation; (2) whether CO2 would
change potato phenology, growth, nitrogen content, and
biomass allocation; and (3) if tuber yields and quality would
be enhanced by increased CO2.

2. Materials and methods


2.1. Chamber design and CO2 delivery/monitoring
An open-top chamber system (OTC) similar to that
described by Rogers et al. (1983) and Allen et al. (1992) was
used. The chambers were 3 m diameter 2.8 m high with a
2.2-m diameter frustum. The chambers were constructed of
structural aluminum and were covered by an 8 mil clear
PVC plastic film (Livingston Coating Corp, Charlotte, NC).
The bottom panel was double walled, with the inside wall
perforated with 2.5 cm diameter holes to distribute air
uniformly to the chamber. Air was supplied with a 600 W
propeller fan in a plenum box with a particulate filter.
Carbon dioxide was injected ahead of the fan to ensure
uniform mixing.
Liquid CO2 from a 23.6 metric T receiver was vaporized,
heated, and pressure reduced to 206 kPa through the use of
two regulators. The CO2 then passed through an electric
solenoid, which acted to turn off CO2 flow in case of a power
outage, and into an aluminum dispensing manifold. Separate
flow meters were used to regulate flow to each individual

chamber. Carbon dioxide was delivered to chambers through


0.58-cm Impolene lines and levels were adjusted manually
between 08:0009:00 h and 16:0017:00 h each day based
on CO2 measurements.
The CO2 concentration in each chamber was monitored
using the system described by Rogers et al. (1983) with a few
modifications. Air samples were constantly drawn from the
chambers through 0.64-cm Impolene lines into 3-way 24VDC stainless steel solenoid valves and then into an
aluminum exhaust manifold. A metal bellows pump
supplied vacuum to the solenoid bank and flows were
adjusted to 5.0 L/min using a flow meter and adjustment
valve in each sample line. A Campbell Scientific SDMCD16 Control Port Expansion Module with Drivers
programmed and run with a Campbell Scientific 21-X data
logger activated the solenoids sequentially for 2 min each
using a Li-Cor LI-6262 CO2/H2O analyzer. Carbon dioxide
levels were monitored from each line from 08:00 to 09:00 h
and from 16:00 to 17:00 h each day by manually stepping
through the solenoids. The concentration of CO2 in each
chamber was hand recorded prior to adjusting flows to
achieve the desired target CO2 levels in each chamber. On
July 25, an automatic data acquisition system was installed
to sample each line for 2 min each hour of the day and record
CO2 levels with a Campbell Scientific 21X data logger. The
first 30 s of each 2-min monitoring interval were not
recorded to allow purging of air from the previous chamber.
2.2. Study area and experiment design
The experiment was conducted at the University of
Alaska Agriculture and Forestry Experiment Station in
Fairbanks, AK (latitude 640 4900 N, longitude 1470 5200 W,
elevation 145 m) where the mean annual temperature is
3.5 8C, and the mean annual precipitation is 28 cm. The
soil was a Tanana silt loam (non-acid loamy, mixed Pergelic
Cryaquept) with a pH of 5.7 and 4.7% organic matter. The
experiment employed a randomized complete block design
with four treatments: ambient CO2 with no chamber (ANC),
ambient CO2 with chamber (A); ambient + 175 mmol mol1
CO2 in chamber (A + 175); ambient + 350 mmol mol1 CO2
in chamber (A + 350). There were four blocks. The
chambers were centered 10.7 m apart within each block.
The plot area, which had been fallow the previous year,
was disked twice and then Shepody potatoes (a popular
variety in Alaska) were planted on May 19, 1994 using a
single row potato planter that also banded fertilizer with
the potato seed pieces (290 kg ha1 N, 63 kg ha1 P,
122 kg ha1 K). Seed pieces were planted 28-cm apart in
rows that were spaced 76-cm apart. Metribuzin [4-amino-6(1,1-dimethyl)3-(methylethlthio)-1,2,4-triazin-5(4H)-one]
was broadcast applied at 1.13 kg ha1 on June 2 to control
weeds. The plot area was irrigated with a drip irrigation
system with emitter lines in alternating rows. Irrigation
scheduling was based on tensiometer measurements made in
each chamber. Chambers were installed on June 10 as the

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

plants were emerging and CO2 was introduced into the


appropriate chambers beginning June 11.
2.3. Chamber performance
Thermocouples to measure air temperature were installed
just above the canopy in each chamber and in each ANC
plot. Soil temperature at 1, 5, and 10 cm depth was also
measured using thermocouples in each plot. Soil temperature at 20, 50, and 100 cm depths were measured for ANC, A
and A + 350 plots. Li-Cor LI-1905A Quantum Light Sensors
and relative humidity sensors were placed in two ANC and
two A + 350 plots and were averaged and recorded hourly
with a Campbell Scientific CR-7 data logger.
Tensiometers were installed at 30 and 45 cm depth. They
were read every 36 days to schedule irrigation and to test
for differences in soil moisture among treatments.

51

Canopy temperature was measured on July 26, August 4,


and 9 using an Everest Infrared Thermometer. Three
readings were taken in each chamber and ANC plot with the
thermometer held 20 cm above and at a 458 angle to the
canopy.
2.4.4. First harvest
On July 2829, six plants were harvested from each OTC
and ANC plot and were separated into stems, leaves, and
flowers. The number of stems, leaves, flowers, number of
leaves above flowers, and internode lengths was determined.
Leaf area was measured with a Li-Cor leaf area meter. Plant
parts were dried at 40 8C, until constant weight was reached.
The weight of roots (those remaining with the plant when
pulled), stolons, and tubers was also determined. Nitrogen
and carbon contents were determined from ground samples
of leaves, stems, and roots using a Leco CNS-2000 carbonnitrogen analyzer.

2.4. Plant measurements


2.4.1. Leaf gas exchange
A Li-Cor LI-6200 Portable Photosynthesis System in a
closed configuration was used to measure gas exchange on
new fully expanded potato leaves on July 13 and August 5.
All measurements of elevated CO2 treatments were
conducted inside the closed chamber. Leaves were measured
in the A and A + 350 treatments on July 13, and for all
treatments on August 5. Three trifoliate leaves were
measured in each of four replicates of each treatment.
Three gas exchange runs were made for each leaf using a
0.25-L cuvette; these readings were averaged. Light PPFD at
the time of gas exchange measurements (12:0015:00 h) on
July 13 ranged from 1200 to 1600 mmol m2 s1 and from
1000 to 1400 mmol m2 s1 on August 5. Leaves that had
been used for gas exchange measurements were harvested
after all measurements were completed. Leaf area was
determined using a Li-Cor leaf area meter. Gas exchange
measurements were calculated on a leaf area basis.
2.4.2. Plant phenology and growth
Plant height, width and number of leaves were
determined every 7 days on the same four plants in each
chamber and ANC plot.
2.4.3. Canopy light and temperature
Measurements of photosynthetic photon flux density
(PPFD) were made within 2 h of solar noon on July 6, 12, 22,
26 and August 4 and 9 in each plot using a Li-Cor LI-1915A
Quantum Line Sensor. Light under the canopy was measured
by averaging two measurements at ground level in an x
pattern. Two readings were also obtained for above-canopy
PPFD and for canopy reflected PPFD by turning the sensor
upside down at 0.5 m height above the canopy. Percent
PPFD intercepted by the plant canopy was calculated by:
[(Above Canopy PPFD  Below Canopy PPFD)/Above
Canopy PPFD]  100.

2.4.5. Final harvest and yield


Eight plants were harvested from each plot the day
following the first killing frost (2.2 8C) on August 23 and
tubers were dug by hand for each plant in each plot. Potatoes
were graded as number 1 (4.88.9 cm without cracks or
deformity), small (<4.8 cm), large (>8.9 cm), knobby,
cracked, or dumbbell-shaped. Because the root system was
senescing and brittle, roots and stolons were not collected
during the final harvest. The above-ground portion of the
plants was dried at 40 8C and weighed when constant weight
had been reached. Tissue carbon and nitrogen measurements
were then made as above.
2.4.6. Tuber chemistry
Tubers from each plot were analyzed for sucrose and
glucose content by the USDA-ARS Red River Valley Potato
Research Lab. An YSI Model 27 Analyzer was used
following the methods of Sowokinos and Preston (1988).
2.4.7. Statistical analysis
Data were analyzed as a randomized complete block
design (four blocks) with four CO2-chamber treatments
within each block. The GLM procedure of the Statistical
Analysis System (SAS) was used for data analysis. A
separate ANOVA was performed using GLM to determine
the effect of CO2 on tuber yield (WW) using only the
chamber treatments.

3. Results
3.1. Chamber performance
Average daily air and soil temperatures were not
significantly different (ANOVA, p > 0.05) between ANC
and OTC plots. The average daily air temperature measured
above the canopy for all plots between June 11 (when

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J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

Table 1
CO2 concentrations measured in ambient and elevated CO2 chambers
CO2 measurement
Mean of 08:0009:00 h and
16:0017:00 h measurements
(6/118/23)
Mean daily (7/258/23)

were 7 mmol mol1 and A + 350 chambers were 40 mmol


mol1 below target values (Table 1).

CO2 treatmenta (mmol mol1)


A

A + 175

A + 350

369  25

543  25

707  51

407  64

570  61

717  91

Values are means plus or minus one standard deviation.


a
A = OTC, ambient CO2; A + 175 = OTC, ambient + 175 mmol mol1
CO2; A + 350 = OTC, ambient + 350 mmol mol1 CO2.

potatoes emerged) and August 23 (final harvest) was 18.3 8C.


Average soil temperatures over the same time period were:
18.8, 17.5, 16.9, 16.4, 14.6, and 11.9 8C for 1, 5, 10, 20, 50,
and 100 cm depths, respectively. The average daily relative
humidity was only slightly higher (t-test, p < 0.05) in OTC
than in the ANC plots (71.2% versus 68.5% RH, respectively)
which, given the lack of a thermal difference, shows that the
air flow through the chambers was nearly correct. If air flows
are too high, water stress may result (Leadley and Drake,
1993). No statistical difference in soil moisture (measured by
tensiometers) was found between treatments.
The average PPFD received from 10:00 to 22:00 h over
June 11 to August 23 was 7% lower in OTC than in ANC plots
(774 mmol m2 s1 versus 833 mmol m2 s1, respectively).
Line quantum sensor readings of PPFD at the canopy
surface were 13.9% lower (ANOVA, p < 0.0001) in OTCs
(1097 mM m2 s1) versus ANC plots (1273 mmol m2 s1).
1). There was no significant difference in canopy PPFD
levels between OTC treatments.
The average ambient CO2 concentration measured at
08:0009:00 h and 16:0017:00 h was 369 mmol mol1. CO2
concentrations in elevated CO2 chambers prior to adjustment
averaged 4 mmol mol1 higher than the target level for the
A + 175 chambers and 12 mmol mol1 lower than the target
value for A + 350 chambers. When CO2 concentrations were
measured over 24 h (July 25August 23), the ambient CO2
concentration was 407 mmol mol1, which reflects the
atmospheric CO2 rise that occurs when light levels decrease
and plants become net emitters of CO2, and A + 175 chambers

3.2. Plant measurements


3.2.1. Leaf gas exchange
On July 13, leaf internal CO2 concentrations were higher
and stomatal conductance was lower in plants growing in the
A+350 plots than in the A plots, but there was no difference in
net photosynthesis between ambient and elevated CO2 plants.
On August 5, the same results were found with leaf
intercellular CO2 and stomatal conductance but net photosynthesis was significantly (ANOVA, p < 0.05) greater for
plants growing at elevated than at ambient CO2 (Table 2). The
net photosynthesis rate on August 5 was 53% greater in leaves
grown at A + 350 than at ambient CO2 levels in chambers.
3.2.2. Plant phenology and growth
There were no differences in number of leaves, height or
width of plants attributable to treatments on any of the
sampling dates (ANOVA, p > 0.05). Plant development
progressed at similar rates under ambient and elevated CO2,
and both in and out of the chambers. The general appearance
of the plants was similar among all treatments.
3.2.3. Canopy light interception and temperature
There was no difference between treatments in the
percent of PPFD intercepted or reflected by the potato
canopy and measured by the Line Quantum Sensor on any of
the sampling dates also suggesting similar development of
canopies in all treatments. Despite the decrease in stomatal
conductance and resulting transpiration that would have
occurred at elevated CO2, there were no significant
differences in canopy temperatures between treatments
on any of the days canopy temperature was measured.
3.2.4. First harvest
The four treatments (ANC, A, A + 175, A + 350) had a
significant effect (Table 3) on number of stems, stem dry
weight (DW), number of flowers, flower DW, and shoot DW
(ANOVA, p < 0.05). Treatments had below ground effects on

Table 2
Effects of CO2 treatments on potato gas exchange on July 13 and August 5 at Fairbanks, AK
Sampling date

Treatmenta

Photosynthesis
rate (mmol m2 s1)

Stomatal conductance
(m2 s1)

Internal CO2 concentration


(mmol L1)

July 13, 1994

ANC
A + 350

22.1 a
22.5 a

0.31 b
0.12 a

130.2 a
321.3 b

August 5, 1994

ANC
A
A + 175
A + 350

17.4
15.4
19.7
23.6

0.49
0.34
0.24
0.26

249.6
242.7
368.2
492.3

ab
a
b
c

c
b
a
a

a
a
b
c

Means in a column within a date that are followed by different letters are significantly different (t-test, p < 0.05 for July 13; ANOVA, p < 0.05 and Duncans
MRT for August 5).
a
ANC = ambient CO2, no chamber; A = OTC, ambient CO2; A + 175 = OTC, ambient + 175 mmol mol1 CO2; A + 350 = OTC, ambient + 350 mmol mol1
CO2.

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957
Table 3
First harvest ANOVA results
Variable

Treatment

r2

**

NS

NS

0.83
0.38
0.80
0.40
0.31
0.54
0.34
0.75
0.72
0.83
0.72
0.28
0.73

Block

Number of stems
Number of leaves (NL)
Number of flowers
Leaf area (LA)
Total leaf DW (LDW)
Specific leaf DW = LDW/LA
Average leaf DW = LDW/NL
Leaf % N
Total Stem DW (SDW)
Stem % N
Total flower DW (FDW)
Flower % N
Total shoot DW
(SHDW) = SDW + LDW + FDW
Number of tubers (NT)

**

NS
NS
NS
NS
NS
NS

NS
NS
NS
NS

**

NS

*
*

NS
NS

NS

NS

53

percent solid content increased with increasing CO2 content.


The root:shoot ratio was higher at elevated CO2 levels. This
was also reflected in biomass allocated to tubers. Plants in the
A + 350 chambers allocated 54.5% of biomass to tubers
versus 37.4% that was allocated to tubers in the A treatment.
Potato plants grown at elevated CO2 allocated less biomass to
leaves and stems than did plants grown under ambient CO2
(Table 5).
The treatments (ANC, A, A + 175, A + 350) did not
significantly effect the percent N or C in roots, stems, shoots
or tubers (Table 3). However, percent N was 12.6% lower in
leaves from A + 350 plots than in the A plots (4.92% N
versus 5.54% N, respectively).
3.2.5. Final harvest
At final harvest there was no difference in shoot DW
attributable to chambers or CO2 (Table 6). Despite the
increased allocation of biomass below ground found in the
first harvest for plants in the above-ambient CO2 treatments,
final total tuber wet weight (WW) or WW of number 1
potatoes for the above ambient CO2 treatments did not differ
significantly from the ANC treatment (Table 7). However,
when only the chamber treatments were included in the
ANOVA, there was a highly significant positive relationship
between CO2 level and total tuber WW ( p < 0.01). Linear
regression was used to fit the data yielding:

0.64

NS = not significant at p = 0.05.


*
Statistically significant at p < 0.05.
**
Statistically significant at p < 0.01.

stolon DW and the percent solid content of tubers but had no


effect on total root or tuber weight. The treatments also
significantly influenced biomass allocation of DW to plant
parts and the root:shoot ratio (Table 3). Potato plants grown at
the A + 350 treatment had significantly fewer stems and lower
stem DW than plants in the ambient chamber (A) treatment
(Table 4). There was a decrease in the number of flowers and
flower DW with increasing CO2 in the chambers, but the
elevated CO2 chamber treatments did not differ from the ANC
treatment. Total stolon DW was significantly higher in A and
A + 175 plots than in ANC or A + 350 plots (Table 4). Tuber

Total tuber WW
19:92 mmol mol1 CO2 above ambient 11685;
p < 0:001;

r 2 0:999:

Table 4
Effects of CO2 and chambers on potato at first harvest
Treatmenta

Leaf N
(%)

Stems
(number)

Flowers
(number)

Stem DW
(g)

Flower DW
(g)

Shoot DW
(g)

Stolon DW
(g)

ANC
A
A + 175
A + 350

5.35
5.54
5.11
4.92

2.5
2.8
2.3
2.0

64
95
65
49

311
396
252
247

33.1
45.4
27.7
17.7

1468
1727
1262
1328

15.3
18.7
17.2
12.4

ab
a
bc
c

ab
a
bc
c

b
a
b
b

b
a
c
c

ab
a
ab
b

ab
a
b
b

ab
a
a
b

Data are expressed on a per plant basis. Numbers in a column that are followed by different letters are significantly different as determined by Duncans multiple
range test ( p < 0.05).
a
ANC = ambient CO2, no chamber; A = OTC, ambient CO2; A + 175 = OTC, ambient + 175 mmol mol1 CO2; A + 350 = OTC, ambient +
350 mmol mol1 CO2.

Table 5
First harvest effects of CO2 on potato tuber gravity, root:shoot ratio, and biomass allocation
Treatmenta Tuber percent solids (%)Root:shoot ratioRoot allocation (%)Leaf allocation (%)Stem allocation (%)Flower allocation (%)Tuber allocation (%)
ANC
A
A + 175
A + 350

13.9
14.7
16.0
16.7

a
ab
bc
c

0.63
0.73
1.13
1.35

a
a
b
b

4.4
4.4
3.9
2.9

a
a
a
a

47.4
43.2
36.9
34.2

a
a
b
b

13.4 a
13.4 a
9.5 b
8.0 b

1.6
1.6
1.2
0.6

a
a
a
a

33.4
37.4
48.6
54.5

a
a
b
b

Numbers in a column that are followed by different letters are significantly different as determined by Duncans multiple range test ( p < 0.05).
a
ANC = ambient CO2, no chamber; A = OTC, ambient CO2; A + 175 = OTC, ambient + 175 mmol mol1 CO2; A + 350 = OTC, ambient +
350 mmol mol1 CO2.

54

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

Table 6
Second harvest ANOVA results
Variable

Block

Treatment

r2

Shoot DW
Shoot % N
Total tuber WW
Number 1 tuber WW
Knobby tuber WW
Cracked tuber WW
Tuber percent Solids
Total tuber DW
Tuber % N
Tuber sucrose
Tuber glucose

NS
NS
NS
NS
NS
NS
NS
NS
NS

NS
NS
NS
NS
NS
NS
NS
ND
NS

**

**

**

**

0.64
0.69
0.56
0.42
0.57
0.40
0.47
0.56
0.65
0.87
0.87

NS = not significant at p = 0.05.


**
Statistically significant at p < 0.01.

3.2.6. Tuber chemistry


There was a significant effect of treatments on tuber
sucrose and glucose content (Table 7). Tuber sucrose and
glucose contents were lower from plants that had been
grown in chambers than outside. Tuber percent N did not
change with increasing CO2.
4. Discussion
Gas exchange measurements made at Fairbanks showed
that potato leaves growing at elevated CO2 exhibited the
typical responses of increased internal CO2 and decreased
conductance found by Ku et al. (1977) and Sicher and Bunce
(1999) for potatoes and for many other plants (Lawlor and
Mitchell, 1991; Drake et al., 1997; Vandermeiren et al.,
2002). A striking difference to other studies is that elevated
CO2 did not result in an increase in net photosynthesis early
in the growing season. Field studies by Sicher and Bunce
(1999) in Maryland (latitude 39820 N), Donnelly et al. (2001)
and Lawson et al. (2001) at Sutton Bonington, UK (latitude
528450 N); Schapendonk et al. (2000) at Wageningen, the
Netherlands (latitude 518580 N) and by Vandermeiren et al.
(2002) for a range of sites in Europe, all showed initial
increases in photosynthetic rates, followed by photosynthetic down regulation in response to increased CO2. A
possible explanation for the initial lack of photosynthetic

response to elevated CO2 at Fairbanks was that photosynthesis was limited by end product feedback inhibition (Guinn
and Mauney, 1980) induced by long days and low total
respiratory losses during short nights (<4.0 h). Extra starch
that accumulates in chloroplasts of leaves at high CO2
during the day is normally exported and used for dark
respiration at night (Ho, 1977; Kolbe and StephanBeckmann, 1997). In addition, since tuber initiation and
growth was not nearly as advanced on July 13 as on August
5, an adequate sink for starch transport may not have been
available. The longer night on August 5 (6.2 h) coupled with
a very strong sink in tubers for photosynthate could have
kept starch from accumulating in chloroplasts and downregulating photosynthesis. Studies by Stutte et al. (1996) add
support to this hypothesis. Norland potato net assimilation
rates were highest under a 12 h/12 h day/night photoperiod
and progressively decreased when plants were grown at 18 h
day/6 h night and 24 h light photoperiods. Moreover, leaf
starch levels increased when the dark period was decreased
to less than 12 h. Starch accumulation in potato leaves under
elevated CO2 was also observed by Goudriaan and de Ruiter
(1983), Sicher and Bunce (1999) and Schapendonk et al.
(2000).
An alternate explanation for the photosynthetic downregulation found in this study and in others is that the
response to elevated CO2 was limited by nitrogen supply.
Stitt and Krapp (1999) reviewed numerous experiments that
examined the interaction between N and response of plants
to elevated CO2 and found that photosynthetic downregulation was especially marked when nitrogen supply was
low. Adamsen et al. (2005) showed that when wheat
(Triticum aestivum L.) was grown at elevated CO2 as much
as 40% more mineral N was removed from the top 0.3 m of
soil than when grown at ambient CO2. At Fairbanks, while
first harvest foliar N was reduced 12.6% at the highest CO2
level (A + 350) compared to ambient CO2 chambers, there
were no significant effects of CO2 treatment on N
concentrations of shoots or tubers at the final harvest. In
the European CHIP experiment, potatoes grown at
680 mmol mol1 CO2 until harvest had significant reductions in nutrient concentrations both above-ground and in
tubers. Above-ground nitrogen declined 14.2%. Concentrations of nitrogen in tubers declined 6.4% (Fangmeier et al.,

Table 7
Effects of CO2 and chambers on potato at second harvest
Treatmenta

Mean shoot dry


wt. (g/plant)

Total tuber wet


wt. (kg ha1)

Total tuber dry


wt. (kg ha1)

No. 1b tuber
wt. (kg ha1)

Tuber solids
(%)

Tuber sucrose
(mg g1)

Tuber glucose
(mg g1)

ANC
A
A + 175
A + 350

99.8
75.4
63.2
75.1

31431
18894
22264
25865

6380
3987
4787
5432

21800
12033
14398
20200

20.3
21.1
21.5
21.0

5.9
5.0
3.8
4.0

0.13
0.10
0.07
0.07

a
ab
b
b

a
b
b
b

Numbers in a column that are followed by different letters are significantly different as determined by Duncans multiple range test ( p < 0.05).
a
ANC = ambient CO2, no chamber; A = OTC, ambient CO2; A + 175 = OTC, ambient + 175 mmol mol1 CO2; A + 350 = OTC, ambient +
350 mmol mol1 CO2.
b
No. 1 tubers are >4.8 and <8.9 cm without defects.

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

2002). Wong (1979) found that increases in C:N ratios with


elevated CO2 range from 10 to 30% while Cotufro et al. (1998)
found that green leaves from herbaceous species experienced
an average 17% decline in N (54 observations). Though N
decreases at Fairbanks and in the CHIP experiment are at the
low end of this range, it is not possible to state that CO2
response was not limited by soil nitrogen.
None of the published studies of CO2 effects in potatoes
have found an increase in leaf number or leaf area index
prior to the late stages of potato growth when senescence
begins to occur. Thus, increases in plant weight or tuber
yields that have been found under elevated CO2 were due to
an increase in photosynthesis rate rather than increased leaf
area.
Atmospheric carbon dioxide levels appeared to have no
effect on phenology or growth rate at Fairbanks. Experiments with a number of species have shown that elevated
CO2 can increase, decrease, or have no effect on rate of plant
development (Hesketh and Hellmers, 1973; Paez et al.,
1980; Carter and Peterson, 1983; Marc and Gifford, 1984;
Garbutt and Bazzaz, 1984; Reekie and Bazzaz, 1991). Other
field experiments testing the effects of elevated CO2 on
potatoes have come to various conclusions regarding
whether CO2 affects growth rates or phenology. Miglietta
et al. (1998) found that flowering and leaf senescence
commenced earlier when CO2 was elevated. Similarly,
Schapendonk et al. (2000) observed that leaf senescence was
earlier in the late-maturing cultivar Elles when grown at
700 mmol mol1 CO2 especially under the warm conditions.
However, elevated CO2 did not affect leaf senescence in the
early-maturing cultivar Gloria. In the European CHIP
experiments, elevated CO2 resulted in shorter plants
(suggesting a premature ending of plant growth), reduced
leaf number at late growth stages (Hacour et al., 2002) and
an earlier decline in chlorophyll content (Bindi et al., 2002)
suggesting that CO2 hastened senescence.
The main effects of elevated CO2 for the first harvest at
Fairbanks were manifested in the pattern of biomass
allocation to various plant organs. The root to shoot ratio
and percent of DW allocated to tubers increased and total
shoot DW, number of stems, number of flowers, and the
percent of DW allocated to leaves and stems decreased under
elevated CO2. An increase in root to shoot ratio is a common
outcome for plants grown at elevated CO2 (Rogers et al.,
1992).
At the final harvest there was no effect of CO2 or chamber
on shoot DW. Miglietta et al. (1998) also found that elevated
CO2 did not increase above-ground DW of potatoes grown in
a FACE experiment conducted in Italy. In the European
CHIP experiment, above-ground biomass at the intermediate harvest was 6.9% greater at 680 mmol mol1 than at
ambient CO2 but there was no difference in above-ground
biomass at the final harvest (Craigon et al., 2002).
Most studies of CO2 effects on tuberous species have
shown increased allocation of biomass to tubers at increased
CO2 (Lawlor and Mitchell, 1991; Bhattacharya et al., 1990;

55

Idso et al., 1988). The percent of biomass allocated to tubers


at Fairbanks increased from 37.5% in AC plots to 54.5% in
A + 350 plots. Though WW and DW of tubers significantly
increased 36.9 and 36.2%, respectively, in chambers when
grown at ambient plus 370 mM M1 CO2, the increased
potato yield and biomass production of 51% predicted by
Cure and Acock (1986) for a doubling of CO2 was not
realized at Fairbanks. Two factors may account for this.
First, PPFD at Fairbanks was reduced in chambers by 7
14%. In many locations further south, PPPD levels are well
above the 1200 mmol m2 s1 PPPD light saturation level
for potato (Schapendonk et al., 2000) and a 14% decrease
would not bring PPFD levels below the light saturation
point. This is not the case at Fairbanks were solar-noon light
levels rarely rise above 1400 mmol m2 s1 and levels in
chambers would barely be above the light saturation point
even at noon on the brightest day. The decreases in PPFD
levels caused by chambers almost certainly decreased
yields.
Low air temperatures may have also limited CO2
response. Idso et al. (1987) predicted crop yields at elevated
CO2 decline at air temperatures below 18.5 8C. The average
air temperature at canopy level at Fairbanks between potato
emergence and final harvest was 18.3 C in 1994. Average
temperatures recorded during this same time frame at the
Fairbanks International Airport were 16.8 C versus the
long-term average (19712000) for this period of 15.8 8C.
Low temperatures are thought to limit CO2 response by
decreasing plant growth and sink strength (Acock and
Allen, 1985). It should be noted, however, that significant
increases in tuber yields under elevated atmospheric CO2
were found in the European CHIP experiments at growing
season temperatures that were considerably lower than at
Fairbanks. Total tuber DW increases of 53.9 and 41.1%
were recorded for potatoes grown at 680 mmol mol1 CO2
at Carlow, Ireland and at Sutton Bonington, UK with mean
growing season chamber temperatures of 15.6 8C. However, tuber yields declined 7.3% when potatoes were grown
under the same CO2 regime at Goteborg, Sweden and the
mean chamber temperature was 14.2 8C (Craigon et al.,
2002).
High reducing sugar content is responsible for
producing overly dark colors when tubers are fried in
oil at high temperatures with the result that tubers with
high levels of reducing sugars cannot be used for making
fries or chips (Sowokinos and Preston, 1988). Since potato
tubers in Alaska are normally characterized by high
reducing sugar content, the decline in reducing sugars
found in this study resulting from elevated atmospheric
CO2 are of practical benefit to potato growers in Alaska
and elsewhere where tuber reducing sugar content is high.
In the European CHIP study, citric acid, the glycoalkaloid chaconine and nitrate concentrations declined when
potatoes were grown at 680 mmol mol1 CO2. Levels of
reducing sugars were also lower, but not significantly so
(Vorne et al., 2002).

56

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957

5. Conclusions
Potatoes grown at elevated CO2 at Fairbanks exhibited
enhanced tuber yields and changes in dry weight allocation
patterns. Biomass allocated to stems, leaves, and flowers
declined while that allocated to tubers increased with
elevated CO2. Root:shoot ratio was larger and percent leaf
nitrogen declined 12.6% with increased CO2. At the final
harvest, total tuber dry weight in the A + 350 chambers was
36% higher than in the A treatment. However, yields in
open-top chamber plots were lower than the no-chamber
plots possibly due to 714% less photosynthetic active
radiation in chambers. Whether global change will result in
higher yields of potatoes and other crops at high latitude
locations such as Fairbanks may depend as much on what
happens to cloud cover, light intensity, growing season
length and average temperature as it does on increasing
atmospheric CO2. This is because the current average
growing season temperature (15.8 8C) is at the lower end of
the range where increasing CO2 has been found to be
stimulatory to crop yields. Any increases in cloudiness that
reduce growing season temperature and PPFD could reduce
plant growth more than rising atmospheric CO2 levels can
stimulate growth. Finally, more field research is needed to
determine the interrelationships between N nutrition and
CO2 response in potato.

Acknowledgements
The authors thank Hugo Rogers and Lee Allen for help in
the design of the OTC system, for suggesting suppliers and
for providing other advice. Bill Saari built the equipment
building, the CO2 monitoring system, helped construct the
OTC system, and collected data. Richard Deck helped with
construction, collected data, and helped with data analysis.
Steve Prior made useful suggestions on an earlier version of
the manuscript.

References
Acock, B., Allen, L.H. Jr., 1985. Crop responses to elevated carbon dioxide
concentrations. In: Strain, B.R., Cure, J.D. (Eds.). Direct effects of
increasing carbon dioxide on vegetation. DOE/ER-0238. U.S. Department of Energy, Carbon Dioxide Research Division, Washington, pp.
5398.
Adamsen, F.J., Wechsung, G., Wechsung, F., Wall, G.W., Kimball, B.A.,
Pinter Jr., P.A., LaMorte, R.L., Garcia, R.L., Hunsaker, D.J., Leavitt,
S.W., 2005. Temporal changes in soil and biomass nitrogen for irrigated
wheat grown under free-air carbon dioxide enrichment (FACE). Agron.
J. 97, 160168.
Allen Jr., L.H., Drake, B.G., Rogers, H.H., Shinn, J.H., 1992. Field
techniques for exposure of plants and ecosystems to elevated CO2
and other trace gasses. Crit. Rev. Plant Sci. 11, 85119.
Benz, S., Roos, M., Hasslen, D., 2002. Alaska Agricultural Statistics. U.S.
Department of Agriculture National Agricultural Statistics Service,
Palmer, Alaska.

Berntson, G.M., McConnaughay, K.D.M., Bazzaz, F.A., 1993. Elevated


CO2 alters deployment of roots in small growth containers. Oecologia
94, 558565.
Bhattacharya, N.C., Hileman, D.R., Ghosh, P.P., Musser, R.L., Bhattacharya, S., Biswas, P.K., 1990. Interaction of enriched CO2 and water
stress on the physiology and biomass production in sweet potato grown
in open top chambers. Plant Cell Environ. 13, 933940.
Bindi, M., Hacour, A., Vandermeiren, K., Craigon, J., Ojanpera, K., Sellden,
G., Hogy, P., Finnan, J., Fibbi, L., 2002. Chlorophyll concentration of
potatoes grown under elevated carbon dioxide and/or ozone concentrations. Eur. J. Agron. 17, 319335.
Carter, D.R., Peterson, K.M., 1983. Effects of a CO2 enriched atmosphere
on the growth and competitive interaction of a C3 and C4 grass.
Oecologia 58, 188193.
Conn, J.S., Cochran, V.L., Deck, R.E., 1994. Rooting volume effects on
barley CO2 response. Agron. Abstr. 143.
Craigon, J., Fangmeier, A., Jones, M., Donnelly, A., Bindi, M., De Temmerman, L., Persson, K., Ojanpera, K., 2002. Growth and marketable-yield
responses of potato to increased CO2 and ozone. Eur. J. Agron. 17, 273
289.
Cotufro, M.F., Ineson, P., Scott, A., 1998. Elevated CO2 reduces the nitrogen
concentration of plant tissues. Glob. Change Biol. 4, 4354.
Cure, J.D., 1985. Carbon dioxide doubling responses: a crop survey. In:
Strain, B.R., Cure, J.D. (Eds.), Direct Effects of Increasing Carbon
Dioxide on Vegetation. DOE/ER-0238. U.S. Dept. of Energy, Carbon
Dioxide Research Division, Washington DC, pp. 99116.
Cure, J.D., Acock, B., 1986. Crop responses to carbon dioxide doubling: a
literature survey. Agric. For. Meteorol. 38, 127145.
De Temmerman, L., Hacour, A., Guns, M., 2002a. Changing climate and
potential impacts on potato yield and quality CHIP: introduction, aims
and methodology. Eur. J. Agron. 17, 233242.
De Temmerman, L., Wolf, J., Colls, J., Bindi, M., Fangmeier, A., Finnan, J.,
Ojanpera, K., Pleijel, H., 2002b. Effect of climatic conditions on tuber
yield (Solanum tuberosum L.) in the European CHIP experiments. Eur.
J. Agron. 17, 243255.
Donnelly, A., Craigon, J., Black, C.R., Colls, J.J., Landon, G., 2001. Does
elevated CO2 ameliorate the impact of O3 on chlorophyll content and
photosynthesis in potato (Solanum tuberosum)? Physiol Plant 111, 501
511.
Drake, B.G., Gonzalez-Meler, M.A., Long, S.P., 1997. More efficient plants:
a consequence of rising atmospheric CO2? Annu. Rev. Plant Physiol.
Plant Mol. Biol. 48, 609639.
Fangmeier, A., De Temmerman, L., Black, C., Persson, K., Vorne, V., 2002.
Effects of elevated CO2 and/or ozone on nutrient concentrations and
nutrient uptake of potatoes. Eur. J. Agron. 17, 353368.
Farrar, J.F., Williams, M.L., 1991. The effects of increased atmospheric
carbon dioxide and temperature on carbon partitioning, source-sink
relations and respiration. Plant Cell Environ. 14, 819830.
Garbutt, K., Bazzaz, F.A., 1984. The effects of elevated CO2 on plants. III.
Flower, fruit and seed production and abortion. New Phytol. 98, 433446.
Goudriaan, J., Ajtay, G.L., 1979. The possible effects of increased CO2 on
photosynthesis. In: Bolin, B., Degens, E.T., Kempe, S., Ketner, P.
(Eds.), The Global Carbon Cycle. John Wiley and Sons, Chichester,
pp. 237249.
Goudriaan, J., de Ruiter, H.E., 1983. Plant growth in response to CO2
enrichment at two levels of nitrogen and phosphorus supply. 1. Dry
matter, leaf area and development. Netherl. J. Agric. Sci. 31, 157169.
Guinn, G., Mauney, J.R., 1980. Analysis of CO2 exchange assumptions:
feedback control. In: Hesketh, J.D., Jones, J.W. (Eds.), Predicting of
Photosynthesis for Ecosystem Models, vol. II. CRC Press, Boca Raton,
Florida, pp. 116.
Hacour, A., Craigon, J., Vandermeiren, K., Ojanpera, K., Pleijel, H.,
Danielsson, H., Hogy, P., Finnan, J., Bindi, M., 2002. CO2 and ozone
effects on canopy development of potato crops across Europe. Eur. J.
Agron. 17, 257272.
Herold, A., 1980. Regulation of photosynthesis by sink activity- the missing
link. New Phytol. 86, 131144.

J.S. Conn, V.L. Cochran / Agriculture, Ecosystems and Environment 112 (2006) 4957
Hesketh, J.D., Hellmers, H., 1973. Floral initiation in four plant species
growing in CO2 enriched air. Environ. Contr. Biol. 11, 5153.
Ho, L.C., 1977. Effects of CO2 enrichment on the rates of photosynthesis
and translocation of tomato leaves. Ann. Appl. Biol. 87, 191200.
Idso, S.B., Kimball, B.A., Anderson, M.G., Mauney, J.R., 1987. Effects of
atmospheric CO2 enrichment on plant growth: the interactive role of air
temperature. Agric. Ecosys. Environ. 20, 110.
Idso, S.B., Kimball, B.A., Mauney, J.R., 1988. Effects of atmospheric CO2
enrichment on root:shoot ratios of carrot, radish, cotton, and soybean.
Agric. Ecosyst. Environ. 21, 293299.
Jarvis, P.G., 1989. Atmospheric carbon dioxide and forests. Phil. Trans.
Royal Soc. London B. 324, 369392.
Jordan, D.B., Ogren, W.L., 1984. The specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose-biphosphate
concentration, pH and temperature. Planta 161, 308313.
Kimball, B.A., 1983. Carbon dioxide and agricultural yield: an assemblage
and analysis of 430 prior observations. Agron. J. 75, 779788.
Kolbe, H., Stephan-Beckmann, S., 1997. Development, growth and chemical composition of the potato crop (Solanum tuberosum L.). I leaf and
stem. Potato Res. 40, 111129.
Kramer, P.J., 1981. Carbon dioxide concentration, photosynthesis, and dry
matter production. Bioscience 31, 2933.
Ku, S.B., Edwards, G.E., Tanner, C.B., 1977. Effects of light, carbon
dioxide, and temperature on photosynthesis, oxygen inhibition of
photosynthesis, and transpiration in Solanum tuberosum. Plant Physiol.
59, 868872.
Lawlor, D.W., Mitchell, R.A.C., 1991. The effects of increasing CO2 on
crop photosynthesis and productivity: a review of field studies. Plant
Cell Environ. 14, 807818.
Lawson, T., Craigon, J., Black, C.R., Colls, J.J., Landon, G., 2001. Effects of
elevated CO2 and O3 on the photosynthetic capacity of potato (Solanum
tuberosum L) in open-top chambers. J. Plant Physiol. 158, 309323.
Leadley, P.W., Drake, B.G., 1993. Open top chambers for exposing plant
canopies to elevated CO2 concentration and for measuring net gas
exchange. Vegetation 104105, 315.
Madsen, E., 1968. Effect of CO2 concentration on the accumulation of
starch and sugar in tomato leaves. Physiol. Plant 21, 168175.
Marc, J., Gifford, R.M., 1984. Floral initiation in wheat, sunflower, and
sorghum under carbon dioxide enrichment. Can. J. Bot. 62, 914.
Miglietta, F., Magliulo, V., Bindi, M., Cerio, L., Vaccari, P., Loduca, V.,
Peressotti, A., 1998. Free air CO2 enrichment of potato (Solanum tuberosum L.): development growth and yield. Glob. Change Biol. 4, 163172.
Morison, J.I.L., Lawlor, D.W., 1999. Interactions between increasing CO2
concentration and temperature on plant growth. Plant Cell Environ. 22,
659682.
Oechel, W.C., Strain, B.R., 1985. Native species responses to increased
atmospheric carbon dioxide concentration. In: Strain, B.R., Cure, J.D.
(Eds.), Direct Effects of Increasing Carbon Dioxide on Vegetation.
DOE/ER-0238. U.S. Dept. Of Energy, Carbon Dioxide Research Division, Washington DC, pp. 117154.

57

Paez, A., Hellmers, H., Strain, B.R., 1980. Carbon dioxide effects on apical
dominance in Pisum sativum. Physiol. Plant 50, 4346.
Pearcy, R.W., Bjorkman, O., 1983. Physiological effects. In: Lemon, E.R.
(Ed.), CO2 and Plants: the Response of Plants to Rising Levels of
Atmospheric Carbon Dioxide. Westview Press, Boulder, Colorado, pp.
65105.
Reekie, E.G., Bazzaz, F.A., 1991. Phenology and growth in four annual
species grown in ambient and elevated CO2. Can. J. Bot. 69, 24752481.
Rogers, H.H., Heck, W.W., Heagle, A.S., 1983. A field technique for the
study of plant responses to elevated carbon dioxide concentrations. Am.
Pollution Contr. Assoc. J. 33, 4244.
Rogers, H.H., Peterson, C.M., McCrimmon, J.N., Cure, J.D., 1992.
Responses of plant roots to elevated atmospheric carbon dioxide. Plant
Cell Environ. 15, 749752.
Schapendonk, H.C.M., van Oijen, M., Dijkstra, P., Pot, C.S., Wilco, J.R.M.,
Stoopen, J., Stoopen, G.M., 2000. Effects of elevated CO2 concentration
on photosynthetic acclimation and productivity of two potato cultivars
grown in open-top chambers. Aust. J. Plant Physiol. 27, 1119
1130.
Shaver, G.R., Billings, W.D., Chapin III, F.S., Giblin, A.E., Nadelhoffer,
K.J., Oechel, W.C., Rastetter, E.B., 1992. Global change and the carbon
balance of arctic ecosystems. Bioscience 42, 433441.
Sicher, R.C., Bunce, J.A., 1999. Photosynthetic enhancement and conductance to water vapor of field-grown Solanum tuberosum (L.) in response
to CO2 enrichment. Photosyn. Res. 62, 155163.
Sowokinos, J.R., Preston, D.A., 1988. Maintenance of Potato Processing
Quality by Chemical Maturity Monitoring (CMM). Station Bulletin
5861988. Minnesota Agricultural Experiment. Station, University of
Minnesota.
Stitt, M., Krapp, A., 1999. The interaction between elevated carbon dioxide
and nitrogen nutrition: the physiological and molecular background.
Plant Cell Environ. 22, 583621.
Stutte, G.W., Yorio, N.C., Wheeler, R.M., 1996. Interacting effects of
photoperiod and photosynthetic photon flux on net carbon assimilation
and starch accumulation in potato leaves. J. Am. Soc. Hort. Sci. 121,
264268.
Vandermeiren, K., Black, C., Lawson, T., Casanova, M.A., Ojanpera, K.,
2002. Photosynthetic and stomatal responses of potatoes grown under
elevated CO2 and or O3results from the European CHIP-programme.
Eur. J. Agron. 17, 337352.
Vorne, V., Ojanpera, K., De Temmerman, L., Bindi, M., Hogy, P., Jones, M.B.,
Lawson, T., Persson, K., 2002. Effects of elevated carbon dioxide and
ozone on potato tuber quality in the European multiple-site CHIPproject. Eur. J. Agron. 17, 369381.
Wheeler, R.M., Tibbitts, T.W., Fitzpatrick, A.H., 1991. Carbon dioxide
effects on potato growth under different photoperiods and irradiance.
Crop Sci. 31, 12091213.
Wong, S.C., 1979. Elevated atmospheric partial pressure of CO2 and plant
growth. I. Interactions of nitrogen nutrition and photosynthetic capacity
in C3 and C4 plants. Oecologia 44, 6874.

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