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Article

Melatonin Increases Drought Resistance through Regulating the Fine Root and Root Hair Morphology of Wheat Revealed with RhizoPot

by
Zhihui Zhang
1,†,
Li Guo
2,†,
Hongchun Sun
1,
Jinhua Wu
1,
Liantao Liu
1,
Jianwei Wang
1,
Biao Wang
1,
Qianyi Wang
1,
Zhimei Sun
1 and
Dongxiao Li
1,*
1
State Key Laboratory of North China Crop Improvement and Regulation, Key Laboratory of Crop Growth Regulation of Hebei Province, College of Agronomy, Hebei Agricultural University, Baoding 071000, China
2
Institute of Agricultural Resources and Environment, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050051, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(7), 1881; https://doi.org/10.3390/agronomy13071881
Submission received: 2 June 2023 / Revised: 3 July 2023 / Accepted: 4 July 2023 / Published: 17 July 2023
(This article belongs to the Section Plant-Crop Biology and Biochemistry)
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Abstract

:
Melatonin application has obvious improving effects on alleviating the drought-induced inhibition of plant growth. However, the root phenotypic dynamics in wheat treated with melatonin remain unknown. This study was conducted using RhizoPot, a novel and improvised in situ root observation device, with three treatments, including normal water condition (CK), drought condition (Ds, relative water content 45–50%), and 100 µM melatonin treatment under drought condition (MT). Results showed that MT application effectively improves root morphological indicators, including root (specific root) length, surface area, and volume; root length density; and the average root diameter of wheat plants. Also, the inhibitory effect of drought on shoot morphology, including plant height, dry weight, net photosynthesis, and stomatal aperture of leaves, were improved significantly through MT under drought condition. Life span and percent survival of fine root, lateral root, and root hair at different segments were also effectively improved under MT treatment. Compared with those shown under CK and Ds, the melatonin contents in leaves and roots were increased, and the expression levels of melatonin-synthesis-related genes (TaCOMT and TaTDC) were upregulated significantly under MT treatment. The findings of this study may clarify the drought resistance mechanism of wheat treated with melatonin under drought stress.

1. Introduction

Winter wheat (Triticum aestivum L.), one of the most widely grown crops in the Huang-Huai-Hai Plain, contributes to more than 72% of China’s wheat production and plays a crucial role in ensuring food security [1]. However, precipitation during the winter wheat growing season exhibits a slow downward trend due to climate change in this region [2]. Following the depletion of groundwater resources, drought is a chronic question. In particular, wheat roots were shallower at the seeding stage and the plants were sensitive to drought, which resulted in the slow growth of wheat seedlings, deteriorated seedling quality, and further affected the construction of population and finally yield [3]. Therefore, some necessary irrigation is needed to ensure a high and stable yield in these dry regions [4]. The root system is the main organ of a plant for absorbing water and mineral nutrients. Good root system construction is an important foundation for improving water and nutrient supply in the aboveground part of a plant and the material exchange between aboveground and underground organs. Through sensing soil water status, the root system can adjust its architecture, physiological and biochemical characteristics, and anatomical structure, while transmitting an adversity signal to enhance the ability of plants to resist drought stress [5]. The physiological activity of root hair, the main water-absorbing part of the root, is sensitive to the soil environment and greatly affects plant growth and development [6,7,8,9]. Therefore, optimization of the root structure and root establishment is of great practical significance for enhancing plant resistance, improving resource utilization efficiency, and promoting crop yield increase [10].
Melatonin (MT), a kind of indole-like tryptamine, can significantly alleviate the stress of drought, saline-alkali, low temperature, and heavy metals and improve the ability of crops to resist adversity [11,12,13,14]. Application of MT could promote the germination of wheat seeds, increase the root–shoot ratio of seedlings, and enhance the drought response of wheat plants [15,16,17]. Variations in melatonin content have been reported to be involved in improving the architecture of a plant’s root system [18,19]. MT can increase the occurrence of main, lateral, and adventitious roots, and increase the number, length, and density of lateral roots, thereby affecting the ability of plants to obtain water and nutrients under stress [20,21,22]. One possible mechanism is related to the MT-induced synthesis of signal molecules, such as reactive oxygen species (H2O2 and Ož−), which regulate the expression of primordial root-cell-cycle regulation genes and promote the differentiation and development of lateral roots [23,24,25]. Another possibility is that MT also mediates the increase in endogenous NO levels downstream in plants through upregulating nitrate reductase activity, and feedback regulates the biochemical synthesis ability of melatonin in plants [26]. Also, MT interacts with many hormones to regulate root growth. Liang et al. [21] suggested that MT can effectively activate the auxin signaling pathway in rice and participate in the root-structure-shaping process. Tryptamine, an intermediate product of melatonin synthesis, is a substrate for the synthesis of auxin (IAA). Melatonin and auxin act synergically to promote the lateral root growth of Arabidopsis Thaliana wild-type plants [27]. However, the regulation of melatonin on Arabidopsis root development is also reported to be independent of auxin [28]. There is cross-talk directly or indirectly between hormones [29,30], and since melatonin is a hormone-like substance, it would affect root development via physiological regulation. So far, however, relevant studies on root growth and decline processes mediated by MT have been reported infrequently. The effect of MT-mediated root formation and its related signal transduction mechanism under drought treatment still require further study.
The root tip is the site of lateral root generation and root hair growth [31,32]. The phenotypic changes of lateral root, root hair growth and senescence in the main functional regions of a wheat root system treated with melatonin would be helpful to clarify its regulatory mechanism [33,34]. Although increasingly more in situ root observation methods have been developed, a series of apparent defects are still unavoidable such as microroot canals destroying the original soil structure [35], the immature and unstable function of electrical capacitance [36], the inhibition of cell growth by X-ray computer tomography [37], the poor identification precision of ground-penetrating radar [38], high production cost, and so on. Therefore, a new method, the RhizoPot system, has been designed to obtain in situ root images using a high-resolution scanner [34,39]. Moreover, studies on the effect of drought on the morphology and lifespan of lateral roots and root hairs have yet to be conducted on winter wheat under varying soil conditions. In this study, we tested the following hypotheses: (i) MT alleviates the inhibition effect of drought on the diameter and density of lateral roots, (ii) MT extends the lifespan of lateral roots and root hairs, and (iii) MT adjusts corresponding physiological signal transportation between roots and aerial tissues to improve wheat plants to acclimatize to a drought environment.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

This experiment was conducted in the phytotron of Hebei Agricultural University, Hebei, China (38°85′ N, 115°30′ E). The culture conditions for plants were as follows: 20 °C/15 °C day/night (14 h/10 h), and 60–70% indoor relative humidity. A commercial wheat (Triticum aestivum L.) cultivar Jimai 22 was used as the experimental material, and the seeds were provided by the Shandong Academy of Agricultural Sciences, China. The planting vessels (35 cm in height, 20 cm in length, 8 cm in width) were sealed with transparent acrylic plates, and the slope side was equipped with a scanner (Figure 1). This system allowed for much more crop roots to grow along the scanner-fixed wall of culture container, which was beneficial to effectively obtain clear images of lateral roots and root hairs every day during the root growth trait assays.
The planting matrix is a mixture of 0–20 cm topsoil and sand (5:1, v:v). Both were firstly air-dried and passed through a 0.85-mm-sieve. Each vessel was filled with about 16 kg of soil–sand matrix. Before seed sowing, sufficient water was provided to ensure the planting matrix was fully attached to the vessel walls, especially to the scanner side. The matrix was comprised of the following nutrient content: organic matter 17.38 g/kg, alkali-hydrolyzed nitrogen 52.5 mg/kg, available phosphorus 61.75 mg/kg, and available potassium 152.25 mg/kg with a pH 7.4. Wheat seeds were surface-sterilized with a solution of 75% (v/v) ethanol for 5 min, then washed three or four times using sterile distilled water and placed into an incubator at 25 °C for 24 h without light for germination. Afterwards, the germinated seeds with consistent behaviors were selected and transplanted into the vessels, closer to the scanner side. When relative soil water content decreased to 70–75%, a suitable moisture range for wheat plant growth, the germinated seeds were transplanted into the vessels. The treatments, namely normal water condition (control CK), drought treatment (Ds), and drought combined with 100 µM melatonin (D + MT, abbreviated as MT) were established at the seedling stage with 6 replicates for each treatment. Among these, the relative soil water contents were maintained at 70–75% for CK, 40–45% for D, and 40–45% for D + MT, respectively. The water condition was monitored by weighing the Rhizopots every day [33]. Melatonin solution (100 µM) was prepared by dissolving the powdered melatonin (Shanghai Yuanye Biotechnology Co., Ltd., Shanghai, China; J19GS155217) in a few drops of absolute alcohol, then it was diluted to a working concentration with distilled water.

2.2. Measurements of Morphological Traits of Aboveground Plant and Photosynthetic Indicators

Plant height, leaf length, and the width of wheat plants under various treatments were measured using a manual ruler at 30 days after seedling emergence. Leaf area (LA) was calculated using the formula reported by Li et al. [40], namely LA = Leaf length(L) × Leaf width(W) × 0.76. The net photosynthetic rate (Pn) and transpiration rate (Tr) of fully unfolded leaves in plants were measured using a LI-6400 portable photosynthesis system (LI-COR, Lincoln, NE, USA). Instantaneous water use efficiency (WUEins) was calculated using the following formula [41]:
WUEins = Pn/Tr

2.3. Stomata Detection and Pore Measurement

For each leaf sample, 2–3 cm in length of both abaxial and adaxial surfaces of the leaf was coated with nail polish, and air dried for about 5 min. The epidermis of each side was then peeled off, mounted on a glass microscope slide, and examined under an optical microscope (BX51, Olympus, Japan). The guard cell length and length and width of stomatal aperture were determined under 40× magnification with the measuring condition of the microscope.

2.4. Assessment of Antioxidant Enzymes Activities, Hydrogen Peroxide Content, Soluble Protein Content and Detection of H2O2

Samples of leaves and roots were collected from wheat plants after various treatments, and 500 mg was ground into a homogenate with (w:v = 1:9) 4.5 mL of 0.1 mol/L phosphate buffer (pH 7.4). Subsequently, the resulting mixture was mixed by swirling for 3 min and centrifuged under 899.1 g for 10 min at 4 °C. After centrifugation, the supernatant was collected for assessing the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) and the malondialdehyde (MDA) contents. The assay kit (A064, Nanjing Jiancheng Bioengineering Institute, Nanjing, China) was used to measure above parameters according to the manufacturer’s instructions.
Hydrogen peroxide (H2O2) and soluble protein contents in wheat plants were determined after treatments using a hydrogen peroxide assay kit (A145-1-1, Nanjing Jiancheng Bioengineering Institute, Nanjing, China) and a BCA assay kit (BCAP-1-W, Suzhou Comin Biotechnology Co., Ltd., Suzhou, China), respectively, according to the manufacturer’s user manual [42].

2.5. Collection and Calculation of Root Growth Data

Root image collection: Each observation window covering 18 groups in situ root phenotypes system was scanned each time every day across all of the seedling stage [33]. Scanning process was performed at 8 a.m. Firstly, the observation window was scanned globally using a resolution of 1200 DPI, which took 3–5 min. Then, the area of each observation window was divided into four sections for scanning at a higher resolution (4800 DPI), which took about 60 min. The daily scanning work lasted 40 days, which started at 7–10 days after seeds sowing. The images collected daily were systematically analyzed to obtain the phenotype data of fine roots and root hairs (Figure 2A).
Root data calculation: Clear and representative images obtained under three treatments were selected and subjected to segment elucidation using a deep learning tool (DeepLabv3+), which displayed the root system in white and the culture medium in black [43] (Figure 2B). The segmented root pictures were further analyzed for root length (RL, cm), area of contour (AC, cm2), root surface area (RSA, cm2), average root diameter (AD, mm), and root volume average (RA, cm3) using software WinRHIZO REG2009 (Regent Instruments, Inc., Quebec City, Canada). The root length density per unit volume (RLD) was defined as the basic parameter, and was calculated using the following formula: RLD (cm/cm3) = RL/A × DOF. In this formula, RL is the root length, A (cm2) is the area of the observation window, and DOF (cm) is the observed soil thickness (0.25 cm) [33].
Average root hair length (ARHL, mm) and root hair density (RHD) were measured using the software “Ruler Tool” installed in Adobe Photoshop CC 2019 (Adobe, San Jose, CA, USA). In addition, Adobe Photoshop was also used to analyze different time-series images collected from RhizoPot to determine root hair life span (RHL) and calculate the root hair longevity [33].
Specific root length (SRL, cm g−1) = total root length/root dry weight
Specific root surface area (SRA, cm−2 g−1) = total root surface area/root dry weight
Specific root volume (SRV, cm−3 g−1) = total root volume/root dry weight

2.6. Statistical Analysis

All data were processed using one-way ANOVA in triplicate in Excel 2003 and IBM SPSS Statistics 17.0 (IBM Corp, Armonk, NY, USA). Significant differences between treatments were determined at a p < 0.05 threshold and considered to be significant according to Duncan’s test. The average life span of the root hairs was shown using the average survival days and were measured using the Kaplan–Meier method [39,44]. The median RHL (i.e., the time at which the survival rate reached 50%) was estimated, and survival curves were generated as previously described [33].

3. Results

3.1. Effect of MT on Wheat Shoot Morphology under Drought Stress

Figure 3 shows that the plant height, dry weight of shoot, and leaf area of plants under Ds treatment decreased significantly by 23.8%, 76.54%, and 81.70% compared with CK, respectively. However, compared with Ds, the plant height, dry weight of shoot, and leaf area were increased by 24.96%, 115.75%, and 132.24%, respectively, under MT treatment, of which significant differences have been shown on dry weight of shoot and leaf area (p < 0.05). Meantime, Pn, Tr, and WUEins were significantly decreased under Ds condition by 62.98%, 28.33%, and 47.75%, respectively, compared with those under CK. In contrast, MT treatment alleviated the adverse effects of drought stress on Pn and recovered it to the CK level, which increased Tr significantly by 44.15% and 101.12% compared to CK and Ds. However, WUEins was not significantly altered under MT treatment compared with that under Ds.

3.2. Length and Width of Stomatal Aperture

Figure 4 shows that Ds significantly decreased the guard cell lengths and stomatal aperture length by 3.85% and 12.12%, respectively, compared with CK. MT significantly increased the stomatal guard cell lengths, recovering them to the level of CK. There were no significant differences on stomatal aperture width among the three treatments (i.e., CK. Ds, and MT). Moreover, changed stomatal aperture structure was observed to be consistent with the results under different treatments.

3.3. Antioxidant Enzymes Activities, Hydrogen Peroxide Content, Soluble Protein Content and Detection of H2O2

The CAT activities, contents of soluble protein, amounts of H2O2, and MDA in wheat leaves were significantly increased by 25.70%, 37.00%, 38.69%, and 25.35%, respectively, under Ds treatment compared to CK. MT application decreased these indicators by 43.14%, 36.09%, 36.24%, and 7.27%, respectively. Meanwhile, MT also increased the SOD activities by 22.06% and 10.11% compared to CK and Ds, respectively (Table 1).
Assessment on roots indicated that the SOD activities under Ds and MT treatments were decreased significantly, whereas CAT activities, soluble protein contents, and H2O2 amounts increased significantly in roots under Ds compared to CK (Table 1). MT application did not significantly change these indices compared to Ds treatment. The MDA contents in roots were comparable with CK under Ds, but were obviously decreased under MT compared with those under Ds condition (Table 1).

3.4. Root Morphology Indicators of Wheat Plants under Different Treatments

Table 2 shows that root lengths, areas of contour, root surface areas, and root volumes were all significantly decreased under Ds treatment (53.17%, 56.51%, 56.51%, and 63.36%, respectively) compared to CK. MT increased these indicators significantly, and recovered most of them to the CK level. Compared with Ds, MT increased root length, area of contour, root surface area, and root volume by 80.42%, 96.26%, 96.26%, and 146.08%, respectively. However, no significant variation was observed for the average root diameter among the three treatments.

3.5. Effect of MT on Root Length Density (RLD) and Average Root Diameter of Wheat Fine Roots under Drought Condition

Figure 5 shows that the root length density (RLD) was significantly decreased under Ds compared with CK when assessed at all of the time points. RLD displayed the highest difference among treatment (between 1.45–1.60 cm/cm3, 68.49–71.15%) 28–35 days after seed sowing. MT application clearly increased RLD at 17 days after sowing under drought condition, but its RLD values were lower significantly than those of CK. The average root diameter under MT was the highest 13–26 days after sowing. No significant differences were observed in the RLD values among the three treatments at other times.

3.6. Effect of MT on Specific Root Length, Specific Root Surface Area, and Specific Root Volume of Wheat

Figure 6 shows that the specific root lengths, specific root surface areas, and specific root volumes of wheat plants were decreased significantly by 13.58%, 28.44%, and 42.65%, respectively, under Ds compared to CK. MT significantly increased these indices by 15.01%, 40.54%, and 62.93%, respectively, compared to Ds. There were no significant differences in these indicators between MT and CK.

3.7. Effect of MT on Root Hair Phenotypes under Drought Condition

D s significantly decreased the average root hair length (ARHL) of wheat plants compared to CK (Figure 7). The reduction percentage varied between 22.67% and 51.00%. MT significantly increased ARHL by 29.56–64.04% compared to the Ds condition. The similar patterns were observed in root hair density (RHD) and percent survival of root hairs. Ds significantly reduced RHD by 34.31% compared to CK, but it was increased significantly by 46.87% under MT treatment and recovered the level of CK. Both percent survival of root hairs and survival time decreased significantly under Ds compared with CK, in which the survival percent was reduced from 12.55% to 82.24% and survival time was shortened by 8 days. MT significantly improved both of these indicators, in which survival percent increased by 11.76–458.82% and survival time was prolonged by 5 days compared to Ds.
Root hair life span shows the period from the appearance of root hair to the termination of its distortion (Figure 8). All of the fine roots, lateral roots and root hairs were all in white color and activated at 22 days after sowing (Figure 8A–E). Afterwards, the root system gradually declined and fell (Figure 8F–H). All the changing process of roots was shown in wheat plants under three treatments, but the extents of decline (e.g., percent survival) were different at the same stage.

3.8. Effect of MT on Content of Melatonin in Wheat under Drought Condition

Figure 9 shows that the melatonin contents in leaf and root tissues were different, with higher values shown in leaves than in roots. Under Ds condition, the melatonin contents were not significantly different compared to CK. However, they were increased significantly under MT condition compared with CK and Ds. This result suggests that exogenous melatonin was absorbed directly by roots and further transported to the whole stool.

3.9. Relative Expression of Caffeic Acid-3-O-Methyltransferase Gene (TaCOMT) and Tryptophan Decarboxylase Gene (TaTDC)

Realtime-PCR was conducted to understand if the expression of TaCOMT and TaTDC, the melatonin-synthesis-related genes, which were modified significantly in leaves under the Ds condition (Figure 10). The expression levels of TaCOMT were not significantly different in roots under Ds compared to CK. MT treatment significantly increased their expression levels in leaf and root tissues. These results suggest that melatonin plays an important role in mediating the drought response of wheat plants through the activation of stress-responsive genes.

4. Discussion

4.1. MT Effectively Improves Aboveground Morphology of Wheat Plants under Drought Condition

It has been widely documented that melatonin exerts a role in regulating plant growth and development, especially under abiotic stress conditions. In this study, our results indicated that melatonin recovered the aboveground plant growth effectively, including plant height, dry weight of shoot, and leaf area of wheat plants under drought stress. The recovery effect on these indices by MT for drought-challenged wheat plants partly ascribed to its role in increasing Pn. However, the similar instantaneous water use efficiency of leaves were shown under MT and Ds conditions, which was different with the report of Cui et al. [16]. The divergence on this index shown in our study and previous investigation is possibly due to the increased Tr under our experimental condition, which resulted in much more obvious change of the stomatal structure, including stomatal aperture length and the guard cell length (Figure 4). Similar related results of melatonin on the regulation of stomatal traits were also reported by Ahmad et al. [45].

4.2. MT Mitigates Oxidative Damage on Physiology Function of Wheat Shoot and Root under Drought Condition

Melatonin plays a key role in improving the antioxidant capacity of drought-stressed plants [16,46]. The antioxidant components regulate the behaviors of aerial and root parts, showing tissue-selective characteristics [16]. In this study, drought stress elevated the accumulation of soluble protein, namely MDA and H2O2, and improved CAT activities in leaf and root tissues. Our results indicated that melatonin application decreased the levels of the ROS-associated indicators, namely accumulative amounts of MDA and H2O2 in leaves and roots. We also found that there are different regulatory effects of drought and MT on behaviors of SOD activities in leaf and root tissues. These results indicate that melatonin significantly impacts the physiological functions regarding growth traits of aerial tissues and roots with different regulatory degrees, of which the root characters mediated by MT are acclimated to maintain the biomass and keep signaling cross-talk with the shoot according to the changed environmental factors [47,48].

4.3. MT Effectively Improves Root Characteristics of Wheat under Drought Condition

As the soil’s moisture contents decreases, the signals initiated by the drought are perceived by roots and further transported to aerial tissue; in the meantime, the root morphological traits, e.g., root length, root weight, were adjusted promptly to adapt the modified ambient environment. Screening root traits at plant early stages has been reported to be linked with increased crop productivity under drought [49]. Therefore, much more understanding the early establishment of root system can help effectively acquire of soil water for crop plants under water-limited conditions [50,51]. In this study, compared with CK, we found that drought stress treatment (Ds) significantly decreased root length, area of contour, root surface area, root volume, and root length density, but Ds does not affect the average root diameter of wheat plants. This finding is different from previous research that indicated that moderate drought exerts the promoted effects on root length [52]. The different results are possibly attributed to the drought extent degree, drought mode, and drought duration in the studies. Research has shown that drought stress (45 ± 5% soil-relative water content) could promote the length of fine roots and root hairs of cotton plants but reduce the root diameter and accelerate the death process [33]. This may be thought to function as a resource conservation strategy that inhibits plants access to resources, saving higher root-construction costs by extending root life duration [53].

4.4. Root Hair Phenotypes Are Sensitive to Drought Conditions and MT Treatment

In our research, melatonin exerted a significant effect in improving the root traits indicators and root hair phenotypes of wheat plants under drought conditions, but it did not change the average root diameter at various sampling times. These results are not fully consistent with other reports [54]. We observed that the traits of root growth phenotypes were dynamically changed during all of the growth stage, during which the average root diameters were increased significantly at 15–20 days after sowing and kept stable at other times under MT compared with other treatments. These results are closely associated with the functional duration of different root segments/parts. For example, the MT-mediated drought signaling in root hairs depend largely on its effects in regulating the protein interaction and phosphorylation processes [31,42]. Therefore, the life span and percent survival of fine root, lateral root, and root hair under different treatments mediated by MT should be considered for the crucial roles of this regulator in regulating drought resistance in crop plants.
Our assays on MT content in leaves and roots suggest the increase of this regulator when melatonin was applied to the rhizosphere under drought condition, which is consistent with the upregulated expression levels of TaTDC and TaCOMT in leaf and root tissues. Ds decreased the expression levels of TaTDC and TaCOMT in leaves, but it did not change the melatonin content in the tissue. This inconsistency is possibly attributed to IAA regulation for the precursor—tryptophan [55]. In addition, with the increased MT content in plants, a subset of physiological processes associated with osmoregulation, germination, photosynthesis, senescence, primary/secondary metabolism, and hormonal cross-talk were improved to contribute to plant drought resistance [56]. Besides these interior factors, a lot of external factors, including edaphic condition, planting density, plant size, intercropping pattern, agronomic practice, and seasonal weather pattern should be considered as impacting the root architecture during the application of MT during wheat production [57]. The detailed mechanism that melatonin regulates in situ root phenotypes and plant productivity under drought condition need to be explored in future works.

5. Conclusions

The application of melatonin effectively alleviates the inhibitory effect of drought on morphological indicators of roots and aerial tissues of wheat plants. The traits of root growth phenotypes were modified dynamically during the seedling stage. Under drought stress, the life span and percent survival of fine roots, lateral roots, and root hairs at different root segments were significantly improved by MT treatment, which led to the improved drought resistance of wheat plants. The findings of this study provide novel insights into clarifying the drought resistant mechanism of wheat plants underlying melatonin regulation.

Author Contributions

Conceptualization, D.L. and Z.S.; methodology, L.G.; software, H.S. and J.W. (Jinhua Wu); methodology, L.L.; validation, J.W. (Jianwei Wang) and B.W.; formal analysis and investigation, Q.W.; writing—original draft and preparation, Z.Z., L.G. and D.L.; writing—review and editing, Z.S.; funding acquisition, Z.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (32201908), the National Key Research and Development Program of China (2021YFD1901004), and the Natural Science Foundation of Hebei Province (C2022204070).

Data Availability Statement

Not applicable.

Acknowledgments

We are grateful to the laboratory staff and the undergraduate students Heyang Tian, Dongwei Han, Jinrong Ma, Hongyan Zhang, Shan Li of the Hebei Agricultural University for their contributions. The valuable comments of the editor and anonymous reviewers are greatly acknowledged.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Diagram (A) and real picture (B) showing wheat root cultivation in RhizoPot device.
Figure 1. Diagram (A) and real picture (B) showing wheat root cultivation in RhizoPot device.
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Figure 2. The scanning picture (A) and image after cutting (B).
Figure 2. The scanning picture (A) and image after cutting (B).
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Figure 3. Growth traits and water-utilization-associated physiological parameters of wheat plants under Ds, MT, CK conditions. Plant height (A), dry weight of shoot (B), leaf area (C), net photosynthetic rate (Pn) (D), transpiration rate (Tr) (E), and the maximum photochemical efficiency (WUEins) (F). Depicted are the means of five replicates ± standard errors. Different lowercase letters in each bar chart indicated that there were significantly different on indices among the three treatments (p < 0.05).
Figure 3. Growth traits and water-utilization-associated physiological parameters of wheat plants under Ds, MT, CK conditions. Plant height (A), dry weight of shoot (B), leaf area (C), net photosynthetic rate (Pn) (D), transpiration rate (Tr) (E), and the maximum photochemical efficiency (WUEins) (F). Depicted are the means of five replicates ± standard errors. Different lowercase letters in each bar chart indicated that there were significantly different on indices among the three treatments (p < 0.05).
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Figure 4. Stomatal properties of wheat plants under various treatment conditions. (A) Stomata guard cell length, (B,C) stomatal aperture length and width, (D–F) structure picture of stomatal aperture of wheat leaves under different treatments. Different lowercase letters in each bar chart (A–C) indicate that there were significantly different on indexes among the three treatments (p < 0.05).
Figure 4. Stomatal properties of wheat plants under various treatment conditions. (A) Stomata guard cell length, (B,C) stomatal aperture length and width, (D–F) structure picture of stomatal aperture of wheat leaves under different treatments. Different lowercase letters in each bar chart (A–C) indicate that there were significantly different on indexes among the three treatments (p < 0.05).
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Figure 5. Behaviors of root length density (RLD) and average root diameter (ARD) of wheat plants under different treatments.
Figure 5. Behaviors of root length density (RLD) and average root diameter (ARD) of wheat plants under different treatments.
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Figure 6. Effect of MT on specific root length, specific root surface area, and specific root volume of wheat. Different lowercase letters in each bar chart indicated that there were significant differences between indices among the three treatments (p < 0.05).
Figure 6. Effect of MT on specific root length, specific root surface area, and specific root volume of wheat. Different lowercase letters in each bar chart indicated that there were significant differences between indices among the three treatments (p < 0.05).
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Figure 7. Behaviors of in average root hair length (ARHL), percent survival, and root hair density (RHD) of wheat plant under different treatments. Different lowercase letters in the bar chart indicated that there were significantly different on RHD among three treatments (p < 0.05).
Figure 7. Behaviors of in average root hair length (ARHL), percent survival, and root hair density (RHD) of wheat plant under different treatments. Different lowercase letters in the bar chart indicated that there were significantly different on RHD among three treatments (p < 0.05).
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Figure 8. Images of the wheat root hairs at same root area taken at different times during the life span. Scale bar, 0.2 mm. Images shown are taken on (A) 23 December, (B) 25 December, (C) 27 December, (D) 29 December, (E) 31 December, (F) 2 January, (G) 4 January, and (H) 6 January.
Figure 8. Images of the wheat root hairs at same root area taken at different times during the life span. Scale bar, 0.2 mm. Images shown are taken on (A) 23 December, (B) 25 December, (C) 27 December, (D) 29 December, (E) 31 December, (F) 2 January, (G) 4 January, and (H) 6 January.
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Figure 9. Effect of MT on melatonin content in root and leaf tissues of wheat plants seedings. Different lowercase letters in the bar chart indicated that there were significant differences between MT content in leaves and roots among the three treatments (p < 0.05).
Figure 9. Effect of MT on melatonin content in root and leaf tissues of wheat plants seedings. Different lowercase letters in the bar chart indicated that there were significant differences between MT content in leaves and roots among the three treatments (p < 0.05).
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Figure 10. Relative expression of TaCOMT and TaTDC in roots and leaves under different treatments. Different lowercase letters in the bar chart indicated that there were significant differences between expression levels of TaTDC and TaCOMT in leaves and roots among the three treatments (p < 0.05).
Figure 10. Relative expression of TaCOMT and TaTDC in roots and leaves under different treatments. Different lowercase letters in the bar chart indicated that there were significant differences between expression levels of TaTDC and TaCOMT in leaves and roots among the three treatments (p < 0.05).
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Table
Table 1. Effects of MT on antioxidant enzyme activities, hydrogen peroxide contents, soluble protein contents, and H2O2 accumulation.
Table 1. Effects of MT on antioxidant enzyme activities, hydrogen peroxide contents, soluble protein contents, and H2O2 accumulation.
OrgansTreatmentsSOD Activity (U/g FW)POD Activity (U/g FW)CAT Activity (U/mg prot.)Soluble Protein Content (μg/mL)H2O2 Content (mmol/g prot.)MDA Content (nmol/g)
LeafCK501.71 ± 33.11 b593.17 ± 20.57 a191.87 ± 21.86 b2514.51 ± 286.35 b2663.92 ± 19.12 b355.00 ± 21.79 c
Ds556.15 ± 50.94 ab621.53 ± 42.13 a241.19 ± 2.86 a3444.91 ± 369.34 a3694.54 ± 18.83 a445.00 ± 30.41 a
MT612.40 ± 12.86 a582.75 ± 17.39 a137.13 ± 13.83 c2201.49 ± 201.49 b2355.71 ± 20.00 c412.67 ± 20.60 b
RootCK797.48 ± 29.10 a550.35 ± 12.03 a39.02 ± 6.14 b210.12 ± 13.73 b597.74 ± 8.23 b26.67 ± 2.89 ab
Ds636.90 ± 7.20 c544.56 ± 13.03 a73.98 ± 17.21 a248.17 ± 9.82 a661.25 ± 6.61 a38.3 ± 12.58 a
MT689.21 ± 36.75 b576.39 ± 51.15 a70.73 ± 15.45 a233.47 ± 22.47 ab652.99 ± 1.66 a16.67 ± 2.89 b
Note: FW, fresh weight; prot, protein. Different lowercase letters in each column indicated that there were significantly different between indexes among the three treatments (p < 0.05).
Table
Table 2. Root morphological indicators of wheat plants under different treatments.
Table 2. Root morphological indicators of wheat plants under different treatments.
TreatmentRoot Length (RL, cm)Area of Contour (AC, cm2)Root Surface Area (RCA, cm2)Average Root Diameter (ARD, mm)Root Volume (RV, cm3)
CK16,672.25 ± 520.02 a530.48 ± 81.91 a1666.55 ± 257.31 a0.33 ± 0.05 a14.03 ± 4.48 a
Ds7807.56 ± 1420.07 c230.68 ± 11.42 b724.71 ± 35.89 b0.30 ± 0.04 a5.49 ± 0.61 b
MT14,086.05 ± 1630.21 b452.74 ± 63.48 a1422.33 ± 199.42 a0.32 ± 0.05 a13.51 ± 0.93 a
Note: Different lowercase letters in each column indicated that there were significantly different between indices among the three treatments (p < 0.05).
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Zhang, Z.; Guo, L.; Sun, H.; Wu, J.; Liu, L.; Wang, J.; Wang, B.; Wang, Q.; Sun, Z.; Li, D. Melatonin Increases Drought Resistance through Regulating the Fine Root and Root Hair Morphology of Wheat Revealed with RhizoPot. Agronomy 2023, 13, 1881. https://doi.org/10.3390/agronomy13071881

AMA Style

Zhang Z, Guo L, Sun H, Wu J, Liu L, Wang J, Wang B, Wang Q, Sun Z, Li D. Melatonin Increases Drought Resistance through Regulating the Fine Root and Root Hair Morphology of Wheat Revealed with RhizoPot. Agronomy. 2023; 13(7):1881. https://doi.org/10.3390/agronomy13071881

Chicago/Turabian Style

Zhang, Zhihui, Li Guo, Hongchun Sun, Jinhua Wu, Liantao Liu, Jianwei Wang, Biao Wang, Qianyi Wang, Zhimei Sun, and Dongxiao Li. 2023. "Melatonin Increases Drought Resistance through Regulating the Fine Root and Root Hair Morphology of Wheat Revealed with RhizoPot" Agronomy 13, no. 7: 1881. https://doi.org/10.3390/agronomy13071881

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