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Article

Morphology and Nitrogen Uptake and Distribution of Wheat Plants as Influenced by Applying Remedial Urea Prior to or Post Low-Temperature Stress at Seedling Stage

by
Chunyan Li
1,2,*,†,
Mingmin Liu
1,2,†,
Cunhu Dai
1,2,
Yangyang Zhu
1,2,
Min Zhu
1,2,
Jinfeng Ding
1,2,
Xinkai Zhu
1,2,
Guisheng Zhou
1,3 and
Wenshan Guo
1,2
1
Jiangsu Key Laboratory of Crop Genetics and Physiology, Agricultural College of Yangzhou University, Yangzhou 225009, China
2
Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China
3
Joint International Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, Yangzhou 225009, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2022, 12(10), 2338; https://doi.org/10.3390/agronomy12102338
Submission received: 13 September 2022 / Revised: 23 September 2022 / Accepted: 24 September 2022 / Published: 28 September 2022
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Abstract

:
Wheat production is dramatically influenced by temperature. Low-temperature stress that frequently occurs seriously hampers the growth and development of wheat seedlings. In order to alleviate the damage of low temperature to wheat plant growth, remedial nitrogen was applied prior to or post low-temperature stress at seedling stage using controlled-temperature incubators to explore the difference in wheat morphology and nitrogen absorption and utilization efficiency. Nitrogen amendment significantly increased the leaf area, seedling height, tiller number and dry matter weight of wheat plants as compared with the treatment without nitrogen amendment under temperature stress. Remedial nitrogen applied prior to low-temperature stress (N-LT) was more conducive to increase the above parameters than that applied post low-temperature stress (LT-N). In addition, N-LT enhanced the ability of roots to absorb remedial 15N urea, promoted the growth and development of wheat plants under low-temperature stress, resulting in higher leaf SPAD readings, more new tillers, as well as increased dry weight of roots and above-ground organs. This study suggested that remedial nitrogen should be applied prior to low-temperature stress because it is more effective in restoring the growth of wheat plants under low-temperature stress.

1. Introduction

Wheat (Triticum aestivum L.) is the third largest cereal crop in the world behind corn and rice, with more than 700 million tons produced globally per year [1,2]. China is currently one of the major wheat-producing countries in the world, accounting for more than 18% of global wheat production. Good climate is often beneficial for enhancing higher wheat grain yield and better grain quality. However, extreme weather events have significantly increased over the past few decades, and will occur even more frequently in the future, which will pose a threat to global wheat production [3,4,5]. Freezing injury caused by cold waves with strong wind and low temperature is one of the main meteorological dangers in winter wheat production around the world [4,5,6,7].
Freezing injury during vegetative growth generally results in poor germination, leaf wilting, tiller damage, and lower seedling survival rate [8,9]. It was observed that mortality of winter wheat seedling was 9% per day, with the lasting duration of stress under average soil temperature of −12.5 °C during winter, and that grain yield and spike number decreased by 8.4% and 21.6% under stress lasting for 8 days [6]. Cold stress leads to dehydration of plant tissues and cellular membrane disintegration, commonly exhibiting water stress symptoms [10], which reduces root hydraulic conductivity [11], the length and biomass of root system and ultimately hampers the root and above-ground growth [12]. Additionally, branching angles between the primary root and lateral root of plants became smaller under low-temperature stress [13], resulting in lower contacting area with surface soils and lower absorption of nutrients and water [12]. The growth of the above-ground part of seedlings is also reduced due to the restricted supply of nutrients via roots under low-temperature stress [14,15].
Wheat plants respond to low-temperature stress via a series of physiological processes. These responses to coldness can be effectively adjusted by agronomic measures. Jouyban et al. [16] reported that changes in the levels of gene transcription and gene expression among different organs were the main responses of plants to low-temperature stress. For instance, high levels of expression of TaEXPB7-B in the tillering nodes enhanced the resistance of wheat plants to low temperature [17]. Several agronomic measures have been proved to mitigate the damage caused by low-temperature stress in wheat development [18]. For example, the treatment of wheat seeds with GA3 mitigated the low-temperature damage to germination [19]. Short-term cold acclimation can increase the activities of several enzymatic antioxidants in crops to mitigate the cellular oxidative damage [20,21]. This mitigation is beneficial for wheat plants to resist lower-temperature stress. In addition, exogenous application of nitrogen fertilizer can be effective in alleviating the adverse effects of low-temperature stress at tillering and elongation stages and reducing the yield loss of wheat because nitrogen fertilization can significantly improve the levels of antioxidants and maintain the balance of the hormones in wheat plants under low-temperature stress [22,23].
To date, a number of studies have been conducted to elucidate the adaptive responses of wheat plants to low-temperature stress. It is emphasized in these studies that nitrogen fertilization can regulate the growth of wheat plants after freezing injury and reduce the yield loss through various physiological mechanisms. Nevertheless, little focus has been laid on the differences in the growth and the nitrogen absorption and utilization efficiency of above-ground and underground parts of wheat plants between nitrogen application post and prior to low-temperature stress. We hypothesized that the effect of nitrogen applied prior to low-temperature stress might be better than that applied post low-temperature stress in promoting the recovery growth of wheat plants.
Therefore, the objectives of this study were: (1) to identify the changes in the morphology of wheat with remedial urea application post and prior to low-temperature stress at seedling stage; (2) to elucidate the differences in nitrogen absorption and utilization of wheat with urea amendment post and prior to low-temperature stress using labelled 15N; (3) to clarity the best timing of nitrogen application in alleviating the damage of cold stress to wheat seedlings.

2. Materials and Methods

2.1. Materials and Growth Conditions

This study was conducted at the Yangzhou University (32°23′ N, 119°25′ E) in Jiangsu Province, China. Two wheat varieties differing in cold sensitivity, spring wheat genotype Yangmai 25 and semi-winter wheat genotype Xumai 35 were selected. The same full-size seeds were selected and sterilized with 1% sodium hypochlorite for 3 min and washed with distilled water three times, and then germinated in incubation chamber for 36 h at a constant temperature of 25 °C. Square culture boxes (24 cm × 24 cm × 1.5 cm, L × W × H) were full of nutritional soil (1 kg soil per box). Two seedlings with radicle downwards were planted in the box with 2 cm soil covered. The transparent square culturing boxes were wrapped with tin-foil paper for shading and placed vertically in the low-temperature incubator (Model DLTM-1008C, Zhejiang, China). The normal temperature of the seedling was set at 25 °C/20 °C (day/night). The humidity was maintained at 70% RH, and light intensity was 300 μmol·m−2·s−1 in the incubator. Before seedling planting, 0.05 g urea (46.3% N) and 0.08 g compound fertilizer (N:P:K = 15:15:15%) were incorporated into the soil in the box. Enough water was supplied to ensure the wheat seedling grew normally without suffering drought stress. The overview of the experimental process is showed in Figure 1.

2.2. Experimental Design

Depending on the natural temperature variation, the temperature was set at 25 °C/20 °C (day/night) at germination, 20 °C/15 °C (day/night) during the 2-leaf stage, 15 °C/10 °C (day/night) during the 3-leaf stage, and 10 °C/5 °C (day/night) during the 4-leaf stage, respectively. Wheat seedlings were treated by low temperature during the 4-leaf stage. The low-temperatures regime was 4 °C/−3 °C (day/night) lasting for 4 days. The experiment was conducted in randomized-block design with two factors (cultivar × nitrogen and temperature combination). Each treatment had 3 replications and each replicate had 5 boxes, so 15 boxes in all per treatment. Nitrogen and temperature combination included: (1) seedlings under the normal temperature condition (NT); (2) seedlings under low-temperature stress (LT); (3) seedlings with 15N-labelled urea (46.3% N, 0.06 g per box) applied 3 days prior to low-temperature stress (N-LT); (4) and seedlings with the same amount of 15N-labelled urea applied on the end day of low-temperature stress (LT-N). The boxes were moved back to the normal-temperature incubators on 4th day after low-temperature treatment. 15N-labelled urea was produced by Shanghai Institute of Chemical Engineering, China.

2.3. Sampling and Measurement

2.3.1. SPAD Readings of Wheat Leaves

SPAD readings of the second fully expanded leaves was measured by a handheld chlorophyll meter (Nissan SPAD-502, Konica Minolta, Tokyo, Japan) on 0, 3, 8 and 14 days after low-temperature treatment. There were 3 replicates for each treatment.

2.3.2. Agronomic Traits

Plant height, leaf area as well as tiller number per plant were recorded on the 21st d after low-temperature stress. Plant samples were separated into roots and the above-ground part, dried to a constant weight at 80 °C, then weighed for the determination of the above-ground dry matter and root dry matter, respectively.

2.3.3. Root Phenotype

The roots of wheat plants were washed with distilled water on the 21st d after low-temperature stress, and then spread on the surface of a root scanner (Phantom 9900XL, Microtek, Shanghai, China) to obtain the scan images of roots. Root images were analyzed using Win RHIZO Pro software (2003b, Regent Instrument, Quebec, QC, Canada) to estimate total root length, root surface area, root volume, root average diameter, and root tip numbers.

2.3.4. Plant Nitrogen Content

The dry matter of wheat root, stem and sheath, as well as leaf were weighed on the 21st day after low-temperature stress. Nitrogen content in plant different organs were analyzed following Kjeldahl procedures (Kjeltec 8400, FOSS, Hoganas, Sweden). The 15N content in plant was analyzed by Shanghai Research Institute of Chemical Industry.
The following calculation were made based on total N and 15N content [24]:
(1) Nitrogen accumulation in an organ (mg/plant) = [nitrogen content in this organ × total dry matter of this organ];
(2) Percentage of N in plant derived from the 15N-labelled fertilizer (%) = [atom % 15N excess in plant/atom % 15N excess in the fertilizer];
(3) N accumulation derived from the 15N-labelled fertilizer (mg/plant) = [atom % 15N excess in plant × N accumulation amount of plant/atom % 15N excess in the fertilizer];
(4) Nitrogen absorption rate of each organ in plant (μg/d) = N accumulation in an plant organ/days after applying fertilizer.

2.4. Data Analysis

This study was arranged in a randomized-block experiment design of two factors. All the data were analyzed using DPS 7.05 Statistical Software (DPS, Zhejiang, China) and significant difference were defined as p < 0.05.

3. Results

3.1. Effects of Nitrogen Amendment Post or Prior to Low-Temperature Stress on SPAD Readings of Wheat Leaves

The SPAD readings of both Yangmai 25 and Xumai 35 leaves were significantly reduced on the end day of low-temperature treatment (Table 1). Compared with the NT treatment of each cultivar, SPAD readings decreased by 7.90% and 5.56% under low-temperature stress (LT) in Yangmai 25 and Xumai 35, respectively. The SPAD readings of the treatment with nitrogen amendment prior to low-temperature stress (N-LT) showed the decrease of 3.19% and 2.31% in both cultivars, while the SPAD readings of the treatment with nitrogen amendment post low-temperature stress (LT-N) showed the decrease of 8.39% and 5.02%. Results showed that nitrogen application prior to low temperature alleviated the damage of low-temperature stress to wheat plants to a significant larger degree than that post low-temperature stress.
The SPAD readings of nitrogen amendment treatments gradually increased on the 3rd day after low-temperature treatment. The increasing trend in LT-N was more pronounced than that in N-LT in both cultivars. Compared with that SPAD readings on the end day after low-temperature stress, the average of SPAD readings of both two varieties increased by average 3.58% under N-LT treatment and by average 7.55% under LT-N treatment, respectively. There was no significant difference in SPAD readings between nitrogen amendment treatments and NT treatment in both cultivars on the 3rd day post low-temperature stress.
On the 8th and 14th days after low-temperature stress, the SPAD readings of all the treatments still maintained the ascending tendency. On the 14th day after low-temperature treatment, there was no significant difference in the SPAD readings among the low-temperature treatments in Yangmai 25. For Xumai 35, the SPAD readings of nitrogen amendment treatments were higher than that under LT.

3.2. Effects of Nitrogen Amendment Post or Prior to Low-Temperature Stress on the Root Morphology of Wheat Plants

The morphology of the seedlings post low-temperature stress was shown in Figure 2. The roots of wheat seedlings were damaged more seriously post low temperature than that growing under the normal temperature conditions. Wheat grown under the normal temperature had more branching roots and denser root hair. However, the root hairs of two cultivars were significantly sparse on the 21st day post low-temperature stress. The total length, surface area, volume and tip number of root decreased by 49.15–73.53%. Meanwhile, these above parameters reduced by 32.03–53.82% in the N-LT treatment and 37.11–67.65% in the LT-N treatment, respectively, which were both lower than those in the NT treatment. Nitrogen amendment prior to low-temperature stress more remarkably alleviated the cold damage to wheat roots than that applied post stress (Figure 3).
Average root diameter was the least affected among these low-temperature treatments. Compared to NT, the root diameter decreased by 10.07% in Yangmai 15 and 18.65% in Xumai 35 under low-temperature treatment, respectively. Changes were 5.81% (N-LT) and 11.13% (LT-N) of two wheat varieties, respectively. Although nitrogen amendment may alleviate the stress from low temperature in some sense, it could not fully make the damaged root restore normal growth, just like the plant root growing under natural conditions. The response of the root average diameter of Xumai 35 to low temperature was significantly greater than that of Yangmai 25.

3.3. Effects of 15N Urea Amendment Post or Prior to Low-Temperature Stress on Nitrogen Accumulation and Distribution in Wheat Seedlings

The differences in nitrogen absorption and utilization efficiency of roots were observed due to the different timings of nitrogen application (Table 2). The percentages of nitrogen from the 15N-labelled urea in the roots, stems and leaves under the N-LT treatment were significantly higher than those under LT-N treatment. In the N-LT treatment, the percentage of nitrogen from the 15N-labelled urea in the roots, stems, leaves of the two varieties was 11.19–21.51%, with only 0.35–0.61% recorded in the LT-N treatment. Xumai 35 had significantly higher 15N percentage in all the organs than Yangmai 25 in the N-LT treatment. However, there was no difference in 15N percentage between the two varieties under LT-N treatment.
Nitrogen accumulation of the various organs followed the order of leaf > stem > root among all the treatments. The average nitrogen accumulation in leaves was 23.39 mg per plant, 2.32 times as much as that in the stems and 7.43 times as much as that in the roots. In both cultivars, nitrogen accumulations in the roots, stems and leaves of the N-LT treatment was significantly higher than those of the LT-N treatment.
The rate of 15N absorption by various organs also followed the order of leaf > stem > root among all the treatments. The N-LT treatment more significantly promoted the wheat plants to utilize the added nitrogen than LT-N treatment. The 15N accumulation and absorption rate of Yangmai 25 under N-LT treatment were increased by 28.5 times and 23 times as much as that under LT-N treatment, whereas for Xumai 35, they increased by 40.2 times and 23 times as much, respectively.

3.4. Effects of 15N Urea Amendment Prior to or Post Low-Temperature Stress on Agronomic Characteristics of Wheat Plant

Low-temperature stress induced significant reductions of 38.75% in leaf area per plant, 43.75% in tiller number per plant, and 15.16% in seedling height in both cultivars as compared to the control plants (Table 3). Nitrogen application, whether prior to or post low-temperature stress, promoted plant growth. The restoring effect of N-LT was increased to a further extent, compared with LT-N. Leaf area per plant, tiller number per plant, and seedling height under N-LT were merely reduced by average 17.44%, 19.21% and 5.55% in both cultivars, respectively, as compared with LT treatment.
Canopy dry weight and root dry weight decreased by 39.54% and 52.20% on average in the two cultivars, respectively, post low-temperature stress, as compared with the control. Nitrogen amendment before stress was also further benefit to restore wheat growth, resulting in higher dry weight both in root and canopy than nitrogen applied after stress. The correlation analysis of root surface area to leaf area, and root dry weight to canopy dry weight, were shown in Figure 4. Significant positive linear relations were found between root surface area and leaf area for both cultivars (A). Similarly, root dry weight and dry weight above ground had significantly positive relations (B).

4. Discussion

4.1. Response of Morphology to Remedial Nitrogen Prior to or Post Low-Temperature Stress at Seedling Stage

Changes in above-ground and underground morphology of wheat plants are obvious under low-temperature stress. Plant roots are more sensitive to low temperature than the above-ground organs, because of the particularity of root growth position [25]. It was reported that cold stress reduced the rate of root elongation in plant, resulting in a decrease in root length and in fresh and dry root weight [26,27]. We also observed the same phenomenon in our experiments (Figure 2). The damage to root by low-temperature stress became worse, with lower root tip number, root surface area as well as root dry matter. Therefore, normal water and nutrient uptake were disrupted [12].
Nitrogen is an important element to promote plant root growth, especially in high-yielding wheat production. It has also been proved to play a more important role in recovering the damaged root growth [28]. Our previous studies indicated that nitrogen amendment post low-temperature stress alleviated wheat yield loss caused by cold stress to a certain extent [22]. In this study, our results showed that nitrogen applied prior to or post low-temperature stress both promoted root growth as compared with the LT treatment without nitrogen amendment, which was beneficial to protect root from low-temperature stress and recover seedling growth faster, resulting in higher total root length, total root surface area and volume (Figure 3). Previous studies have found that topdressing nitrogen fertilizer at elongation stage significantly improved wheat activity, which was beneficial to root growth [29]. After moving the cold-damaged wheat seedlings to optimal temperature, remedial urea more significantly promoted root growth and stimulated the activity of glucose-6-phosphate dehydrogenase and malate dehydrogenase than the other two nitrogen forms: nitrates and ammonia [28]. These results suggest that urea can effectively help wheat seedling recover better post low temperature.
In this study, we confirmed the hypothesis that urea applied prior to low temperature can better work in the recovery of wheat growth as compared with the urea applied post low temperature. We found that the N-LT treatment had better root morphology parameters than the LT-N treatment (Figure 3). Longer root length, more root surface area and root hair, as well as thicker root diameters could make wheat seedling uptake water and nutrient element more effectively. In this study, the prevention treatment (N-LT) allowed the wheat root tissue to retain better growth than remediation treatment (LT-N). Compared with semi-winter wheat variety Xumai 35, spring wheat variety Yangmai 25 was more sensitively affected by low temperature. Furthermore, the protection and remediation effect of nitrogen amendment on Yangmai 25 were better than those on Xumai 35 under low-temperature stress.
Wheat root morphology determines the function of root, which affects the growth of above-ground organs. Prolonged exposure to low-temperature stress reduces the nutrient absorption and translocation of roots, which limits the supply of nutrients to the above-ground parts of the plants, ultimately resulting in decreased above-ground and root biomass [18]. In addition, wheat leaves experience physiological and biochemical reactions accordingly post low temperature, such as reduced synthesis of Rubisco subunit and chlorophyll content in wheat leaves [30], which limits the photosynthesis of wheat, and ultimately leads to leaf chlorosis and wilting [31]. Similarly, in the present study, the cold-damaged leaves of the two wheat varieties had significantly lower SPAD readings than that under normal-temperature treatment. The SPAD readings of leaves under N-LT was significantly higher than that under LT-N from the ending day of stress to the 8th day post low-temperature stress. Up to 14 days post low temperature, the SPAD readings of leaves under low-temperature stress gradually returned to the normal levels. These results indicated that the positive effects of urea amendment supply on root development were a contributing factor in improving N uptake during the recovery of wheat, especially for the N-LT treatment.
Low temperature damaged not only wheat root growth, but also above-ground growth, resulting in lower leaf number and photosynthetic areas [32]. It has been reported that the utilization of the absorbed light energy in electron transport in N-adequate plants was much higher than that in N-deficient plants [33]. It is also well evidenced that increasing nitrogen supply significantly enhanced both the above-ground and root growth, and the positive effects of nitrogen on above-ground growth were more pronounced [34]. We also observed the similar phenomenon in this study (Figure 2). The above-ground dry weight was positively correlated with root dry weight (Figure 4), which further indicated that nitrogen application both prior to and post low-temperature stress promoted the recovery and growth of root system and the above-ground leaves. Moreover, nitrogen application prior to low-temperature stress was more conducive to the recovery and growth of root system, and finally leaf area, tiller number and dry weight of above-ground parts were significantly increased, compared with the LT and LT-N treatments. Our results were in agreement with the report of Shah et al. [35], who reported that presoaking wheat seeds with ascorbic acid enhanced tiller number, chlorophyll content and yield under low temperature due to late sowing.

4.2. Changes in Nitrogen Uptake and Utilization with Remedial Fertilizer Prior to or Post Low-Temperature Stress at Wheat Seedling Stage

Nitrogen plays an important role in the utilization of absorbed light energy as well as photosynthetic carbon metabolism in plants. As one of the major agricultural practices in crop production, nitrogen management is considered to be helpful in improving cold tolerance in wheat [18]. Our results showed nitrogen amendment prior to or post low-temperature stress improved wheat cold tolerance to some extent. However, the N uptake amount of the two varieties was significantly different between urea application prior to low temperature and urea application post low temperature. Hence, in order to explore the different nitrogen absorption between the treatments with nitrogen applied prior to or post low-temperature stress, stable (N-15) isotope-labelled urea was used. Nitrogen content in the wheat plants was increased with increased nitrogen application rate by isotopic techniques [36]. From our results of 15N labelled urea amendment experiment, the percentage of total nitrogen from 15N urea was more than 10% higher under N-LT than that under LT-N, indicating that nitrogen applied prior to low temperature better mitigated the injury of wheat roots caused by low-temperature stress (Table 3). Our finding was in agreement with the reports by Azam et al. [37] and Hu et al. [38], who reported that better roots were conducive to the absorption and utilization of soil nitrogen and fertilizer. These results further confirmed our hypothesis from the perspective of nitrogen uptake and utilization that nitrogen application prior to low-temperature stress was more beneficial to recover wheat growth, as compared with the nitrogen post low-temperature stress.
The impacts of low temperature on growth rate differed among organs, with the greatest increase in the 15N absorption velocity in leaves, then followed by the shoot (Table 2), indicating that leaf growth recovered faster than other organs. After low-temperature stress, newly developed leaves were thicker and contained more cell layers, which likely contributed to the restoration of respiratory and photosynthetic rates [39]. It has also been tested that the relative growth rate of newly developed leaves was increased by around 50%, as compared with that of the earlier cold-injury leaves [40]. The recovery growth of above-ground parts requires both the stored N and new N uptake, while low-temperature stress could have influenced directly on nitrogen uptake or utilization. In the present study, the above-ground dry mass was significantly increased under N-LT, as compared with the LT-N. Additionally, N-LT treatment increased both the stored nitrogen in the wheat plants prior to low temperature and new nitrogen post low-temperature stress, which could supply more carbohydrates to the recovery of roots that contributing to N uptake in turn. These were different from the LT-N treatment. These differences may result from the fact that the enhanced nitrogen level in the soils caused by increased N supply and the enzymatic defense mechanisms in plants were earlier induced when the wheat plants were subject to stress [41], which helped the plants cope with low-temperature constraints.
Nitrogen absorption 15N rate of the two varieties with urea remedial was higher in the above-ground parts than that in roots under low-temperature stress (Table 3). It could be speculated that nitrogen (N) is an important component of chloroplasts, and the accumulation of nitrogen in the above-ground parts directly affects the photosynthesis of plants. This suggests that in large-scale winter wheat production, weather forecast should be frequently checked and topdressing nitrogen at tillering stage should be applied at the appropriate time prior to the occurrence of low-temperature stress. This practice will enhance the ability of wheat plants to deal with low-temperature disasters.

5. Conclusions

Low-temperature stress significantly decreased the total root length, total root surface area and root tip number of wheat plants at seedling stage. The leaf area, tillering number, seedling height and dry matter accumulation were also reduced on the 21st day after low-temperature stress. However, the SPAD readings of main stem leaves first decreased on the end day of low-temperature stress, then gradually returned to normal levels under normal temperature on the 14th day after low-temperature stress. Compared with the remedial urea applied post low-temperature stress, urea amended prior to low-temperature stress significantly mitigated the decreasing speed of the above parameters in wheat. Compared with LT-N and LT, N-LT was more conducive to the absorption and utilization of nitrogen by wheat plants, resulting in faster recovery of the growth and development of underground roots and above-ground organs. This study suggests that remedial nitrogen should be applied prior to low-temperature stress. Our research offered theoretical knowledge and practical approaches to minimize the damages of low temperature to wheat production.

Author Contributions

Conceptualization, C.L. and M.L.; formal analysis, M.L. and M.Z.; investigation, M.L. and Y.Z.; methodology, M.L. and C.D.; project administration, C.L. and W.G.; resources, J.D. and X.Z.; writing—original draft, C.L. and M.L.; writing—review and editing, G.Z. and W.G.; supervision, C.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by China National Key R & D Program (2016YFD0300107, 2017YFD0301205), Jiangsu Provincial Key R & D Program (BE2020319), Independent Innovative Agricultural Project of Jiangsu Province (CX(22)1001), Jiangsu Special Program for Morden Agriculture (2021), and Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Acknowledgments

We thank the editor and anonymous reviewers for their constructive comments.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02338 g001 550
Figure 1. Overview of the experimental process.
Figure 1. Overview of the experimental process.
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Agronomy 12 02338 g002 550
Figure 2. Plant morphology under NT, LT, N-LT and LT-N treatments on the 21st day post low-temperature stress. NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low temperature at 4-leaf stage; LT-N, Application of 15N urea post low temperature at 4-leaf stage.
Figure 2. Plant morphology under NT, LT, N-LT and LT-N treatments on the 21st day post low-temperature stress. NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low temperature at 4-leaf stage; LT-N, Application of 15N urea post low temperature at 4-leaf stage.
Agronomy 12 02338 g002
Agronomy 12 02338 g003 550
Figure 3. Total root length (A), number of root tips (B), total root average diameter (C), root surface area (D), and total root volume (E) of Yangmai 25 and Xumai 35 among the different treatments. Vertical bars denote standard error of mean, and different letters were significantly different at p ≤ 0.05 probability level. NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low-temperature stress at 4-leaf stage; LT-N, Application of 15N urea post low-temperature stress at 4-leaf stage.
Figure 3. Total root length (A), number of root tips (B), total root average diameter (C), root surface area (D), and total root volume (E) of Yangmai 25 and Xumai 35 among the different treatments. Vertical bars denote standard error of mean, and different letters were significantly different at p ≤ 0.05 probability level. NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low-temperature stress at 4-leaf stage; LT-N, Application of 15N urea post low-temperature stress at 4-leaf stage.
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Agronomy 12 02338 g004 550
Figure 4. Correlation analysis of root surface area to leaf area (A), and root dry weight to above-ground dry weight (B) of Yangmai 25 and Xumai 35.
Figure 4. Correlation analysis of root surface area to leaf area (A), and root dry weight to above-ground dry weight (B) of Yangmai 25 and Xumai 35.
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Table
Table 1. Effects of remedial urea applied post or prior to low temperature on SPAD readings of wheat leaves.
Table 1. Effects of remedial urea applied post or prior to low temperature on SPAD readings of wheat leaves.
CultivarTreatmentDays Post Low-Temperature Stress
0 d3 d8 d14 d
Yangmai 25NT44.80 bc45.11 b46.00 cd56.50 a
LT41.26 e43.04 c44.96 d54.17 b
N-LT43.37 d45.10 b46.86 bcd54.79 ab
LT-N41.04 e44.01 bc47.40 bc55.10 ab
Xumai 35NT46.23 a46.89 a47.20 bc55.20 a
LT43.66 cd44.31 bc46.51 bcd50.89 b
N-LT45.16 ab46.59 a48.31 b53.63 ab
LT-N43.91 cd47.36 a50.10 a54.81 a
NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low temperature at 4-leaf stage; LT-N, Application of 15N urea post low temperature at 4-leaf stage; The data in the same column followed by different letters are significantly different at the 0.05 probability level.
Table
Table 2. Effects of 15N urea amendment post or prior to low-temperature stress on nitrogen accumulation and distribution in wheat seedlings.
Table 2. Effects of 15N urea amendment post or prior to low-temperature stress on nitrogen accumulation and distribution in wheat seedlings.
CultivarTreatmentNitrogen Accumulation (mg/plant)Percentage of Total Nitrogen from 15N Urea (%)15N Accumulation (mg/plant)15N Absorption Rate
(μg/d)
RootStemLeafRootStemLeafRootStemLeafRootStemLeaf
Yangmai 25N-LT3.7 a11.3 a26.1 a12.8 b11.2 b13.8 b0.5 a1.3 b3.6 b17.0 a45.2 b128.8 b
LT-N3.0 b10.3 b23.9 b0.6 c0.4 c0.4 c0.02 b0.1 c0.1 c0.9 b2.1 c4.6 c
Xumai 35N-LT3.0 b9.2 c22.9 c16.7 a18.4 a21.5 a0.5 a1.7 a4.9 a17.9 a60.7 a176.1 a
LT-N2.9 b9.5 c20.6 d0.6 c0.5 c0.4 c0.02 b0.1 c0.1 c0.8 b2.4 c3.5 c
NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low-temperature stress at 4-leaf stage; LT-N, Application of 15N urea post low-temperature stress at 4-leaf stage. The data in the same column followed by different letters are significantly different at the 0.05 probability level.
Table
Table 3. Effects of 15N urea amendment post or prior to low-temperature stress on agronomic characteristics of wheat seedlings.
Table 3. Effects of 15N urea amendment post or prior to low-temperature stress on agronomic characteristics of wheat seedlings.
CultivarTreatmentLeaf Area
per Plant
(cm2)		Leaf Area
Change
(%)		Tiller Number
per Plant		Tiller Number
Change
(%)		Seedling Height (cm)Seedling Height Change (%)Above-
Ground Dry Weight (g)		Above-
Ground Dry Weight Change
(%)		Root Dry Weight
(g)		Root Dry
Weight
Change
(%)		Ratio of Root to Shoot (%)
Yangmai 25NT144.7 a—10.2 a—32.9 a—1.1 a—0.3 a—29.6 a
LT81.6 d−43.65.4 d−47.127.6 c−16.10.6 d−40.20.1 e−56.322.3 bc
N-LT110.9 bc−23.47.8 bc−23.530.8 b−6.30.8 b−25.30.2 c−40.624.4 b
LT-N97.3 cd−37.86.2 cd−39.229.6 b−10.00.7 bcd−33.60.2 de−50.022.7 bc
Xumai 35NT140.2 a—9.4 ab—26.9 cd—1.1 a—0.3 b—25.2 b
LT92.7 cd−33.85.6 d−40.423.1 f−14.20.7 cd−38.90.1 e−48.221.1 c
N-LT124.0 ab−11.58.0 bc−14.925.6 de−4.80.8 bc−28.70.2 cd−33.323.3 bc
LT-N114.6 bc−18.27.2 cd−23.424.3 ef−9.70.7 bcd−36.10.2 de−40.722.4 bc
NT, Normal temperature control; LT, Low-temperature treatment at 4-leaf stage; N-LT, Application of 15N urea prior to low-temperature stress at 4-leaf stage; LT-N, Application of 15N urea post low-temperature stress at 4-leaf stage. The data in the same column followed by different letters are significantly different at the 0.05 probability level.
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Li, C.; Liu, M.; Dai, C.; Zhu, Y.; Zhu, M.; Ding, J.; Zhu, X.; Zhou, G.; Guo, W. Morphology and Nitrogen Uptake and Distribution of Wheat Plants as Influenced by Applying Remedial Urea Prior to or Post Low-Temperature Stress at Seedling Stage. Agronomy 2022, 12, 2338. https://doi.org/10.3390/agronomy12102338

AMA Style

Li C, Liu M, Dai C, Zhu Y, Zhu M, Ding J, Zhu X, Zhou G, Guo W. Morphology and Nitrogen Uptake and Distribution of Wheat Plants as Influenced by Applying Remedial Urea Prior to or Post Low-Temperature Stress at Seedling Stage. Agronomy. 2022; 12(10):2338. https://doi.org/10.3390/agronomy12102338

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Li, Chunyan, Mingmin Liu, Cunhu Dai, Yangyang Zhu, Min Zhu, Jinfeng Ding, Xinkai Zhu, Guisheng Zhou, and Wenshan Guo. 2022. "Morphology and Nitrogen Uptake and Distribution of Wheat Plants as Influenced by Applying Remedial Urea Prior to or Post Low-Temperature Stress at Seedling Stage" Agronomy 12, no. 10: 2338. https://doi.org/10.3390/agronomy12102338

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