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Functions of Nitrogen, Phosphorus and Potassium in Energy Status and Their

Influences on Rice Growth and Development

Article in Rice Science · August 2021

DOI: 10.1016/j.rsci.2022.01.005

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Rice Science, 2022, 29(2): 166−178

Research Paper

Functions of Nitrogen, Phosphorus and Potassium in Energy

Status and Their Influences on Rice Growth and Development

MA Jiaying1, #, CHEN Tingting1, #, LIN Jie1, 2, FU Weimeng1, FENG Baohua1, LI Guangyan1, LI Hubo1,
LI Juncai1, 2, WU Zhihai2, TAO Longxing1, FU Guanfu1
(1National Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China; 2Agronomy College,
Jilin Agricultural University, Changchun 130118, China; #These authors contributed equally to this work)

Abstract: Nitrogen (N), phosphorus (P) and potassium (K) are important essential nutrients for plant
growth and development, but their functions in energy status remains unclear. Here, we grew Nipponbare
rice seedlings in a growth chamber for 20 d at 30 ºC/24 ºC (day/night) under natural sunlight conditions
with different nutrient regimes. The results showed that N had the strongest influence on the plant growth
and development, followed by P and K. The highest nonstructural carbohydrate content, dry matter
weight, net photosynthetic rate (Pn), ATP content, as well as NADH dehydrogenase, cytochrome oxidase
and ATPase activities were found in the plants that received sufficient N, P and K. The lowest values of
these parameters were detected in the N-deficient plants. Higher dry matter accumulation was observed
in the K-deficient than in the P-deficient treatments, but there was no significant difference in the ratio of
respiration rate to Pn between these two treatments, suggesting that differences in energy production
efficiency may have accounted for this result. This hypothesis was confirmed by higher ATP contents and
activities of NADH dehydrogenase, cytochrome oxidase and ATPase in the K-deficient plants than in the
P-deficient plants. We therefore inferred different abilities in energy production efficiency among N, P and
K in rice seedlings, which determined rice plant growth and development.
Key words: rice; nutrient element; photosynthesis; respiration; plant growth and development; energy
production efficiency

Elements such as nitrogen (N), phosphorus (P) and
potassium (K) are the most essential nutrients for
plant growth and development (Ye et al, 2019; Wang
Y et al, 2021). Higher plant tissues typically contain
approximately 1.5% N, 0.2% P and 1.0% K
(Hawkesford et al, 2012), suggesting that plant growth
demands large amounts of these macronutrients
(Bernstein et al, 2019). Indeed, the increased supply of
N, P and K in crop production systems has been the
main contributor to yield enhancement over the past
several decades. However, the overuse of chemical
fertilizers has severely damaged the environment by
enhancing greenhouse gas levels and promoting
eutrophication, mainly as a result of low fertilizer
utilization efficiency (Glibert, 2017; Yao et al, 2018;
Song et al, 2020; Wang H X et al, 2021). Therefore,
maintaining nutrient homeostasis and enhancing
fertilizer efficiency are critical for reducing fertilizer
use in crop production systems and thereby protecting
the environment (Tang et al, 2021).
Among the three major macronutrients, N affects
the organic structure, physiological characteristics and
biomass synthesis and distribution of plants, and has
the greatest effect on dry matter production (Zhu et al,
2014; Lin et al, 2016; Schmierer et al, 2021).
Insufficient N supply seriously impairs the structure

Received: 6 April 2021; Accepted: 6 July 2021

Corresponding authors: FU Guanfu (fugf1981@sina.com); TAO Longxing (taolongxing@caas.cn)
Copyright © 2022, China National Rice Research Institute. Hosting by Elsevier B V
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Peer review under responsibility of China National Rice Research Institute
http://dx.doi.org/10.1016/j.rsci.2022.01.005
MA Jiaying, et al. Nitrogen, Phosphorus and Potassium Affect Rice Energy Production Efficiency
and function of photosynthesis, thereby reducing crop
yields (Kalaji et al, 2014; Zhao et al, 2017). Similarly,
P deficiency in plants can markedly reduce leaf area,
alter photosynthesis and carbon metabolism, and
ultimately limit tillering, biomass accumulation and
yield (Xu et al, 2007; Chaudhary et al, 2008). In
contrast to N and P, K does not bind covalently to
organic molecules. However, it is the most abundant
cellular cation, regulating stomatal movement, osmotic
adjustment, charge balance, steady-state enzyme
activation, membrane potential and membrane protein
transport (Schroeder, 2003; Shabala, 2003; Britto and
Kronzucker, 2008; Maathuis, 2009; Blatt et al, 2014;
Wang and Wu, 2015). These results indicate that
complex interactions among N, P and K determine
nutrient homeostasis and thus plant growth and
development. However, previous studies of the
functions of N, P and K in plant growth and
development have primarily focused on leaf
morphology, carbon dioxide absorption, biochemical
capacity, or a combination of these factors, whereas
the effects of these elements on plant energy
metabolism in plants are still not well understood.
Energy is the basis of life, and all living things
depend on a constant energy transmission mechanism
in order to grow and reproduce (Sousa et al, 2018).
ATP provided by mitochondria through oxidative
phosphorylation plays an essential role in plant
development, reproduction and various biochemical
processes (Bauwe et al, 2010; Millar et al, 2011; Liao
et al, 2018). N affects plant energy homeostasis by
regulating photosynthesis and respiration (Aspinwall
et al, 2016; Inomura et al, 2019; Moriwaki et al, 2019).
However, N assimilation and translocation are high
energy processes (Taiz and Zeiger, 2010) and can
limit N use efficiency when N fertilizer is overused or
P and K are deficient, leading to nutrient imbalance. P
is found in essential biomolecules, including nucleic
acids, ATP and phospholipids, which is closely linked
to energy metabolism (Poirier and Bucher, 2002). K+
is used as a major solute to maintain turgor and drive
irreversible and reversible changes in cell volume, and
it also plays an important role in numerous metabolic
processes. Indeed, the circulation of K+ in the phloem
serves as a form of decentralized energy storage that
can be used to overcome local energy limitations
(Dreyer et al, 2017). It has been documented that
posttranslational modification of the phloem-expressed
K+ channel AKT2 taps the ‘K battery’ in Arabidopsis,
which then efficiently assists the plasma membrane
167
H+-ATPase in transmembrane phloem (re)loading
processes (Gajdanowicz et al, 2011). These findings
indicate that N, P and K influence energy metabolism
by affecting photosynthesis, respiration, charge balance
and phosphorylation regulation. Nutrient imbalance in
the soil or the plant can inhibit plant growth and
development by disturbing energy homeostasis.
Although a large body of research has focused on
the effects of N, P and K on plant growth and
development under different nutrient conditions, the
rational use of fertilizers to ensure food supply and
environmental security remains one of the great
challenges of the 21st century (Ju and Christie, 2011;
Zhang et al, 2012). Thus, understanding the relationship
between N, P and K and energy homeostasis in plants
is necessary for improving grain yield and quality
while reducing fertilizer supply. In addition, most
experiments have been conducted in nutrient solution,
which differs significantly from actual agricultural
production. Here, we investigated the effects of N, P
and K on the energy metabolism of rice plants grown
at eight N, P and K levels in soil. These eight
treatments were: no fertilization (H2O); standard N, P
and K fertilization (NPK); P and K fertilization
without N (-N); N and K fertilization without P (-P);
N and P fertilization without K (-K); ½N with
standard P and K fertilization (½N); ½P with standard
N and K fertilization (½P); and ½K with standard N
and P fertilization (½K).
RESULTS
Leaf chlorophyll content, tiller number, plant
height and dry matter weight
As shown in Fig. 1, rice plants from different nutrient
treatments differed markedly in chlorophyll content,
plant height and tiller number per plant. Leaf
chlorophyll content in the NPK treatment was
significantly higher than those in other treatments (Fig.
1-B). There was little difference in leaf chlorophyll
content among the -P, -K, ½N, ½P and ½K treatments,
but leaf chlorophyll contents in these treatments were
markedly higher than those in the -N and H2O
treatments. Remarkable increases were observed in
chlorophyll content as the supply of N enhanced, but
such results were not found in plants treated with P or
K. However, slightly increases in chlorophyll content
were found in the -K and ½K treatments compared
with the corresponding -P and ½P treatments.
Plant height in the ½K treatment was significantly
168 Rice Science, Vol. 29, No. 2, 2022

Fig. 1. Effects of N, P and K on plant morphology of rice.

A, Phenotype of rice plants at 20 d after nutritional treatments. Scale bar is 10 cm. B, Total chlorophyll content. C, Plant height. D, Tiller number per
plant. E, Dry matter weight per plant.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 8). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.

higher than the other treatments, in which no obvious
differences were found among the treatments of NPK,
-P, -K and ½N (Fig. 1-C). Similarly, the lowest plant
height was observed in the H2O treatment, followed
by the -N treatment, which was significantly lower
than the other treatments. Interestingly, the plant
heights in the treatments of -P and ½P were lower
than the corresponding -K and ½K treatments. About
3.7 and 2.6 of tiller numbers per plant were found in
the NPK and ½K treatments, respectively, which were
obviously higher than the other treatments, in
particular the H2O and -N treatments (Fig. 1-D). As
the supply of N, P and K enhanced, the tiller number
per plant clearly increased. Compared with the -P and
½P treatments, about 27.0% and 32.9% increase in
tiller numbers per plant were observed in the
corresponding -K and ½K treatments. Similar change
pattern was observed in the dry matter weight. The
highest dry matter weight was found in the NPK
treatment, followed by the ½K and -K treatments,
while the lowest dry matter weight was showed in the
H2O treatment (Fig. 1-E). The dry matter weight per
plant increased significantly as N, P and K were
enhanced. Compared with the -P and ½P treatments,
remarkable increases in dry matter weight by 43.7%
and 21.3% were observed in the corresponding -K and
½K treatments.
Soluble sugar, starch and nonstructural
carbohydrate (NSC) contents
The production and consumption of carbohydrates
play a key role in the accumulation of plant dry matter
weight, and we therefore measured NSC, soluble
sugar and starch contents in plants grown under
different nutrient conditions. The highest content of
soluble sugar was showed in the NPK treatment, while
the lowest value was observed in the H2O treatment
(Fig. 2-A). The soluble sugar content increased as the
N and P supply enhanced. There was a slight increase
in the -K treatment compared with the ½K treatment,
and the soluble sugar contents of the -K and ½K
treatments were higher by 16.1% and 0.4% than those
of the corresponding -P and ½P treatments.
Similar patterns were found in the starch and NSC
contents, in which the highest and lowest values were
found in the NPK and H2O treatments, respectively
MA Jiaying, et al. Nitrogen, Phosphorus and Potassium Affect Rice Energy Production Efficiency 169

Fig. 2. Effects of N, P and K on contents of carbohydrates in rice plant leaves.

A, Soluble sugar content. B, Starch content. C, Nonstructural carbohydrate (NSC) content.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 3). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.

(Fig. 2-B and -C). As the supply of N, P and K enhanced,
the starch and NSC contents increased. The contents
of starch and NSC in the ½K and -K treatments were
higher than those of rice plants treated with ½P and -P,
respectively. About 14.8% and 13.8% increases in
starch content were showed in ½K and -K treatments
compared with the corresponding -P and ½P
treatments, while for NSC, the increases were 17.1%
and 30.1%, respectively.
Photosynthesis, respiration and photorespiration in
rice leaves
Plant carbohydrate levels are determined by the
photosynthesis and respiration, and we therefore
measured the net photosynthetic rate (Pn), respiration
rate (Rd), photorespiration rate (Pr) and Rubisco
activity in leaves from different nutrient treatments.
The highest value of Pn was found in the NPK
treatment, while the lowest value was found in the
H2O treatment (Fig. 3-A). Among the -N, -P and -K
treatments, Pn was the lowest in the -N treatment,
followed by the -P and -K treatments. A similar
pattern was found in the ½N, ½P and ½K treatments.
Overall, leaf Pn increased significantly as N, P or K
supply enhanced. For Rd, the highest value was
showed in the treatment of ½K, while the lowest value
was found in the -N treatment (Fig. 3-B). Among the
½N, ½P and ½K treatments, Rd was the highest in the
½K treatment, followed by the ½P and ½N treatments.
A similar pattern was observed for the -N, -P and -K
treatments. Interestingly, there was no obvious
difference in Rd between the -P and -K treatments or
the ½P and ½K treatments, although they were
significantly higher than the corresponding -N and
½N treatments. There were no obvious differences in
Pr among the treatments, with the exception of the
NPK treatment, which had a significantly lower Pr
value than the ½N treatment (Fig. 3-C).
The ratios of Rd to Pn and Pr to Pn responded
differently to N, P and K supply (Fig. 3-D and -E).
The highest values of Rd / Pn and Pr / Pn were found in
the H2O treatment, followed by the -N and ½N
treatments, which were significantly higher than the
other treatments. Interestingly, there were no obvious
differences in these parameters between the -K and -P
treatments or the ½K and ½P treatments.
Pn and Pr are determined by the balance between
the Rubisco carboxylase and oxygenase activities. For
the Rubisco carboxylase, the highest and lowest
activities were observed in the NPK and H2O
treatments, respectively (Fig. 3-F). Among the -N, -P
and -K treatments, the highest Rubisco carboxylase
activity was found in the -K treatment, followed by
the -P and -N treatments. A similar pattern was
observed in the ½N, ½P and ½K treatments. By
contrast, the highest and lowest Rubisco oxygenase
activities were observed in the H2O and NPK
treatments, respectively (Fig. 3-G). There were no
obvious differences in the Rubisco oxygenase activity
among the treatments with the exception of the NPK
treatment. The Rubisco oxygenase activity of the NPK
treatment was significantly lower than those of the
H2O, -N, and ½N treatments. The highest ratio of
oxygenase to carboxylase activity was measured in the
H2O treatment, and the lowest ratio was found in the
NPK treatment, which were almost significantly
higher or lower than the other treatments (Fig. 3-H).
For the -N, -P and -K treatments, the highest value
was found in the -N treatment, followed by the -P and
-K treatments. A similar pattern was observed in the
170 Rice Science, Vol. 29, No. 2, 2022

Fig. 3. Effects of N, P and K on photosynthesis, respiration and photorespiration in rice plant leaves.
A, Net photosynthetic rate (Pn). B, Respiration rate (Rd). C, Photorespiration rate (Pr). D, Ratio of Rd to Pn. E, Ratio of Pr to Pn. F, Ribulose
1,5-bisphosphate carboxylase activity. G, Ribulose 1,5-bisphosphate oxygenase activity. H, Ratio of oxygenase to carboxylase.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 3). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.

½N, ½P and ½K treatments.
Energy production in rice leaves under different
nutrient treatments
Respiration is the main pathway by which plants and
animals produce energy, and the activities of
mitochondrial complexes I, IV and V determine the
energy production efficiency of plants. Here, the
activities of complexes I, IV and V in the NPK treatment
were higher than the other treatments, particularly in
the H2O treatment (Fig. 4-A to -C). The activities of
the three complexes increased as the N, P and K were
enhanced. Among the -N, -P and -K treatments, the
highest values were observed in -K, followed by -P
and -N. A similar pattern was observed among the ½N,
½P and ½K treatments. Compared with the -P and ½P
treatments, higher activities of these three complexes
were showed in the -K and ½K treatments,
respectively, in particular the ATPase activity. The
ATPase activities of the plants treated with -K and

Fig. 4. Effects of N, P and K on energy production efficiency in rice plant leaves.

A, NADH dehydrogenase (Complex I) activity. B, Cytochrome oxidase (Complex IV) activity. C, ATPase (Complex V) activity. D, ATP content.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 3). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.
MA Jiaying, et al. Nitrogen, Phosphorus and Potassium Affect Rice Energy Production Efficiency 171

½K were significantly higher by 16.5% and 17.7%
than those treated with -P and ½P, respectively.
Without exception, the ATP content in the NPK
treatment was significantly higher than the other
treatments, in which the lowest value was found in the
H2O treatment (Fig. 4-D). N had the greatest effect on
ATP content, followed by P and K. Among the -N, -P
and -K treatments, the ATP content in the -K
treatment was markedly higher by 75.1% and 32.7%
than the -N and -P treatments, respectively. A similar
pattern was observed among the ½N, ½P and ½K
treatments, although there was no obvious difference
between the ½P and ½K treatments.
Antioxidant capacity and contents of H2O2 and
malondialdehyde (MDA)
Antioxidant capacity affects plant survival under
stress conditions, and nutrient deficit itself is a source
of stress. We therefore measured the antioxidant
enzymes such as superoxide dismutase (SOD), catalase
(CAT), peroxidase (POD) and ascorbate peroxidase
(APX) activities as well as the contents of H2O2 and
MDA in plants from different nutrient conditions. The
highest SOD activity was showed in the ½K treatment,
which was significantly higher than the other
treatments except the NPK treatment (Fig. 5-A).
Except for these two treatments, there were no
obvious differences for SOD activity among the other
treatments. As to POD, CAT and APX, the highest
and lowest activities were found in the NPK and H2O
treatments, respectively (Fig. 5-B to -D). Among the
-N, -P and -K treatments, the highest activities of
these enzymes were observed in the -K treatment,
followed by the -P and -N treatments. Similar results
were found among the ½N, ½P and ½K treatments.
By contrast, the highest contents of H2O2 and MDA
were showed in the H2O treatment, while the lowest
contents were found in the NPK treatment (Fig. 5-E
and -F). Among the -N, -P and -K treatments, the
highest contents of H2O2 and MDA were observed in
the -N treatment, followed by the -P and -K treatments.
Similar results were found among the ½N, ½P and
½K treatments. Overall, the H2O2 and MDA contents
decreased as N, P and K enhanced, in particular for
the H2O2 content.
N, P and K contents in rice plants under different
nutrient treatments
Different changing patterns were observed in the N, P
and K contents of plants grown under different
nutrient regimes (Fig. 6). The N content enhanced as
the supply of N and P increased, but such result was
not found for K supply (Fig. 6-A). It is noteworthy
that the highest N content was showed in the plants

Fig. 5. Effects of N, P and K on the antioxidant capacity, H2O2 and lipid peroxidation in leaves of rice plants.
A, Superoxide dismutase (SOD) activity. B, Peroxidase (POD) activity. C, Catalase (CAT) activity. D, Ascorbate peroxidase (APX) activity. E, H2O2
content. F, Malondialdehyde (MDA) content.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 3). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.
172 Rice Science, Vol. 29, No. 2, 2022

Fig. 6. Changes in contents of total N (A), available P (B) and available K (C) in rice plant leaves under different nutrient conditions.
Eight treatments were used: no fertilization (H2O); standard N, P and K fertilization (NPK); P and K fertilization without N (-N); N and K fertilization
without P (-P); N and P fertilization without K (-K); ½N with standard P and K fertilization (½N); ½P with standard N and K fertilization (½P); and
½K with standard N and P fertilization (½K). Data are Mean ± SD (n = 3). One-way analysis of variance was conducted to compare the difference
with least significant difference test at P ≤ 0.05. Different lowercase letters above the bars indicate significant differences among treatments.

from the -K treatment rather than the NPK treatment. Table 1. Ratios among N, P and K contents in rice plants under
Without exception, the lowest N content was observed different nutrient conditions.

in the H2O and -N treatments. Among the treatments Treatment N P K

of ½N, ½P and ½K treatments, the highest value was H2O 10.0 3.1 9.4
NPK 10.0 2.0 5.9
showed in the ½K treatment, which was higher by -N 10.0 3.1 10.1
4.4% and 15.5% than that in the ½P and ½N -P 10.0 2.1 7.6
treatments, respectively. The highest available P -K 10.0 1.9 4.6
content was observed in the -K treatment, followed by ½N 10.0 2.2 7.5
½P 10.0 2.1 6.8
the NPK treatment, which was significantly higher ½K 10.0 1.9 6.1
than the other treatments, with the exception of ½P N content was set to 10.0 in each treatment, and accordingly the values
treatment (Fig. 6-B). The available P content was the of P and K were showed as ‘10 × P content / N content’ and ‘10 × K
content / N content’, respectively.
lowest in the H2O treatment, but there were no
obvious differences among the H2O, -N, -P, ½N and treatments, respectively. However, the value for K in
½K treatments. As to the K content, the highest and the other treatments was significantly higher or lower
lowest values were showed in the -P and H2O treatments, than 5.9, especially for the H2O and -N treatments.
respectively. Compared with the -P treatment, about
11.3% and 18.6% decreases were showed in the -N DISCUSSION
and -K treatments (Fig. 6-C). Among the treatments of The effects of N, P and K on the growth and
½N, ½P and ½K, the highest value was showed in the development of crop plants have been extensively
½N treatment, which was higher by 0.7% and 6.7% documented (Milla et al, 2005; Wang Y et al, 2021),
than the ½P and ½K treatments, respectively. and N plays the most important role in these processes
N, P and K ratios of rice plants under different (Kant, 2018; Wang et al, 2018; Iqbal et al, 2020). This
nutrient treatments was consistent with the present results that the plant
height, chlorophyll content, tiller number per plant
The balance of N, P and K determines plant growth and dry matter weight, were markedly lower in those
and development and is frequently disturbed by plants without N than the other treatments (Fig. 1).
environmental conditions, we therefore measured the Similarly, such results were also found in plants
ratios of N, P and K contents in plants under different grown in hydroponic with tap water, in which the
nutrient regimes. The value for N was set to 10.0 in tiller number per plant and plant height of those plants
each treatment, and N:P:K in the NPK treatment was without N were markedly decreased compared with
10.0:2.0:5.9 (Table 1). The values of P in most the plants from the other treatments (Fig. S1).
treatments were about 2.0, with the exception of the As to P and K, remarkable increases in the dry
H2O and -N treatments. The value for K was 5.9 in the matter weight and tiller number per plant were
NPK treatment and 6.8 and 6.1 in the ½P and ½K observed in the plants from the -K or ½K treatments
MA Jiaying, et al. Nitrogen, Phosphorus and Potassium Affect Rice Energy Production Efficiency
compared with those from the corresponding -P or ½P
treatments (Fig. 1). This result seemed to suggest that
P may play a more important role in plant growth and
development than K (Nam et al, 2006). However, in
potato plants, the partitioning of dry matter to tubers is
markedly reduced by K deficiency but is increased by
P deficiency (Jenkins and Mahmood, 2003). Indeed,
the functions of P and K in plant growth and
development may depend on the background values of
nutrient and environment (Gaspar et al, 2017; Wang Y
et al, 2021). We found higher decreases in tiller number
per plant and plant height in the plants from the -P
treatment compared with those from the -K treatment
in hydroponic with tap water (Fig. S1). It is notable
that the -K treatment in nutrient solution (distilled
water) was lethal to rice plants under warm conditions,
whereas such results were not found in other
treatments, even for plants grown without any
additional nutrients (data not shown). This phenomenon
has not been reported previously, and more research is
required to reveal the underlying mechanism.
Carbohydrate metabolism is involved in plant
growth and development under both normal and stress
conditions, including nutrient deficit (Hermans et al,
2006; Li et al, 2006; Islam et al, 2019; Jiang et al,
2020). Here, the lowest NSC content was showed in
plants without N (Fig. 2). This finding was inconsistent
with previous reports that N, P and K fertilization
increases the sugar and starch contents of kernels and
that the effect of K fertilization is the most significant
(Li et al, 2006). This might be related with assimilate
production and consumption in rice plants under
different nutrient conditions, which is determined by
the ratio of Rd to Pn. It has been reported that a large
amount of assimilates produced by photosynthesis is
consumed through respiration. In the present study,
photosynthesis and respiration was almost significantly
inhibited by N deficit (Fig. 3-A and -B), but the
highest values of Rd / Pn were showed in the H2O and
-N treatments (Fig. 3-D). This result suggested that N
deficit significantly decreased the accumulation of dry
matter not only through lower assimilate production
but also higher relative carbohydrate consumption
(Reich et al, 1998; Foyer et al, 2011).
Higher NSC content was showed in the -K treatment
than in the -P treatment (Fig. 2). In this process,
higher Pn was showed in the -K treatment than in the
-P treatment (Fig. 3-A). However, little difference was
found in Rd / Pn between the -P and -K treatments,
which was inconsistent with their differences in dry
173
matter weight, tiller number per plant and NSC content
(Figs. 1–3). Such results have not been documented in
previous studies, and we speculated that this finding
might be related to the differences in energy metabolism
under different nutrient conditions (Fig. 4).
In the mitochondria, multiprotein complexes such
as NADH dehydrogenase (Complex I), succinate
dehydrogenase (Complex II), cytochrome bc1 (Complex
III), cytochrome oxidase (Complex IV) and ATPase
(Complex V) are involved in the respiratory process
and drive cellular energy (ATP) production (Milla et al,
2011; Meyer et al, 2019). These proteins are frequently
affected by abiotic stress (Dahal et al, 2014; Shameer
et al, 2019; Li et al, 2020) and nutrient status (Wang H
X et al, 2021), thereby affecting the efficiency of ATP
production. In this experiment, the ATP content and
the activities of NADH dehydrogenase, cytochrome
oxidase and ATPase were much lower in plants
without N than those from the other treatments (Fig.
4). This result indicated that the energy production
efficient can be obviously inhibited by N deficit (Liu
et al, 2020). As to the functions of P and K, we found
that P had a more important role in energy production
efficiency compared with K, as ATP content was
significantly higher in the -K treatment than in the -P
treatment (Fig. 4-D). Furthermore, the activities of
NADH dehydrogenase, cytochrome oxidase and
ATPase were lower in the -P treatment than in the -K
treatment, although this difference was not significant
(Fig. 4), which has not been found in the previous
documents. This finding might be mainly due to their
different functions in energy production in plants. As
reported, P is an important component of nucleic acids,
ATP and phospholipids (Poirier and Bucher, 2002),
while K always servers as an essential cofactor of
enzymes and a decentralized energy storage (Gajdanowicz
et al, 2011).
H2O2 is a signaling molecule involving in the
response of plants to environmental stress (Sierla et al,
2016), but it is also toxic for plants when
overproduced (Singh et al, 2017). Its homeostasis is
therefore important for plant growth and development.
The contents of H2O2 and MDA were significantly
higher in the plants without N than those in the other
treatments (Fig. 5-E and -F). This finding was consistent
with previous reports that N has a strong ability to
maintain reactive oxygen species (ROS) homeostasis
in plants (Chokshi et al, 2017; Shao et al, 2020).
Likewise, P and K also function in maintaining plant
ROS homeostasis, since the H2O2 and MDA contents
174
decreased as the supply of P and K increased (Fig. 5).
Interestingly, higher increases in contents of H2O2 and
MDA were observed in the -P treatment than in the -K
treatment compared with those in the NPK treatment
(Fig. 5). We speculated that P might be more
important than K for maintaining ROS homeostasis in
plants under soil conditions. The capacity of the
antioxidant system is almost certainly the primary
contributor to this process. To cope with the harmful
effects of ROS, plant cells are equipped with a well-
developed antioxidant defense system comprising
multiple enzymes (Li et al, 2016). In particular, APX
activity may be the main contributor by which P
deficit increased the overproduction of ROS, as its
activity was clearly lower in the -P treatment than in
the -K treatment (Fig. 5-D). It has been well
documented that antioxidant capacity exacts a high
energetic cost (Jiang et al, 2020; Li et al, 2020). Under
cold stress, glutathione content and APX activity are
significantly reduced when ATPase activity is
decreased in rice plants (Yu et al, 2020). Therefore,
the lower energy status associated with P deficit may
have contributed significantly to lower antioxidant
capacity as well as higher H2O2 and MDA contents in
the -P treatment than in the -K treatment.
Complex interactions have been found between N,
P and K in plants, and these can strongly influence
plant growth and development (Milla et al, 2005;
Rosenstock et al, 2016). Interestingly, the highest N
and P contents were observed in plants from the -K
treatment (Fig. 6-A and -B). This finding may reflect
interactions among N, P and K metabolism in plants.
Plants typically absorb N as nitrate (NO3−) and
ammonium (NH4+). The absorption and transport of
K+ and NO3− are coordinated (Triplett et al, 1980),
whereas antagonism has been shown between NH4+
and K+ (Wang et al, 1996; ten Hoopen et al, 2010).
Although the interaction between P and K is unclear,
there is a crosstalk between signaling pathways for
plant responses to K and P (Wang Y et al, 2021).
External high K+ concentrations can inhibit Pi uptake
in Arabidopsis (Ródenas et al, 2019). Indeed, plants
have evolved complex signaling networks to respond
to fluctuating external levels of nutrients, and these
mechanisms help plants to utilize nutrients efficiently
(Wang Y et al, 2021). These results can explain the
higher accumulation of dry matter in the -K treatment
than in the -P treatment (Fig. 1-B).
The N, P and K ratios of plant tissue differed
among different nutrient treatments. Rice plants in the
Rice Science, Vol. 29, No. 2, 2022
NPK treatment had the highest dry matter weight and
ATP content and the lowest Rd / Pn, in which their
ratio among N, P and K was 10.0:2.0:5.9 (Table 1).
The next highest dry matter weight was measured in
the ½K treatment, and its N, P and K ratio was
10.0:1.9:6.1. These findings indicated that the balance
of nutrients in plants is important for their growth and
development and can enhance fertilizer utilization
efficiency to reduce fertilizer use in crop production
systems. The N, P and K ratio in plants is not constant
and can change among different varieties and
environments. Therefore, more research is required to
characterize the mechanisms that underlie the N, P
and K ratios in rice plants under different nutrient
conditions.
In sum, sufficient N, P and K can enhance the growth
and development of rice seedlings by enhancing
photosynthetic capacity and energy production efficiency
to improve the energy status (Fig. 7). In contrast, these
seedling plants were inhibited under the conditions of
N, P or K deficit. Among these three important
nutrients, N deficit not only significantly decreased the
photosynthetic capacity, but also markedly enhanced the
assimilate consumption, and thus reduced the energy
production efficiency. P, rather than K, played a more
important role in the growth and development of rice
seedling plants grown in soil through regulating
Fig. 7. Model of NPK functioned in energy production efficiency
in rice plants.
When the plants was provided adequate NPK, the photosynthesis of
leaves and the energy production efficiency such as the activities of
NADH dehydrogenase, cytochrome oxidase and ATPase of leaves in
the electron transport chain of oxidative phosphorylation in mitochondria
were enhanced, which would produce more energy in plants, and thus
significantly increased the accumulation of dry matter weight. In
contrast, when the NPK was insufficient, the photosynthesis and
energy production were inhibited, resulting in lower ATP production,
which can reduce the dry matter accumulation.
MA Jiaying, et al. Nitrogen, Phosphorus and Potassium Affect Rice Energy Production Efficiency
energy production efficiency (Fig. 7). Therefore,
rational application of fertilizer including N, P and K
can improve the rice plant growth and development by
maintaining nutrient homeostasis to increase energy
production and reduce assimilate consumption.
METHODS
Plant materials and growth conditions
The study was performed at the experimental farm of the China
National Rice Research Institute, Hangzhou, China. Seeds of
rice variety Nipponbare were soaked for 48 h and then
germinated for 24 h at 35 ºC. Nearly 25 seeds were sown in a
pot with 10 cm height and 10 cm diameter with 1 kg of paddy
soil (pH 7.1) that contained 1 400 mg/kg total N, 1 470 mg/kg
total P, 400 mg/kg total K, 33.74 mg/kg available N, 10.8
mg/kg available P, 58.4 mg/kg available K and 0.99% organic
matter. The seedlings were grown in a chamber under natural
sunlight of 1 000 μmol/(m2·s), the temperature was set to 30 ºC
during the day and 24 ºC at night, and the relative humidity was
maintained at 70%–80%. The seedlings were thinned to 10
plants per pot at the three-leaf stage, and fertilizers, including
urea (46% N), superphosphate (12% P) and potassium chloride
(50% K) were applied. The standard application of nitrogen,
phosphate and potash fertilizers is 0.683, 2.87 and 0.353 g/kg
of dry soil, respectively. The experiment was designed with
five replicates of eight treatments: 1) no fertilization (H2O); 2)
standard N, P and K fertilization (NPK); 3) P and K
fertilization without N (-N); 4) N and K fertilization without P
(-P); 5) N and P fertilization without K (-K); 6) ½N with
standard P and K fertilization (½N); 7) ½P with standard N and
K fertilization (½P); and 8) ½K with standard N and P
fertilization (½K). About 20 d after treatments, the photosynthesis,
respiration and photorespiration of rice leaves were measured
as well as the number of tillers per plant, plant height and dry
matter weight per plant were determined. Whereafter, the
youngest fully expanded leaves were harvested to measure
chlorophyll content, Rubisco activity, carbohydrates, energy
metabolism, antioxidant capacity and the contents of total N, P
and K.
Measurements of tiller number, plant height and dry matter
weight
At 20 d after treatment, the average number of tillers per plant
was investigated, and representative plants were selected based
on the average number of tillers to measure plant height from
the root to the top of the uppermost leaf. Afterwards, the whole
seedlings were harvested, dried to a constant weight at 80 ºC
for at least 48 h, and weighed.
Chlorophyll content analysis
Chlorophyll contents were determined according to the method
described by Sartory and Grobbelaar (1984). Leaf samples (0.1
g) were extracted in 20 mL of 95% ethanol for 48 h. The
175
absorbance of the resulting extract was measured at 665 and
649 with a spectrophotometer (Lambda25; Perkin Elmer,
Freemont, CA, USA). Chlorophyll a (Ca) and b (Cb) contents
were calculated according to the formulas: Ca = 13.95 × A665 −
6.88 × A649; Cb = 24.96 × A649 − 7.32 × A665. Total chlorophyll
content was determined by calculating the sum of the
chlorophyll a and b contents.
Carbohydrate measurement
According to the method of Dubois et al (1956), 0.2 g fresh
leaves were boiled with 10 mL deionized water in a 100 ºC
water bath for 20 min. The resulting extract was collected to
measure total soluble sugar and starch contents using the
sulfuric acid anthrone colorimetric method with modifications.
Total NSC content was calculated as the sum of the soluble
sugar and starch contents.
Measurements of ribulose 1,5-bisphosphate carboxylase
and oxygenase activities
Ribulose 1,5-bisphosphate carboxylase and oxygenase activities
were measured according to Feng et al (2020). About 0.2 g of
leaf sample was weighed and finely ground in liquid nitrogen in
a pre-cooled mortar and transferred to a 2-mL tube filled with 1
mL of 0.1 mol/L PBS buffer containing 0.2 mol/L Na2HPO4
and NaH2PO4 (pH 7.2). The crude enzyme extract was
centrifuged at 13 400 × g for 5 min. The double-antibody
sandwich enzyme-linked immunosorbent assay (ELISA)
technique was used following the manufacturer’s instructions
(Shanghai Enzyme-linked Biotechnology Co., Ltd., China), and
absorbance was monitored at 450 nm with a spectrophotometer
(UV-2600, Shimadzu, Kyoto, Japan). A standard curve was
used to calculate the activities of Rubisco carboxylase and
oxygenase.
Measurements of Pn, Pr and Rd
Pn, Pr and Rd were analyzed from the Pn-Ci curve with a
portable photosynthesis system (Li-Cor 6400, Lincoln, NE,
USA) according to Sharkey et al (1988) and Feng et al (2020).
The maximum Pn (Pnmax), CO2 compensation point (Γ*),
intercellular CO2 concentration (Ci) and Rd were estimated
based on the non-rectangular hyperbola model. The ratio of
Rubisco oxygenation to carboxylation (Φ) was estimated by the
equation: Φ = 2 ×Γ* / Ci. Pr was calculated by the equation: vo =
(Pnmax + Rd) / (1 / Φ ‒ 0.5), in which vo is the rate of
oxygenation and also twice of the rate of Pr.
Measurements of mitochondrial complexes and ATP
The activities of mitochondrial Complex I (NADH dehydrogenase),
Complex IV (cytochrome oxidase) and Complex V (ATPase)
were measured with an assay kit according to the
manufacturer’s instructions (Comin Biotechnology Co. Ltd.,
Suzhou, China). ATP content was determined using an ATP
assay kit according to the manufacturer’s instructions (Geruisi
Biotechnology Co., Ltd., Suzhou, China).
176
Antioxidant enzyme activity, H2O2 and lipid peroxidation
measurements
About 0.2 g of frozen leaf tissue was homogenized in 5 mL of
extraction buffer (100 mmol/L phosphate buffer, pH 7.0). The
homogenate was centrifuged at 10 000 × g at 4 ºC for 10 min,
and the supernatant was used to determine SOD, CAT, POD
and APX activities according to the methods of Giannopolitis
and Ries (1977), Aebi (1983), Maehly and Chance (1954) and
Bonnecarrère et al (2011), respectively.
The method of Brennan and Frenkel (1977) was used to
measure H2O2 content. Frozen leaf tissue (0.2 g) was ground to
homogeneity in 4 mL of 10 mmol/L 3-amino-1,2,4-triazole,
and the homogenate was centrifuged at 8 000 × g for 10 min.
Next, 1.5 mL of 0.1% titanium tetrachloride in 20% H2SO4 was
added to 1.5 mL of the supernatant. The reaction solution was
further centrifuged to remove insoluble matter, and the
absorbance was measured at 410 nm.
MDA content was estimated by measuring the concentration
of thiobarbituric acid reactive substances. Frozen leaf tissue
(0.1 g) was homogenized in 3 mL of 5% trichloroacetic acid,
and the homogenate was centrifuged at 6 000 × g for 15 min.
The reaction mixture (1.5 mL of the supernatant, 1.5 mL of
20% trichloroacetic acid and 0.5% thiobarbituric acid) was
incubated in a water bath at 100 ºC for 30 min and then quickly
cooled in running water. The solution was centrifuged at 6 000 ×
g for 10 min, and the absorbance of the supernatant was
measured at 450, 532 and 600 nm.
Determination of total N, available P and K contents
Rice leaves were placed in an oven at 105 ºC for 30 min and
then dried to constant weight at 60 ºC for 24 h. After grinding
with a pulverizer, about 0.2 g sample was placed into a
digestion tube, and the CuSO4-Na2SO4 (1:10) catalyst and
concentrated sulfuric acid were added. N and P contents were
measured using a fully automatic intermittent chemical analyzer
(Smart Chem 450, AMS Group Westco, Italy), and total K
content was measured by the H2SO4-H2O2 digestion-flame
photometer method (Bernhart et al, 1961).
Statistical analysis
The test data were processed using Microsoft Excel 2019.
Figures showed the mean and standard deviations of three
replicate experiments. Treatment differences were assessed
with one-way analysis of variance and the least significant
difference test (P ≤ 0.05) using SPSS v.11.5 (SPSS Inc.,
Chicago, USA).
ACKNOWLEDGEMENTS
This study was supported by the Zhejiang Provincial Natural
Science Foundation, China (Grant Nos. LY19C130006 and
LY20C130011); the Open Project Program of State Key
Laboratory of Rice Biology, China (Grant No. 20190403); the
National Rice Industry Technology System, China (Grant No.
Rice Science, Vol. 29, No. 2, 2022
CARS-01); and the Central Public Interest Research Institute
Special Fund in China (Grant No. 2017RG004-1).
SUPPLEMENTAL DATA
The following material is available in the online version of this
article at http://www.sciencedirect.com/journal/rice-science;
http://www.ricescience.org.
Fig. S1. Effects of NPK on plant growth and development of
rice in hydroponic with tap water.
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