Goudriaan, J.

Keulen, H., van

English

Wageningen Yield 

Reprint: N(•th. J. awic. Sci. 27 ( 1979) 227-234 
The direct and indirect effects of nitrogen shortage 
on photosynthesis and transpiration in maize and sunflower 
J. Goudriaan 1 and H. van Keulen 2 
1 Department of Theoretical Production Ecology, Agricultural University, Wage-
ningen, the Netherlands 
2 Centre for Agrobiological Research (CABO), Wageningen, the Netherlands 
Accepted: 15 May 1979 
Key words: photosynthesis, transpiration, stomatal resistance, water use efficiency, 
nitrogen nutrition 
Summary 
Experiments were carried out to investigate the effect of nitrogen shortage in the 
leaf tissue on stomatal behaviour. The results show that in maize a linear relation 
exists between the rate of net C02 assimilation and the conductance for water 
vapour, independently of the nitrogen status of the tissue. In sunflower a similar 
relation exists although the evidence is less conclusive. It is concluded that stomatal 
behaviour cannot explain differences in water use efficiency between plants, grow-
ing at different levels of nitrogen. 
Introduction 
Numerous experiments have been carried out to investigate the relation between 
dry matter production and water use. It has been shown that in many situations 
there is a constant ratio between the two values for a given plant species under well 
defined environmental conditions (de Wit, 1958). However, too often exceptions 
are encountered that are difficult to explain physiologically. 
One way to obtain insight in the influence of external factors on stomatal be-
haviour and on the ratio between photosynthesis and transpiration is simultaneous 
measurement of transpiration and C02 assimilation of individual leaves. The results 
presented in a previous paper (Goudriaan & van Laar, 1978) showed that in maize 
and bean plants, functioning under presumably optimum conditions, the rate of net 
photosynthesis and the leaf conductance for water vapour are proportional to each 
other. Since this proportionality was maintained at non-saturating light intensities, 
it was concluded that leaf resistance was not the limiting factor for C02 assimila-
tion. The stomata did close, however, over some range in response to increase in 
external C02 concentration, so that regulation by the C02 concentration in the sub-
227 
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J. GOUDRIAAN AND H. VAN KEULEN 
stomatal cavity seems the most likely explanation for the observed proportionality. 
In maize the mechanism maintains internal C02 concentrations around 120 tJ-1/1, in 
bean (Phaseolus) on the other hand around 220 tJ-1/1. In sunflower the regulation 
appeared to be absent, leading to higher and more variable values for the internal 
C02 concentration. Further experiments carried out since then have shown, how-
ever, that the regulatory mechanism can be present to a greater or lesser extent in 
the same plant species, depending on (as yet) unknown external or internal condi-
tions. Absence of regulation leads to higher transpiration losses in plant stands at 
the same photosynthetic performance and hence to lower values of water use effi-
ciency. This phenomenon may explain part of the so far unexplicable values of 
water use efficiency. 
Field and container experiments indicate that nutrient shortage in general cau-
ses deterioration of the water use efficiency (Lof, 1976; Nielsen, 1963), a pheno-
menon that was treated in some detail by Viets (1962). It was speculated therefore 
whether nitrogen shortage could bring about differences in stomatal behaviour, 
that could account for the observed decrease in water use efficiency. This paper 
describes the results of experiments, carried out to investigate the influence of 
nitrogen shortage on photosynthesis and transpiration of individual leaves. 
Materials and methods 
Seeds of maize (Zea mays, cv. LG11) and sunflower (Helianthus annuus, cv. Fran-
sol) were germinated on perlite and one-week old seedlings were transferred to 
pots, filled with a Hoagland nutrient solution of half strength, with iron added as 
ferric sodium-EDTA. The plants were grown in a growth chamber at a temperature 
of 20 o C, a light intensity of 60 W m-2 at plant height and a relative humidity 
around 70%. 
At the age of three weeks, half of the maize plants were transferred to nutrient 
solutions in which the NQ-3 was replaced by CI-, while the remainder, serving as 
control, continued to grow on the normal solution. After one week on the nitrogen-
depleted solution, the plants showed visible signs of nitrogen shortage: light green 
leaves, browning tips in old ones. At that moment the measurements started. 
The sunflower plants were grown on the half-Hoagland solution for two weeks, 
after which they were divided into four groups, growing on solutions in which 0 
(control), 50, 80 and 90 % of the nitrate was replaced by chloride respectively. 
The measurements started three weeks later. The nutrient solutions were replaced 
twice a week. 
The measurements were carried out on leaves attached to the plants, at a tem-
perature of 25 oc, an irradiance up to ± 400 W m-2 (400-700 nm) and, unless 
indicated otherwise, a C02 concentration of 280 pJ/1. 
Results and discussion 
Maize 
The photosynthesis-light response curve of the maize leaves, averaged over 20 
228 Neth. J. agric. Sci. 27 (1979) 
' 
' 
EFFECTS OF NITROGEN SHORTAGE ON MAIZE AND SUNFLOWER 
Pn 
10-6 kg co2 m-2s-1 
1.2 
0.8 
0.6 
0.4 A A 
o Control 
A -N 
-o.2 ~ 
_J 100 200 I 300 400 I wm-2 
Fig. 1. The relation between the incident tight intensity (I) 
and the net rate of C02 assimilation (Pn) for maize plants 
grown with and without nitrogen. C02 concentration 280 
JLI/1. 
plants, of both the control and the nitrogen stressed treatment is given in Fig. 1. 
These curves can be described by: 
Pn == (Pm+R) X (1.-exp(el/(Pm+R)))-R 
in which I absorbed visible radiation (W m-2) 
Pm the light saturated net assimilation rate (kg (C02) m-2 (leaf) s-1) 
R == dark respiration rate (kg (C02) .m.-2 (leaf) s-1) 
e light use efficiency (kg (C02) J - 1) 
The numerical values of these parameters are given in Table 1a, which shows that 
nitrogen shortage reduced P m to less than half the value of the control and the 
light use efficiency to about 80 %. (Unfortunately the nitrogen concentration in the 
tissue was not determined, so that its nitrogen status can only be described in qua-
litative terms.) There is surprisingly little difference in the dark respiration rate 
between the two treatments. That may, however, be understandable when it is taken 
into account that the plants in the growth chamber are operating at a very low 
energy level, so that the actual level of 'activity', which accounts for about 70 % 
of the respiratory requirements (de Wit et al., 1978) does not differ too much be-
tween the control and the nitrogen deficient plants. It may therefore not be con-
cluded from these observations that, when the plants are operating at higher energy 
levels, a greater proportion of the fixed energy is lost from the nitrogen-stressed 
plants. 
To investigate whether the observed decline in photosynthetic performance of 
the nitrogen-deprived plants was an indirect effect, caused by the accumulation of 
assimilates in the leaves as a result of growth inhibition, the two treatment groups 
were further subdivided. One group was measured directly after a 28-hour dark 
period, the other one after a 16-hour period in light at an intensity of 300 W m-2 
visible. Two main effects could be distinguished. The dark respiration rate was 
considerably higher after the light period for both the control (from 18 X 10-9 to 
35.5 X 10-9 kg (C02) m-2 s-1), and the nitrogen-stressed plants (from 17.5 X 10-9 to 
27 X 10-9 kg (C0
2
) m-2 s-1). There was also a significant difference in the specific 
Neth. J. agric. Sci. 27 (1979) 229 
===========================================================================================================-j 
J. GOUDRIAAN AND H. VAN KEULEN 
Table 1. The maximum rate of photosynthesis (Pro), the light use efficiency (s) and the rate 
of dark respiration (R) for maize and sunflower leaves at different levels of N supply and, for 
sunflower, different concentrations of C02 external. 
Maize Sunflower 
con- -N Nl N 1/2 N 1/5 N 1/10 
trol 280 
280 ,ul/1 280 480 280 480 280 480 280 480 
~-till ,ul/1 ,ul/1 ,ulll ,ul/1 ,ul/1 ,ul/1 ,ul/1 ,ul/1 
Pm (10- 6 kg (C02) m - 2 s- 1) 1.16 0.47 0.69 1.11 0.44 0.58 0.49 0.81 0.42 0.64 
s (10- 9 kg (C02) J - 1) 11.9 9.2 9.7 14.2 8.6 10.6 8.6 11.1 8.6 9.2 
R (10- 6 kg(C02)m2 - s- 1) 0.035 0.027 0.032 0.030 0.036 0.041 
leaf dry weight of the nitrogen-stressed plants after the dark (27 X 10-3 kg m-2) and 
after the light period (33 X 10-3 kg m-2), whereas in the control group it was in both 
cases the same (31 X 10-3 kg m-2). When the respiration rates are calculated on a 
dry weight basis, the values amount to 0.58 X 10~ kg (C02) kg (dm)-1s-1 and 
1.15 X 10-6 for the control plants and to 0.65 X 10-6 and 0.82 X 10-6 for the nitro-
gen-stressed plants after dark and after light respectively. These observations in-
dicate considerable assimilate accumulation in the leaves of the nitrogen-stressed 
plants, and fast export from the leaves of the non-stressed ones, the higher respira-
tion rate being partly the result of higher photosynthetic activity, partly associated 
with transportation cost. Comparison of the respiration rates, measured after the 
(r1 +rbf
1 
10"3m s"1 
8 
7 
6 
5 
4 
3 
Maize (control ) 
:. 
0.4 0.6 
.. 
.. . 
.. 
0.8 t t2 t4 
Pn 10'"6 kg C02 m-2 s"1 
Fig. 2. The relation between the net rate of C0-2 assimilation (Pn) and the total conductance 
((r1 + rb) -1) for water vapour for leaves of maize plants well supplied with nitrogen. 
AC~ = 166 ,ul/1. 
230 Neth. J. agric. Sci. 27 (1979) 
EFFECTS OF NITROGEN SHORTAGE ON MAIZE AND SUNFLOWER 
(rl +rbf' 
10"3m s"1 
8. 
7. 
6. 
5. 
4. 
2. 
. . ·
· .. 
1. •• 
0.2 
maize (-N) 
.. 
.. 
. : .... , .. . 
.... 
. ' . ' . 
...... ;·~ . 
0.4 0.6 0.8 
J 
Fig. 3. The relation between the net rate of C02 assimilation (Pn) and the total conductance 
for water vapour ((r1 + rb) - 1) for leaves of maize plants growing at sub-optimum nitrogen 
nutrition. 
light period, with the P m values in Table 1 could suggest a somewhat higher respira-
tory loss per unit of assimilation in the nitrogen-stressed plants, but the evidence is 
not very convincing. 
There was, however, no difference in the maximum rate of photosynthesis nor 
in light use efficiency between the stressed plants that had been in the dark and 
those that had been in the light. The reduction in photosynthetic performance 
therefore seems not to be associated with assimilate accumulation in the leaves. 
Since the water use efficiency is a main point of interest, the relation between 
the conductance for water vapour (the inverse of the sum of leaf resistance and 
boundary layer resistance) and the net rate of C02 assimilation was determined. 
The data points for the control group, measured at various light intensities, are 
given in Fig. 2. A linear relationship seems a reasonable approximation, indicating 
an almost constant C02 concentration in the substomatal cavity. The eye-fitted 
straight line, forced through the origin represents a difference between external 
and internal C02 concentration of 166 111/l, so that the internal concentration was 
maintained around 110-120 111fl. This agrees very well with earlier observations 
(Goudriaan & van Laar, 1978). The results of the measurements at the lowest light 
intensity (27 W m-2 visible, incident), however,~ are all situated above the eye-fitted 
line, indicating disproportionally higher conductance values and hence higher inter-
nal C02 concentrations, amounting to ca. 160 111/l, indicating that the regulatory 
mechanism is not operating perfectly over the complete range of photosynthesis 
rates. 
Neth. J. agric. Sci. 27 (1979) 231 
~~~~~~--~--~~~-~~---~ --~~ ~---~--~ ----- -~----~~----~------ ---- -~-~~------~----~- ~- -- --- ------~--~~~~---~---- -- ~~---~~~ --- ---~----~-----~~-~--- -~- - - ~----- - - - - ----~--~-
================================-,~==~-
Pn 
10" 6kg C02 m"
2s" 1 
1.2 
1. 
0.8 
0.6 
0 
0.4 .f 
0.2 I! 
0 
6. 
X 
01~---L----L---~----L 
100 200 300 400 I 
w m"2 
J. GOUDRIAAN AND H. VAN KEULEN 
Pn 
10" 6kg C02 m·2s·1 
1.2 
1 
0.8 
0.6 
0.4 
0 
0.2 i 
J 100 
0 
0 
t;. 
)( 
200 
0 
)( 
t;. 
300 400 I 
wm· 2 
Fig. 4. The relation between incident light intensity (I) and the rate of net C02 assimilation 
(Pn) for leaves of sunflower plants, grown in solutions where 0(0), 50(6), 80(0) or 90(X) % 
of the nitrate had been replaced by chloride, measured at an external C0-2 concentration of 
280 f(lll (left) and 480 f(lll (right). 
Crt •r..>·' 
to·:Dms-1 
16 
14 
12 1-
10 
8 
0 
6 
0 
~ 
0 
0 
'A 
A 
2 
q 
I' AD 
-
0 I 
0.1 0 
232 
0 
0 
" . 
0 
0. 
D 
- 0 R 
D 
A 
A 
• 
I 
0.2 
. 
Ill' 
• 
. 
. 
• 
I 
. 
• .. 
• a a 
0 0 
• 
0 
0 
,. 
a 0 
A 
.... 
D 
. 
Sunflower 
280 vpm 
0 
Fig. 5. The relation between the net rate 
of C~ assimilation (Pn) and the total 
conductance for water vapour (r1 + rb)-1) 
for leaves of sunflower plants, grown in 
solutions where 0(0), 50(6), 80(0) or 
90( X) % of the nitrate had been re-
placed by chloride, and measured at an 
external C02 concentration of 280 f(lll. 
Neth. J. agric. Sci. 27 (1979) 
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----- ----- --------------------------------··-·--.. -·------
.. ----~-=-=====================================' 
EFFECTS OF NITROGEN SHORTAGE ON MAIZE AND SUNFLOWER 
(r1•rbr' 
10"3ms 
10 
. . 0 0 
. 
6 0 0 
0 
0 0 
6 .. 
.. 
0 0 
~ . 0 
. 
"" 0 
0 0 
4 D .. 
0 
.... 
.. 
0 
ao . 
A . 
0 Ao 
0 
2 .A A A D 0 D 
. 
0 AA 
4iW' 
0 I I I I I I 0.1 0 0.2 0.4 0.6 0.6 1. 12 
Pn 1<?"6kg C02m·\·' 
Fig. 6. The relation between the net rate of CO~ assimilation (Pn) and the total conductance 
for water vapour (fJ + rb) - 1) for leaves of sunflower plants, grown in solutions where 0(0), 
SO(L::,), 80(0) or 90(X) % of the nitrate had been replaced by chloride, and measured at an 
external C02 concentration of 480 J.Ll/1. 
The data points for the nitrogen-deficient plants are give in Fig. 3. Surprisingly, 
the points are arranged in a similar fashion as in Fig. 2 around the same straight 
line, which has been repeated here for comparison. These results indicate that as 
far as stomatal regulation is involved, only a small effect of nitrogen stress on 
water use efficiency may be expected in maize plants. 
Sunflower 
The photosynthesis-light response curves for sunflower plants grown at different 
levels of N supply, measured at external C02 concentrations of 280 and 480 ~1/1 
respectively, are given in Fig. 4. Net C02 assimilation is positively related to both 
the level of N in the nutrient solution and the C02 concentration in the external air. 
This holds for the maximum rate, P m• as well as for the light use efficiency, E 
(Table 1b). 
In Fig. 5 and 6 the relation between conductance for water vapour and net C02 
assimilation is given for the two levels of C02 in the external air. In both cases 
there is a positive correlation between the variables, which, when expressed in 
terms of the difference in C02 concentration between the outside air and the sub-
stomatal cavity, corresponds to values of 40 and 80 ~1/1 for the low and high exter-
nal concentration respectively. Hence in this case the stomata of the plants did 
respond to some extent to the increased C02 level in the external air, contrary to 
earlier observations (Goudriaan & van Laar, 1978). Lower levels of nitrogen in 
the solution, and presumably therefore in the plat~t tissue, lead to decreased rates 
Neth. J. agric. Sci. 27 (1979) 233 
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J. GOUDRIAAN AND H. VAN KEULEN 
of photosynthesis as well as transpiration, but due to the scatter in the individual 
observations, the conclusion of an invariant conductance/assimilation ratio cannot 
be drawn with certainty. 
Conclusions 
The results presented in this paper indicate that for maize and sunflower very little 
difference in water use efficiency at different levels of nitrogen nutrition may be 
expected, on basis of assimilation and transpiration of individual leaves. There is 
some indication that at lower N levels a proportionally larger part of the assimilated 
carbon is lost by respiration, which could be associated with breakdown and trans-
port of nitrogeneous compounds. 
Observations showing deterioration of water use efficiency for whole plants or 
crops under conditions of N shortage may thus have to be attributed to differences 
in the distribution pattern of the ·assimilates, notably a larger share for the under-
ground plants parts. Measurement of the carbon balance for different organs over 
a 1onger time period could elucidate this hypothesis. 
References 
Goudriaan, J. & H. H. van Laar, 1978. Relations between leaf resistance, C02-concentration 
and C02-assimilation in maize, beans, lalang grass and sunflower. Photosynthetica 12: 241-
249. 
Lof, H., 1976. Water use efficiency and competition between arid zone annuals, especially the 
grasses Phalaris min(j.r and Hordeum murinum. Agric. Res. Rep. (Versl. landbouwk. Onderz.) 
853, Pudoc, Wageningen. 
Nielsen, B. F., 1963. Plant production, transpiration ratio and nutrient ratios as influenced by 
interactions between water and nitrogen. Thesis, Royal Veterinary & Agricultural College, 
Copenhagen. 
Viets Jr, F. G., 1962. Fertilizers and the efficient use of water. Adv. Agron. 14: 223-264. 
Wit, C. T. de, 1958. Transpiration and crop yields. Verst. !andbouwk. Onderz. (Agric. Res. 
Rep.) 64.6, Pudoc, Wageningen. 
Wit, C. T. de et al., 1978. Simulation of assimilation, respiration and transpiration of crops. 
Simulation Monographs, Pudoc, Wageningen. 
234 Neth. J. agric. Sci, 27 (1979) 
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Fertilizers and the efficient use of water.

Plant production, transpiration ratio and nutrient ratios as influenced by interactions between water and nitrogen. Thesis, Royal Veterinary & Agricultural College,

Relations between leaf resistance, C02-concentration and C02-assimilation in maize, beans, lalang grass and sunflower.

Simulation of assimilation, respiration and transpiration of crops. Simulation Monographs,

Transpiration and crop yields.

Water use efficiency and competition between arid zone annuals, especially the grasses Phalaris min(j.r and Hordeum murinum.

The direct and indirect effects of nitrogen shortage on photosynthesis and transpiration in maize and sunflower

The direct and indirect effects of nitrogen shortage on photosynthesis and transpiration in maize and sunflower

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