Root Foraging in Soybean (Glycine max) under Nitrogen Deprivation
Muhammad Adnan Tabassum1, Yi Dai1,
Zhenzhi Pan1, Lin Chen1, Muhammad Saleem2, Muhammad Aurangzaib3, Guisheng
Zhou1 and Li Song1*
1Joint
International Research Laboratory of Agriculture and Agri-Product Safety, The
Ministry of Education of China, Institutes of Agricultural Science and
Technology Development, Yangzhou University, Jiangsu, P. R. China
2College of
Bioscience and Biotechnology, Yangzhou University, Jiangsu, P. R. China
3Dept. of Agronomy,
Faculty of Agriculture and Environmental Sciences, The Islamia University of
Bahawalpur, Pakistan
*Correspondence: songli@yzu.edu.cn
Received 24 October 2020; Accepted 20 February 2021; Published 16 April 2021
Abstract
Nitrate is one of the key sources of nitrogen in natural
and agricultural soils. The distribution and concentration of nitrate determine
root system architecture in plants. Soybean (Glycine max L) is one of the key leguminous crops, while farmers
rarely apply nitrogen in soybean crops except for a starter nitrogen dose at
the time of sowing. However, the effects of severe deficiency nitrate on early
seedling establishment of soybean before nodulation are not yet studied.
Therefore, this study evaluated the effects of
high dose of nitrate (54.3 mM) and its deprivationon (0 mM) on the
root system architecture of soybean during seedling establishment.
Results showed that the root traits including primary root length, fresh
biomass, total length, surface area, tips, forks, and its crossings were
significantly higher under no nitrate condition than nigh nitrate condition
except for root volume, its dry biomass and diameter. Shoot growth attributes
such as shoot length, shoot fresh biomass, shoot dry biomass, single leaf area,
soil-plant analysis development value, and photosynthesis was significantly
decreased while leaf dry mass per area was increased significantly under no
nitrate condition. Furthermore, high nitrate supply significantly enhanced the
content of nitrate in root tissue, but there was no significant difference
between low and optimal nitrate supply. In summary, this study indicated that
soybean root system architecture adopts a foraging strategy under nitrogen
deprived environment. © 2021 Friends Science Publishers
Keywords:
Soybean;
Nitrate; Root system architecture; Foraging
Introduction
Nitrogen (N) is a primary mineral nutrient required in
huge quantity for plants to support plant growth and development, but it is
present in less quantity in natural and agricultural soils (Lark et al. 2004). There are various sources of
N like nitrate (NO3-), ammonium (NH4+),
organic amino acids and peptides that plants can absorb. Nitrate is the key
form of N found in both natural and agricultural soils which may act as a
signaling molecule that shapes the root system architecture (RSA) (Alboresi et al. 2005; Marín et
al. 2011; Alvarez et al. 2012). The NO3-
distribution and concentration are key players to determine the plant RSA
(Gruber et al. 2013;
Tian et al. 2014).
Roots are vital in
plant production as roots anchor plants in soil/growth medium, provide
mechanical support, ensure water and nutrient uptake, facilitate symbiosis
development and serve as storage organs in plants. The root elongation, lateral root branching as well as root angles, and
root longevity make the root system, while genetic, environmental, and
physiological factors are the major determinants of the root system (Lynch
and Brown 2012; Smith and Ive 2012). The RSA has developmental plasticity, which depends
upon immediate soil environments such as soil water status, soil nutrients,
soil temperature, soil pH, and soil microbes. As soil resources are distributed
unevenly, therefore, the RSA is crucial for agricultural productivity and is
the primary determinant of plant’s capacity for the acquisition of soil
resources (Lynch 1995).
The
plant’s ability to efficiently and quickly acquire the nutrients from natural
and agricultural soils determine the comparative success rate and production of
plants. As mineral nutrients interact in different ways, with each other and
with soil particles, or water may carry them out of the plant’s root range,
which cause nutrients availability decrease and lead to nutrient scarcity.
Therefore, plants activate their root foraging system to obtain nutrients from
nutrient-rich patches. Root foraging consists of morphological modifications
like RSA modulation or formation of root hairs, as well as physiological
changes like roots release exudates to mobilize nutrients or changes the
expression of nutrient transporters (Gojon et al. 2009; Hinsinger et al. 2009; Gruber et al. 2013). This root foraging enhances the interaction between root and soil and
improve the ability of plant to capture immobile nutrients. Plants symbiosis
with microbes also modifies RSA to some extent (Gutjahr and Paszkowski
2013).
Soybean
is a key oilseed crop with a rich source of protein. The global soybean yield
is increasing continuously and significantly since last several decades (FAO 2012; Kokubun 2013). Almost all
crops require a large amount of N in order to achieve higher production goals,
especially the legumes due to their higher seed protein content (Sinclair
and Wit 1976; Giller and Cadisch 1995). Soybean shoots accumulate on an average of 79 kg N ha−1
to gain additional Mg of seed with seed\ standard moisture content of 0.130 kg
H2O per kg seed (Salvagiotti et al. 2008;
Tamagno et al. 2017).
The soybean crop rarely recieves N fertilizer provided by farmers except for a
starter dose of N that is applied at sowing time, to meet early seedling
emergence/germination stage requirement until nodulation takes place. The
investigation indicates whether soil N mineralization and N fixation can meet
the N requirement for a seed yield of 6 to 8 Mg per hectare under well-managed
field conditions (Menza et al. 2017). However, the effect of
nitrate deficiency on seedling growth in the early seedling stage before
nodulation has not been reported. Therefore, the present study examined the (a)
effects of high nitrate supply or its deprivation on seedling establishment and
root system architecture, and (b) variations in root foraging in soybean in
response to nitrate application.
Materials and Methods
Seed selection, sterilization and sowing
The experiment was conducted using soybean (Glycine max L) variety Williams 82.
Healthy and uniform seeds were selected and sterilized using bleach containing
5% sodium hypochlorite and hydrochloric acid in a ratio of 10:1(v/v). Briefly,
the bleach was taken in a beaker and placed below the porous plate of a glass
desiccator apparatus, while, seeds were placed in petri dishes in a single
layer kept above the porous plate of the glass desiccator. To avoid evaporation
from the glass desiccator apparatus, the lid was closed using wax and left it
in a fume hood overnight. After sterilization, seeds were soaked in tap water
for 3 h, and the imbibed seeds were sown in trays for germination till 7 days.
Experimental treatments
The physiological experiment was comprised of two
treatments viz., with and without KNO3,
which started from the first day of sowing. The treatment with KNO3
was named as high nitrate (54.3 mM)
(N1) while without KNO3 was named as no nitrate (0 mM) (N0). One more treatment
was added for the nitrate content analysis experiment. This treatment was name
as optimum nitrate (18.81 mM). The
KCl was used to make up the concentration of K across three treatments. The
nutrient medium was liquid MS with little modification that NH4NO3,
sucrose, and agar were not used while the additional amount of KCl was used in
N0 treatment, to compensate additional potassium added as KNO3
in high nitrate treatment. The pH of the solution was adjusted to 5.8 with NaOH
solution. After 7 days, seedlings were transplanted into other trays having the
same concentration of MS medium solution and replicated three times. The MS
solution was changed every 5th day.
Growth environment
The experiment was conducted in a growth chamber
(RXZ-500D, model number JN181018, Ningbo Jiangnan Instrument Co., Ltd., Ningbo,
China), with day/night duration of 16/8 h with a relative humidity of 60% and
day/night temperature of 25°C. Data were collected after 4 weeks of sowing.
Gas exchange attributes
Photosynthesis and other gas exchange attributes were
recorded inside the growth chamber using Portable Photosynthesis Instrument
(LI-6400XT; LI-COR Inc., Lincoln, NE, U.S.A.). The light source was red-blue
LED, having 1000 µmol m-2
s-1 light intensity and carbon dioxide concentration of 399 ± 9.45
µmol mol-1. The leaf temperature was kept at 25°C. The first trifoliate leaf was used to record
photosynthesis data and each reading was recorded at a steady state. The SPAD
value was also measured with an SPAD meter before start to each photosynthesis
measurement.
Root and shoot growth attributes
Root and shoot lengths were measured in centimeters (cm).
After measuring the primary root and shoot length, root and shoot fresh biomass
were measured with a digital electric weighing balance (LS220A, Precisa, Shanghai, China). Tissue papers were used to
absorb the water present on the root surface before recording the fresh
biomass. The same roots were packed in plastic bags and kept in the
refrigerator at 4°C to measure the other root parameters. The complete roots of
each plant were scanned with a root scanner (Epson Expression 1680 Scanner,
Seiko Epson Co., Japan), and total root length, root surface area, root
diameter, root volume, root tips, forks, and crossings were determined through
the Root Analyzer (Regent Instruments Inc., Quebec, Canada). Both shoot and
root samples were packed in paper envelopes and kept in an oven at 80°C for 5
days until constant count, and their dry biomass was recorded with a digital
electric weighing balance (LS220A, Precisa, Shanghai,
China).
Leaf attributes
After measuring the fresh biomass of shoots, all leaves
of each plant were separated and the leaf area was measured by LI-3100C leaf
area meter (LI-COR Inc., Lincoln, NE, USA). Then leaf samples were oven-dried
at 80°C for 5 days and leaf dry biomass was recorded with a
digital electric weighing balance. The leaf biomass per area (LMA) was
determined by dividing leaf dry mass with leaf area. The single leaf area was
calculated by dividing the whole leaf area with the number of total leaves on each
plant.
Nitrate assay for soybean tissues
The salicylic acid method was used to evaluate the
nitrate content in soybean root, stem and leaf tissues (Zhao and Wang 2017).
Briefly, 0.1 g of fresh soybean tissues was grinded into powder by liquid
nitrogen using a Tissuelyser-96 (Jingxin, Shanghai, China).
A 1 mL of deionized water was added into the tubes and the mixture was placed
in a water bath at 100 °C for 30 min. The 0.1 mL supernatant and 0.4 mL
salicylic acid-sulphuric acid was used for incubating the reaction. After
adding 9.5 mL of 8% (w/v) NaOH solution into each tube, the tubes were cool
down to room temperature (20–30 min), the OD410 value of each sample was
measured with a visible light spectrophotometer (NanoReady FC-1100, Suizhen, Hangzhou, China) with the control (deionized
water) for reference. The nitrate content were
calculated using the following equation: nitrate concentration (μg/g) = (nitrate content in the
standard curve × the total volume of extracted sample) / (test amount of sample
solution × weight of the sample).
Statistical analysis
Statistical analysis was performed using Statistics 8.1
software and completely randomized design with three replicates to assess
treatment differences.
Results
Effect of nitrate treatments on the root and shoot traits
The effect of nitrate treatment was significant on the
primary root, shoot and plant length (Table 1). The primary root length was
significantly increased while shoot length decreased under no nitrate condition
compared to high nitrate treatment. In addition, plant length was also
significantly decreased under high nitrate treatment. The primary root length
showed a higher increase (42.5%) than the total plant length (14.8%) while the
shoot length decreased by 17.2% under no nitrate condition compared
to high nitrate treatment.
Root fresh biomass
was higher while shoot and plant fresh biomass was lower under no nitrate
condition compared to high nitrate treatment (Table 1). Compared with high
nitrate treatment, root fresh mass was significantly increased by 20.0% while
shoot and plant fresh biomasses decreased under no nitrate condition
by 64.9 and 33.1%, respectively.
The effect of
nitrate supply on shoot dry biomass was significant. As shown in Table 1, the
shoot dry biomass was significantly decreased by 21.4% under no nitrate
condition compared to high nitrate treatment. Although, there was no
significant difference in root and plant dry biomass between nitrate
treatments, root dry biomass increased 8.2% and plant dry biomass decreased 16.0%
under no nitrate condition compared to high nitrate treatment.
Effect of nitrate treatment on gas exchange attributes
The single leaf area was significantly reduced by 25.8%
in no nitrate treatment against high nitrate condition (Table 2). Leaf dry mass
per area was higher in control without nitrate supply than high nitrate treatment
which increased by 29.8%. The SPAD value of no nitrate treatment was
significantly lower than high nitrate treatment by 25.8%.
Photosynthesis (A) significantly increased by 130.7% in
high nitrate treatment compared with no nitrate condition. The inhibition rate of stomatal conductance (gs) was the
highest (154.9%) amongst in photosynthetic traits. Compared with high nitrate treatment,
gs decreased significantly under no nitrate treatment. No
significant treatment effect was found for intercellular CO2
concentration (Ci). However, a significant treatment effect was
observed in the transpiration rate (Tr), and the Tr of high nitrate treatment recorded 117.3% higher than no nitrate treatment.
The effect of nitrate treatment on root system architecture
The effect of nitrate
treatment on root related parameters was significant. The total root length was
25.7% higher under no nitrate condition than high nitrate supply condition
(Table 3). Root surface area was increased by 16.9% under no nitrate treatment
compared with high nitrate treatment. Contrary to total root length and root
surface area, root diameter of no nitrate treatment was significantly lower
than high nitrate treatment. The root volume of high nitrate treatment was
increased by 7.5% compared with no nitrate treatment; but the effect was not
statistically significant. Root tips, forks, and crossings also showed
significant variations in response to nitrate treatment. Under no nitrate
treatment, root crossings had the highest increment (32.9%), followed by root
tips (30.6%) and root forks (23.6%).
The nitrate uptake under
different nitrate concentration
To reveal the nitrate uptake
in soybean, we evaluate the nitrate content in roots, stem and leaf under low (6.27 mM), optimum (18.81 mM), and high (54.3 mM)
nitrate treatments. The nitrate content in root tissue increased with the
increase of nitrate concentration in solution. The higher nitrate content was
found under high nitrate treatment. No significant difference was found between
low and optimal nitrate content. In addition, there was no
significant difference on the effects of the three treatments on soybean stem
and leaf tissues, although optimal nitrate treatment had highest nitrate
content both in leaf and stem tissues of soybean (Table 4).
Discussion
Table 1: Effect of nitrate supply on
shoot and root growth attributes of soybean variety Wm 82
Traits
Name (Units) |
ANOVA |
Treatments (Means ± SE) |
Difference
(%) |
|
Growth
related |
|
N0
(KNO3 = 0 mM) |
N1
(KNO3 = 54.3 mM) |
|
Primary
root length (cm) |
*** |
34.15
± 0.97a |
19.63
± 0.57b |
-42.5 |
Shoot
length (cm) |
*** |
29.49
± 0.68b |
34.56
± 0.65a |
17.2 |
Plant
length (cm) |
*** |
63.64
± 1.07a |
54.19
± 0.94b |
-14.8 |
Root
fresh biomass (g) |
*** |
1.69
± 0.12a |
1.35
± 0.14b |
-20.0 |
Shoot
fresh biomass (g) |
*** |
2.82
± 0.18b |
4.65
± 0.36a |
64.9 |
Plant
fresh biomass (g) |
*** |
4.51
± 0.26b |
6.00
± 0.49a |
33.1 |
Root
dry biomass (g) |
ns |
0.09
± 0.006a |
0.08
± 0.009a |
-8.2 |
Shoot
dry biomass (g) |
* |
0.41
± 0.03b |
0.50
± 0.05a |
21.4 |
Plant
dry biomass (g
seedling-1) |
ns |
0.50
± 0.031a |
0.58
± 0.054a |
16.0 |
Data are presented as mean ± SE
of three replications. Mean values followed by the same letters are
non-significant at P < 0.05
ANOVA was used to test the significance of nitrate treatment. *, ** and
*** show significance at P < 0.05,
P < 0.01, and P < 0.001 levels, respectively, and ns shows non-significance at
P ≥ 0.05 level
The difference of each parameter between two treatments was calculated
from the given equation, (N1-N0/N0)*100
Table 2: Effect of nitrate supply on
leaf and photosynthesis-related attributes of soybean variety Wm 82
Photosynthesis-related |
ANOVA |
Treatments
(Means ± SE) |
Difference (%) |
|
Traits Name (Units) |
|
N0 (KNO3 =
0 mM) |
N1 (KNO3 =
54.3 mM) |
|
Single leaf area (cm2) |
** |
20.70 ± 1.70b |
26.04 ± 1.90a |
25.8 |
Leaf dry biomass/area (gcm-2) |
*** |
21.46 ± 0.018a |
15.07 ± 0.013b |
-29.8 |
Soil plant analysis development |
*** |
18.30 ± 0.61b |
23.02 ± 0.52a |
25.8 |
Photosynthesis (μmol m−2 s−1) |
*** |
5.11 ± 0.25b |
11.78 ± 0.28a |
130.7 |
Stomatal conductance (mol m−2 s−1) |
*** |
0.08 ± 0.008b |
0.20 ± 0.012a |
154.9 |
Intercellular CO2concentration (μmol mol−1) |
ns |
271 ± 6.12a |
271 ± 6.66a |
0.2 |
Leaf transpiration rate (mmol m−2
s−1) |
*** |
1.15 ± 0.11b |
2.49 ± 0.12a |
117.3 |
Data are presented as mean ± SE
of three replications. Mean values followed by the same letters are
non-significant at P < 0.05
ANOVA was used to test the significance of nitrate treatment. *, ** and
*** show significance at P < 0.05,
P < 0.01, and P < 0.001 levels, respectively, and ns shows non-significance at
P ≥ 0.05 level
The difference of each parameter between two treatments was calculated
from the given equation, (N1-N0/N0)*100
Under optimal growth conditions, plants
usually have a lower root to shoot ratio as these distribute more
photosynthates to above-ground plant parts, resulting
in the accumulation of above-ground biomass. Nevertheless, plant growing under
N deficit conditions always have a higher root to shoot ratio, which indicates
that above-ground plant parts were more affected by N deficiency than the
underground roots (Ruggiero and Angelino 2007; Zhang et al. 2009;
Lima et al. 2010; Ju and Christie 2011).
Similarly, researchers reported that moderate N fertilization favored root
growth of winter wheat while higher N supply resulted in reduced root growth in
subsoil (Svoboda 2006). Low N
availability increased root dry biomass (Wang et al. 2009). Similar results were observed in present study as
primary root length, root fresh biomass, and root dry biomass were increased
while shoot length, shoot fresh mass, root dry mass (Table 1) and leaf expansion (Table 2) were decreased under
no nitrate treatment due to reduction in
photosynthesis.
The roots with longer root length and greater surface areas have
resistance to nutrient diffusion, and explore higher soil volume to uptake N
under low NO3- concentrations (Engels and Marschner 1995; Lawlor 2002). In present study, higher primary root length, total root length, root
surface area, root volume, number of root
tips, forks and crossings (Table 3) were observed under no nitrate treatment
than high nitrate treatment. Because NO3- acts as an
essential nutrient that limits growth and a key signaling molecule for gene
expression, plant metabolism, plant growth and development, leaf expansion,
root architecture, flowering time, and seed dormancy (Scheible et al. 2004; Zhang et al. 2007; Vidal
and Gutiérrez 2008; Gojon et al. 2009; Krouk et al. 2010). Therefore, both primary root length
and lateral root length increased (Table 1 and 3) under no nitrate environment
that is consistent with previous results since NO3-
deficient environment promotes primary root elongation and stimulates lateral
root growth by regulating auxin activity (Vidal et al.
2010).
The NRT1.1 or CHL1 is a dual
affinity transporter, while NRT 2.1 is a high-affinity transporter under low NO3- availability.
It has been reported in Arabidopsis
that both are involved in nitrate acquisition from the soil solution. In addition, mutation
studies have shown that these transporters are either indirectly or directly Table 3: Effect of nitrate supply on root architecture of
soybean variety Wm 82
Traits Name (Units) |
ANOVA |
Treatments
(Means ± SE) |
Difference (%) |
|
Root related |
|
N0 (KNO3 =
0 mM) |
N1 (KNO3 =
54.3 mM) |
|
Total root length (cm) |
*** |
1156 ± 79a |
859 ± 66b |
-25.7 |
Root surface area (cm2) |
** |
145 ± 10.58a |
120 ± 10.35b |
-16.9 |
Root diameter (mm) |
* |
0.40 ± 0.007b |
0.48 ± 0.037a |
19.1 |
Root volume (cm3) |
ns |
1.45 ± 0.12a |
1.35 ± 0.13a |
-7.0 |
Root tips (no) |
*** |
1146 ± 94a |
796 ± 59b |
-30.6 |
Root forks (no) |
** |
3105 ± 288a |
2371 ± 290b |
-23.6 |
Root crossings (no) |
*** |
686 ± 76a |
460 ± 50b |
-32.9 |
Data are presented as mean ± SE
of three replications. Mean values followed by the same letters are non-significant at P < 0.05
ANOVA was used to test the significance of nitrate treatment. *, ** and
*** show significance at P < 0.05,
P < 0.01, and P < 0.001 levels, respectively, and ns shows non-significance at
P ≥ 0.05 level
The difference of each parameter between two treatments was calculated
from the given equation, (N1-N0/N0)*100
Table 4: Effect of nitrate supply on
nitrate uptake of soybean variety Wm 82
Nitrate Concentration |
Root (μg/g) |
Stem (μg/g) |
Leaf (μg/g) |
Low nitrate (6.27 mM) |
52.35 ± 5.10b |
91.20 ± 15.87a |
70.07 ± 3.78a |
Suitable nitrate (18.81 mM) |
68.80 ± 14.94b |
102.02 ± 12.50a |
78.89 ± 11.76a |
High nitrate (54.3 mM) |
107.62 ± 20.43a |
85.40 ± 16.85a |
64.47 ± 15.93a |
Data are presented as mean ± SE of three replications. Values followed
by different lowercase letters within different treatments are significantly
different according to LSD test (P
< 0.05)
involved in NO3- signaling (Muños et al. 2004; Little et al. 2005; Remans et al. 2006; Ho et al. 2009; Wang et al. 2009, 2020). It was speculated that these
transporters might also be present as a signaling molecule to promote root
growth and reduce shoot growth in soybean under no or low nitrate condition
(Table 1 and 2). However, the low affinity
transporters family are active under high availability of nitrate (Krapp et
al. 2011; Kotur et al. 2012; Gu et al. 2013,
2014; Léran et al. 2014; Liu et al. 2014). For example, high nitrate treatment promotes shoot growth and
reduces root growth in the present study (Table 1 and 2).
Plant roots could sense nutrient concentration in the
soil environment, increase nutrient uptake or its assimilation systems, as well
as proliferate in nutrient-rich areas. This phenomenon is known as local
signaling. On the other hand, when plant internal nutrient availability becomes
inadequate, this phenomenon boosted the whole plant system, which is called
systemic signaling (Schachtman and Shin 2007). This dual system regulation
controls nutrients, such as NO3-, which is one
of the most growth-limiting nutrients. The current model of dual regulation
indicates that root growth or development and NO3- transport are
regulated by (i) NO3- itself locally and (ii) by reduced N metabolites
through systemic feedback repression (Zhang et al. 1999; Gojon et al.
2009). The experimental results are in accordance where plants under the
absence of local N (N0) increased root foraging by increasing root
related parameters while under higher dose/presence of local N (N1)
reduced root growth and development (Tables 1 and 3). In addition, the
reduction of photosynthesis metabolism due to less photosynthetic
enzymes/components and activities revealed the feedback suppression of the
system under no nitrate condition.
When plant roots
face N deficiency, the root system architecture behaves in two ways based on
the degree of N deficiency (Giehl et al. 2012). The survival strategy in
a severe N deficiency environment constitutes elongation of primary and lateral
roots as well as inhibition of new lateral roots (Giehl et al. 2012; Giehl and Wirén 2014). This kind of adaptation depends upon a regulatory
module along with the NRT1.1 dependent auxin removal from primordia of lateral
roots (Araya et al. 2014, 2016). The
relatively mild N deficiency rather than severe N limitation stimulates the
lateral root emergence as well as primary and lateral root elongation
particularly (Gruber et al. 2013; Giehl and Wirén 2014; Ma et al. 2014). This stimulatory
response is an interesting strategy, in which roots enhance soil foraging
volume is known as the foraging strategy. The
upregulation of the auxin biosynthesis gene TAR2
was observed under low N conditions. Under mild N deficiency environment, tar2 mutant showed inhibition in
lateral root emergence , thus auxin is considered to be an active role player (Ma
et al. 2014). However, as primary and
lateral root length of tar2 mutant
was not affected, so TAR2-dependent auxin biosynthesis alone fails to explain
the root elongation stimulation mechanism under mild N deficiency. In present
study, soyeban root foraging strategy was found under severe nitrate deficiency
as primary root length, total root length, and all other root related
parameters showed increment except root diameter (Table 1 and 3). Further
studies are needed to investigate the genetic behavior of root and shoot growth
under excessive and deficient nitrate environments in soybean.
Conclusion
The NO3- deprivation or high dose/presence is
a signal to monitor plant growth in soybean in the early growth stage before
nodulation. The deprivation of NO3- promoted root growth
in search of NO3- and showed a decrease in above-ground
plant parts through local and systemic signaling. Similarly, the high
dose/presence of NO3- promoted shoot growth and showed a
decrease in root growth through local and systemic signaling. High nitrate supply significantly enhanced the
nitrate contents in root tissue, but there was no significant difference
between low and optimal nitrate supply. In summary, soybean roots act as plant
foraging organs under NO3- absence
environment.
Acknowledgement
This study was supported by Project
of Special Funding for Crop Science Discipline Development of Yangzhou
University (yzuxk202006).
Author Contributions
MT and LS designed experiment and wrote
manuscript. YD, ZP, LC, MS helped in performing experiments and analyzing data.
MA and GZ helped in revising manuscript.
Conflict of Interest
We declare that the authors have no
competing interests as defined by Nature Research, or other interests that
might be perceived to influence the results and/or discussion reported in this
paper.
Data
Availability
All data will be available upon reasonable request to the
corresponding author.
Ethics
Approval
Not applicable.
References
Alboresi A, C Gestin, MT
Leydecker, M Bedu, C Meyer, HN Truong (2005). Nitrate, a signal relieving seed
dormancy in Arabidopsis. Plant Cell Environ 28:500‒512
Alvarez JM, EA Vidal, RA Gutiérrez (2012). Integration of local and
systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15:185‒191
Araya T, NV Wirén, H Takahashi (2016). CLE peptide signaling and
nitrogen interactions in plant root development. Plant Mol Biol 91:607‒615
Araya T, M Miyamoto, J Wibowo, A Suzuki, S Kojima, YN Tsuchiya, S Sawa,
H Fukuda, N von Wirén, H Takahashi (2014). CLE-CLAVATA1 peptide-receptor
signaling module regulates the expansion of plant root systems in a
nitrogen-dependent manner. Proc Natl Acad Sci 111:2029‒2034
Engels C, H Marschner (1995). Plant uptake and utilization of nitrogen.
In: Nitrogen Fertilization in the
Environment, pp:41‒81. Bacan PE (Ed.). Marcel Dekker, Inc., New York, USA
FAO STAT (2012). Soybean production Indices. Available at: http://www.fao.org/faostat/en/#data/QI
Giehl RF, NV Wirén (2014). Root nutrient foraging. Plant Physiol 166:509‒517
Giehl RF, JE Lima, NV Wirén (2012). Localized iron supply triggers
lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin
distribution. Plant Cell 24:33‒49
Giller KE, G Cadisch (1995). Future benefits from biological nitrogen
fixation: An ecological approach to agriculture. In: Management of Biological
Nitrogen Fixation for the Development of more Productive and Sustainable
Agricultural Systems, pp:255‒277. Ladha JK, MB Peoples (eds.). Developments
in Plant and Soil Sciences, Springer, Dordrecht, The Netherlands
Gojon A, P Nacry, JC Davidian (2009). Root uptake regulation: A central process
for NPS homeostasis in plants. Curr Opin
Plant Biol 12:328‒338
Gruber BD, RF Giehl, S Friedel, NV Wirén (2013). Plasticity of the Arabidopsis root system under nutrient
deficiencies. Plant Physiol 163:161‒179
Gu C, X Zhang, J Jiang, Z
Guan, S Zhao, W Fang, Y Liao, S Chen, F Chen (2014). Chrysanthemum CmNAR2 interacts with CmNRT2 in the control of
nitrate uptake. Sci Rep 4; Article 5833
Gu R, F Duan, X An, F Zhang,
NV Wirén, L Yuan (2013). Characterization of
AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515‒1524
Gutjahr C, U Paszkowski (2013). Multiple control levels of root system
remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci 4; Article 204
Hinsinger P, AG Bengough, D Vetterlein, IM Young (2009). Rhizosphere: Biophysics,
biogeochemistry and ecological relevance. Plant
Soil 321:117‒152
Ho CH, SH Lin, HC Hu, YF Tsay (2009). CHL1 functions as a nitrate
sensor in plants. Cell 138:1184‒1194
Ju X, P Christie (2011). Calculation of theoretical nitrogen rate for
simple nitrogen recommendations in intensive cropping systems: A case study on
the North China Plain. Field Crops Res 124:450‒458
Kokubun M (2013). Genetic and cultural improvement of soybean for
waterlogged conditions in Asia. Field
Crops Res 152:3‒7
Kotur Z, N Mackenzie, S
Ramesh, SD Tyerman, BN Kaiser, AD Glass (2012).
Nitrate transport capacity of the Arabidopsis
thaliana NRT2 family members and their interactions with AtNAR2. 1. New Phytol 194:724‒731
Krapp A, R Berthomé, M Orsel,
S Mercey-Boutet, A Yu, L Castaings, S Elftieh, H Major, JP Renou, F
Daniel-Vedele (2011). Arabidopsis
roots and shoots show distinct temporal adaptation patterns toward nitrogen
starvation. Plant Physiol 157:1255‒1282
Krouk G, NM Crawford, GM Coruzzi, YF Tsay (2010). Nitrate signaling: Adaptation
to fluctuating environments. Curr Opin
Plant Biol 13:265‒272
Lark RM, AE Milne, TM
Addiscott, KWT Goulding, CP Webster, S O'Flaherty (2004). Scale‐and location‐dependent
correlation of nitrous oxide emissions with soil properties: An analysis using
wavelets. Eur J Soil Sci 55:611‒627
Lawlor DW (2002). Carbon and nitrogen assimilation in relation to
yield: Mechanisms are the key to understanding production systems. J Exp Bot 53:773‒787
Léran S, K Varala, JC Boyer,
M Chiurazzi, N Crawford, F Daniel-Vedele, L David, R Dickstein, E Fernandez, B
Forde, W Gassmann, D Geiger, A Gojon, JM Gong, BA Halkier, JM Harris, R
Hedrich, AM Limami, D Rentsch, M Seo, YF Tsay, M Zhang, G Coruzzi, BA Lacombe (2014). A unified nomenclature of
NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5‒9
Lima JE, S Kojima, H Takahashi, NV Wirén (2010). Ammonium triggers
lateral root branching in Arabidopsis
in an Ammonium transporter 1; 3-dependent manner. Plant Cell 22:3621‒3633
Little DY, H Rao, S Oliva, F
Daniel-Vedele, A Krapp, JE Malamy (2005).
The putative high-affinity nitrate transporter NRT2.1 represses lateral
root initiation in response to nutritional cues. Proc Natl Acad Sci 102:13693‒13698
Liu X, D Huang, J Tao, AJ
Miller, X Fan, G Xu (2014). Identification
and functional assay of the interaction motifs in the partner protein O s NAR
2.1 of the two‐component system for high‐affinity nitrate transport. New
Phytol 204:74‒80
Lynch J (1995). Root architecture and plant productivity. Plant Physiol 109:7‒13
Lynch JP, KM Brown (2012). New roots for agriculture: Exploiting the
root phenome. Phil Trans Roy Soc B Biol Sci 367:1598‒1604
Ma W, J Li, B Qu, X He, X
Zhao, B Li, X Fu, Y Tong (2014). Auxin biosynthetic gene TAR 2 is involved in
low nitrogen‐mediated reprogramming of root architecture in Arabidopsis. Plant J 78:70‒79
Marín IC, I Loef, L Bartetzko, I Searle, G Coupland, M Stitt, D Osuna (2011). Nitrate regulates floral induction in Arabidopsis, acting independently of
light, gibberellin and autonomous pathways.
Planta 233:539‒552
Menza NCL, JP Monzon, JE Specht, G Patricio (2017). Is soybean yield
limited by nitrogen supply? Field Crops
Res 213:204‒212
Muños S, C Cazettes, C Fizames, F Gaymard, P Tillard, M Lepetit, L Lejay, A
Gojon (2004). Transcript
profiling in the chl1-5 mutant of Arabidopsis
reveals a role of the nitrate transporter NRT1.1 in the regulation of another
nitrate transporter, NRT2.1. Plant Cell 16:2433‒2447
Remans T, P Nacry, M Pervent, S Filleur, E Diatloff, E Mounier, P
Tillard, BG Forde, A Gojon (2006). The
Arabidopsis NRT1.1 transporter participates
in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci 103:19206‒19211
Ruggiero C, G Angelino (2007). Changes of root hydraulic conductivity
and root/shoot ratio of durum wheat and barley in relation to nitrogen
availability and mercury exposure. Ital J
Agron 3:281‒290
Salvagiotti F, KG Cassman, JE
Specht, DT Walters, A Weiss, A Dobermann (2008). Nitrogen uptake, fixation and
response to fertilizer N in soybeans: A review. Field Crops Res 108:1‒13
Schachtman DP, R Shin (2007). Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47‒69
Scheible WR, R Morcuende, T
Czechowski, C Fritz, D Osuna, N Palacios-Rojas, D Schindelasch, O Thimm, MK
Udvardi, M Stitt (2004). Genome-wide
reprogramming of primary and secondary metabolism, protein synthesis, cellular
growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483‒2499
Sinclair TR, CTD Wit (1976). Analysis of the carbon and nitrogen
limitations to soybean yield. Agron J 68:319‒324
Smith S, DS Ive (2012). Root system architecture: Insights
from Arabidopsis and cereal crops. Phil
Trans Roy Soc B Biol Sci 367:1441‒1452
Svoboda PH (2006). The effect of nitrogen fertilization on root
distribution of winter wheat. Plant Soil
Environ 52:308
Tamagno S, GR Balboa, Y
Assefa, P Kovács, SN Casteel, F Salvagiotti, FO García, WM Stewart, IA
Ciampitti (2017). Nutrient partitioning and stoichiometry in soybean: A
synthesis-analysis. Field Crops Res 200:18‒27
Tian H, ID Smet, Z Ding (2014). Shaping a root system: Regulating
lateral versus primary root growth. Trends
Plant Sci 19:426‒431
Vidal EA, RA Gutiérrez (2008). A systems view of nitrogen nutrient and
metabolite responses in Arabidopsis. Curr Opin Plant Biol 11:521‒529
Vidal EA, V Araus, C Lu, G
Parry, PJ Green, GM Coruzzi, RA Gutiérrez
(2010). Nitrate-responsive miR393/AFB3 regulatory module controls root system
architecture in Arabidopsis thaliana.
Proc Natl Acad Sci 107:4477‒4482
Wang B, L Tao, QW Huang, Y Xing-Ming, S Qi-Rong (2009). Effect of N
fertilizers on root growth and endogenous hormones in strawberry. Pedosphere 19:86‒95
Wang W, H Bin, AF Li, CC Chu (2020). NRT1.1s in plants: Functions
beyond nitrate transport. J Exp Bot 71:4373‒4379
Zhang H, H Rong, D Pilbeam (2007). Signalling mechanisms underlying the
morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp
Bot 58:2329‒2338
Zhang H, A Jennings, PW Barlow, BG Forde (1999). Dual pathways for
regulation of root branching by nitrate. Proc
Natl Acad Sci 96:6529‒6534
Zhang X, S Chen, H Sun, Y Wang, L Shao (2009). Root size, distribution
and soil water depletion as affected by cultivars and environmental factors. Field Crops Res 114:75‒83
Zhao L, Y Wang (2017). Nitrate assay for plant tissues. Biochem Biophys Res Commun 43:1274–1279