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Article

Drought Changes the Trade-Off Strategy of Root and Arbuscular Mycorrhizal Fungi Growth in a Subtropical Chinese Fir Plantation

by
Jie Dong
1,†,
Yongmeng Jiang
1,†,
Maokui Lyu
2,*,
Cong Cao
1,
Xiaojie Li
1,
Xiaoling Xiong
1,
Weisheng Lin
1,3,*,
Zhijie Yang
1,2,
Guangshui Chen
1,2,
Yusheng Yang
1,2,3 and
Jinsheng Xie
1,2
1
Key Laboratory for Humid Subtropical Eco-Geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou 350007, China
2
Sanming Forest Ecosystem National Observation and Research Station, Sanming 365002, China
3
College of Geography Sciences, Fujian Normal University, Fuzhou 350007, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2023, 14(1), 114; https://doi.org/10.3390/f14010114
Submission received: 21 November 2022 / Revised: 21 December 2022 / Accepted: 5 January 2023 / Published: 7 January 2023
(This article belongs to the Special Issue Forest Soil Carbon Cycle in Response to Global Change)
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Abstract

:
As a consequence of changing global rainfall patterns, frequent extreme droughts will significantly affect plant growth and ecosystem functions. Fine roots and arbuscular mycorrhizal fungi (AMF) both facilitate Chinese fir nutrient uptake. However, how the growth of fine roots and AMF is regulated for the Chinese fir under drought conditions is unclear. This study used a precipitation reduction treatment (−50% throughfall) to study the seasonal effects of drought on a subtropical Chinese fir plantation. The effects measured included the fine root production, root diameter, specific root length, specific surface area, root tissue density, mycorrhizal hyphal density, spore number, mycorrhizal infection rate and total glomalin. Drought had no significant effect on Chinese fir fine root production but decreased the diameter and tissue density of primary and secondary roots while increasing the specific surface area of secondary roots. Additionally, drought significantly decreased the arbuscular mycorrhizal infection rate and significantly increased hyphal density. The results showed that drought caused the decrease in root diameter, which decreased the surface area available for AMF infection and led to the increase in mycorrhizal hyphal density. Redundancy analyses showed that soil-dissolved organic carbon and nitrogen were the key factors affecting AMF. Our results show that drought could enhance the cooperative strategy of nutrient and moisture absorption by roots and mycorrhizae of the Chinese fir, improving the resistance of Chinese fir growth to drought.

1. Introduction

The climate change-induced increase in the frequency and intensity of global extreme droughts deeply affects the stability of terrestrial ecosystems’ structure and function. Drought is an influential abiotic stressor, affecting plant growth and productivity through morphological, physiological, biochemical and molecular changes [1,2,3]. Drought affects not only the growth and community composition of aboveground plants but also the underground parts of plants and the diversity and community composition of microorganisms [4,5,6]. Arbuscular mycorrhizal fungi (AMF) are a type of fungus that can form a mutually beneficial relationship with the roots of approximately 80% of terrestrial vascular plants, significantly improving plant nutrient uptake and resistance to several abiotic stress factors such as drought [7]. In most arbuscular mycorrhizal symbioses formed by terrestrial plants, absorbing roots and associated mycorrhizal fungi are both important avenues of soil nutrient absorption [8]. Therefore, nutrient acquisition strategies for plants in different environments should depend on the regulation of absorbing roots and their fungal symbionts [9].
Fine roots (diameter ≤2 mm) serve important absorption and transport functions above and below ground in terrestrial ecosystems [10]. Plant roots have complex morphological characteristics and their responses to soil resource changes depend on their task, such as nutrient absorption or transport [11,12]. Changes in root morphology may also alter plants’ strategy for underground resources, such as changing root spatial expansion and nutrient acquisition abilities [3,13]. It is often believed that the variation in specific root length can not only be an indicator of the strength of the physiological function of fine roots but also the input and output efficiency of plants; while the function of the specific surface area is similar to that of the specific root length, it is also an important index of the nutrient absorption efficiency and ability of fine roots [14,15]. For example, higher specific root length represents more efficient soil occupancy and nutrient acquisition strategies [10,16]. As droughts intensify globally, changes in plant fine root morphology as a response to environmental changes have become a research hotspot for ecologists. Previous studies have shown mixed plant responses when the soil moisture content decreases. In certain plants, the diameter of their fine roots and plant lifespan were significantly reduced, while others responded to rainfall reduction by increasing their specific fine root length, and some plants had no significant fine root morphological changes [17,18]. In an experiment using potted plants, mild rainfall reduction promoted an increase in fine roots, specific surface area and specific root length, while moderate and severe rainfall reduction inhibited fine root production [19]. This indicated that the degree of rainfall reduction significantly affected the behavior of plant roots.
Many studies have shown that plant mycorrhizal symbiosis is one of the most effective ways of withstanding stress, improving plant growth [20,21,22]. AMF can form symbiotic relationships with most terrestrial plants and have a great significance in improving plant nutrient uptake and resistance to several abiotic stress factors which is in turn of great significance for maintaining ecosystem stability [23,24]. According to the functional equilibrium model, plants should distribute more photosynthetic products to organs responsible for obtaining limited resources [25]. Therefore, in low-fertility soils, the relative distribution should favor absorbing roots or AMF [26,27,28]. AMF is more effective in obtaining limited soil resources and has a higher surface-area-to-volume ratio than absorbing roots. However, it is unclear whether plants tend to invest more carbon in roots or AMF in response to drought.
Some studies have found that a higher mycorrhizal hyphal distribution allows plants to obtain resources at lower carbon costs [28,29]. However, when plants are subject to more severe nutrient restrictions, they inhibit AMF growth; as a result, AMF may retain any absorbed nutrients for their own growth, which reduces the advantages of resource exchange between plants and fungi [30,31]. Some studies showed that when soil moisture decreased, AMF hyphae could not maintain their structural integrity [32,33] and the root infection rate and mycorrhizal hyphal density decreased [34,35,36]. However, experimental warming on the Qinghai–Tibet Plateau had no significant effect on root infection rate, spore density or mycorrhizal hyphal density [37]. Therefore, there are no definite conclusions on how drought stress affects AMF infection. Moreover, current studies of the effects of soil factors on AMF infection focus on indoor pot experiments. There is limited research on how the AMF of large woody plants respond to drought stress under natural conditions.
With changing climates, plant root-soil-microorganism interactions become increasingly important, especially considering rhizosphere processes and biogeochemical cycles. It is not clear whether and how changes in soil conditions lead to a combined root and AMF response. It is estimated that China’s plantations account for 33% of the world’s total planted forest area [38]. Notably, more than 32% of these plantation forests are dominated by coniferous species such as Chinese fir (Cunninghamia lanceolata), [39,40] which plays an important role in forestry production and as a carbon sink [40]. In recent years, the occurrence of extreme rainfall events and changes in rainfall distribution patterns have frequently led to extreme climates such as drought in the subtropics, seriously affecting the production of Chinese fir forests. Under drought stress, the fir grows slowly to reduce water loss, the lifespan of fine roots is shortened and the nutrient input of the litter is weakened [41]. There are few studies on the drought resistance mechanism of the Chinese fir that investigate the response of roots and AMF at the same time. Chinese fir roots and AMF are the plant’s avenues for acquiring underground resources, so it is extremely important to understand how they respond to the heterogeneity of soil nutrient availability. We hypothesized that under drought conditions, Chinese fir would invest more resources to AMF and lead to high AMF to help the trees uptake nutrients and water resources [42,43]. Furthermore, we theorized that drought in summer would have a larger impact on roots and the AMF growth strategy than in winter, because droughts are more intense in summer than in winter. To explore this regulation of their growth strategy for drought in different seasons, we studied the Chinese fir plantation in the Castanopsis kawakamii Nature Reserve of Sanming City, Fujian Province. This allowed us to examine the physiological adaptability of Chinese fir trees to drought and to provide scientific insights for the change in the productivity and biogeochemical cycles of subtropical forest ecosystems due to global warming.

2. Materials and Methods

2.1. Overview of Sample Plots and Experimental Design

The experimental plots of this study are in the Sanming Forest Ecosystem National Observation and Research Station, Fujian Province (26°7′–26°10′ N, 117°24′–117°27′ E). The region has low mountains and hilly terrain; it has a subtropical monsoon climate, with an annual average temperature of 19.5℃ and rainfall of about 1700 mm. During the study period, the rainfall from March to August accounted for 75% of the year’s total, often accompanied by seasonal drought throughout the year’s annual precipitation averages. A previous study showed that the precipitation in tropical and subtropical regions is declining and thus leading to a severe drought effect on plant growth [44]. The soil is classified as red soil derived from crystalline granite in the Chinese soil classification, equivalent to Oxisol in the USDA soil taxonomy [45,46]. The sample plot of Cunninghamia lanceolata (Chinese fir) used in this study was planted in 1972 after the site’s natural forest of Castanopsis kawakamii was removed by clear-cutting and burning. Chinese fir prefers to grow in a humid climate and humid tropical subtropical areas.
The isolated rainfall control experiment was established in 2018 using a random block design. Each 18 m × 18 m block contained 4 replicates. A “V”-shaped transparent isolation channel was used to intercept throughfall for the precipitation exclusion experimental condition. To account for the rain interceptor’s effect on the light the plants received, an inverted “Λ”-shaped rain interceptor was placed over the control plots (Figure 1). Soil was excavated to a 60 cm depth around each block, separated with permeable materials and backfilled layer by layer. Each experimental sample plot was divided into reserved, sampling and observation areas. The reserved area was free of any interference except for the experimental treatment; all sampling was completed within the sampling area and various observation facilities were arranged in the observation area. A 5 m buffer zone was reserved around each plot, and sampling and observations were not carried out in the buffer zone to reduce edge effects.

2.2. Sample Collection

After two years of precipitation reduction experiments, samples were taken in January 2020 (winter) and July 2020 (summer). Eight groups of sampling points were randomly arranged at each sample plot and the top 10 cm of soil around the surface layer of the Chinese fir was excavated with a soil knife. The soil and roots of 16 samples were separated into self-sealing bags and refrigerated at the field station. After picking out gravel, roots and leaves from the fresh soil samples, they were screened through a 2 mm soil sieve and stored at 4 °C for determination of the dissolved organic carbon (DOC), microbial biomass carbon (MBC), microbial biomass nitrogen (MBN) and other indices. The remaining soil was placed in a cool place to air dry. A small amount of the air-dried soil was screened through a 0.149 mm soil sieve for soil carbon and nitrogen measurements, and the rest was stored at room temperature in self-sealing bags for determination of the glomalin and hyphal density.
The inner growth ring was designated with a diameter of 20 cm and a depth of 20 cm and used for determination of the root production and arbuscular mycorrhizal-related indices. Chinese fir roots were isolated from the inner growth ring in January and July 2020. The inner growth ring soil was removed layer by layer, keeping the roots intact as much as possible. The root samples were washed and the root tips were collected. The soil was then backfilled layer by layer into the growth ring. About 30 root tip portions were collected from each sample and stored in FAA stationary liquid at 4 °C for determination of the AMF infection rate [47].

2.3. Determination of Index Properties

We measured the soil temperature (0–10 cm) and volumetric water content using temperature sensors (T109; Campbell Scientific Inc., Logan, UT, USA) and moisture sensors (CS616; Campbell Scientific Inc., Logan, UT, USA). The soil pH was determined by a pH meter at a soil–water ratio of 1:2.5. The soil bulk density was determined by the cutting ring method. The soil mineral nitrogen was extracted with potassium chloride, and the soil ammonium nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N) concentrations in the filtrate were determined using a continuous flow analyzer (San++, SKALAR Corporation production, Breda, The Netherlands). The soil-dissolved organic carbon (DOC) and dissolved organic nitrogen (DON) were extracted using deionized water (water:soil = 4:1); the DOC was determined using a total organic carbon analyzer (TOC-VCPH, Shimadzu, Kyoto, Japan) and the DON was determined using a continuous flow analyzer. The microbial biomass carbon/nitrogen (MBC/N) was determined by chloroform fumigation extraction with potassium sulfate; the MBC was measured using a total organic carbon analyzer and the MBN was measured using a continuous flow analyzer.
The Chinese fir roots were washed of surface soil and graded according to the root order method; i.e., the most distal roots were defined as primary roots and the roots to which the primary roots were attached were secondary roots. After grading, roots were scanned by an Epson scanner and analyzed via the WinRHIZO system, using morphological indexes such as specific root length, specific surface area and tissue density. The fine roots were then dried and weighed, and the fine root production of each treatment was calculated according to the area of the growth ring [48].
The arbuscular mycorrhizal infection rate was determined by the alkaline dissociation of the roots followed by an acid fuchsin staining method. Fine roots with a length of approximately 1 cm were cleared in 10% KOH (w/v) at 90 °C for 30 min in a water bath. After the KOH was rinsed from the roots, the samples were acidified in 2% HCl (v/v) for 5 min and then submerged in the 0.01% (w/v) acid fuchsin lactate glycerin stain. The next day, stained root segments were selected and observed under a microscope and the intensity of mycorrhizal infection in each field was recorded [49]. Hyphal density was measured using vacuum pump membrane filtration. The following describes the filtration procedure: Five grams of air-dried soil were added to 800 mL of clean water and stirred thoroughly in order to disperse mycelia. Then, 20- and 400-mesh sieves were stacked and pour the suspended mixture onto the sieve surface. Pour the sifted material on the screen into a conical bottle, shake well and let it stand for 1 min, then draw a 5 mL suspension 1 cm below the liquid level. The suspension was filtrated by a 0.45 μm membrane and magenta staining solution was added to the filtrate. The intersections between the mycelium and the grid were observed and recorded [50]. The arbuscular mycorrhizal spore density was determined by an improved centrifugation method using wet sieving and decanting with sucrose: Weigh 20 g fresh soil and add 800 mL water to make a suspension. Select four 0.0385 mm, 0.058 mm, 0.106 mm and 0.25 mm stainless steel sieves and place the small aperture sieve at the bottom, according to the size of the stack. Pour the suspension slowly over the sieve surface. Remove the supernatant and debris, retain the sediment, add 50% sucrose solution, shake well, then centrifuge again. The supernatant was passed through a 0.45 µm filter membrane, the filter membrane was dried and the number of arbuscular mycorrhizal fungi spores was counted under the microscope [51,52]. The extraction and quantitative analysis of easily extractable glomalin (EE-GRSP) and total glomalin (T-GRSP) were optimized according to the methods of Jones and Wright: Weigh 1 g of air-dried soil into the sodium citrate solution and shake evenly. The supernatant was extracted at 103 kPa and 121 °C for 30 min. After centrifugation, the supernatant was collected and stored in the refrigerator at 4 °C. In 0.5 mL of the extract, 5 mL of Coomassie bright blue G250 stain was added for 10 min. Colorimetry was performed using a UV-2450 UV–visible spectrometer at a 595 nm wavelength [53,54].

2.4. Statistical Analysis

An independent sample T-test and multi-factor analysis of variance were used to analyze the significance of differences among different treatments at the same sampling time and within treatment at different sampling times. The AMF structural indices were used as response variables, and the basic physical and chemical properties of the soil were used as the environmental explanatory variables using Canoco 5.0 software (Microcomputer Power Inc. Ithaca, NY, USA). The redundancy analysis (RDA) of the AMF properties and structure was conducted using 16 samples from different sampling times. Pearson’s correlation test was used to test the pair correlation between the soil parameters and roots and AMF indexes (p < 0.05). The figures were mainly created by Origin 9.0 and the data represent the mean ± standard deviation.

3. Results

3.1. Effects of Precipitation Exclusion on Soil Physical and Chemical Properties

Precipitation exclusion decreased soil moisture by an average of 9.55%; the effects were significantly greater in summer than in winter (Figure 2). The soil contents of the DOC, DON and available phosphate (AP) in summer were significantly higher than those in winter, and precipitation exclusion in summer decreased DON by 44.91% (Table 1; p < 0.05). Two-factor analysis of variance (ANOVA) showed that the interactions between the precipitation exclusion and season, as well as the precipitation exclusion and sampling time had significant effects on the DON. Precipitation exclusion in winter significantly increased the content of NH4+ by 54.57% (p < 0.05). The effects of precipitation exclusion on the soil microbial carbon, nitrogen and phosphorus contents differed by season. The precipitation exclusion in summer significantly (p < 0.05) increased the MBC content by 16.3% but had no significant effect on the MBN or MBP (Table 1). Overall, precipitation exclusion had a stronger influence on soil properties in summer than in winter.

3.2. Effects of Precipitation Exclusion on Root Characteristics of Chinese Fir

Precipitation exclusion had no significant effects on the fine root production of Chinese fir (Table 2). The diameters of fine roots of different classes varied seasonally. In the control group, the diameters of primary and secondary roots were significantly smaller in the winter than in the summer (p < 0.05), while in the precipitation exclusion treatment, there was no seasonal difference in root diameters between winter and summer (Figure 3a). Furthermore, the multi-factor analysis also confirmed a significant interaction between seasons and treatments (p = 0.048; Table 2). Precipitation exclusion significantly increased the specific root length of secondary roots in summer (Figure 3b). Seasonal differences in the specific surface area of secondary roots were only found in the precipitation exclusion group and not the control group (p < 0.05; Figure 3c). The tissue density of primary roots was significantly higher in winter than summer (p < 0.01). Secondary root tissue density was also significantly lower in summer than in winter under precipitation exclusion conditions (p < 0.05; Figure 3d), with a marginally significant treatment effect (p = 0.074; Table 3).

3.3. Effects of Precipitation Exclusion on the Arbuscular Mycorrhizal Fungi of the Chinese Fir

The effects of precipitation exclusion on the AMF had obvious seasonal differences. In summer, the treatment significantly increased the hyphal densities of AMF (p < 0.05; Figure 4a) but significantly decreased the AMF infection rate (p < 0.05; Figure 4c). However, in winter, the only factor significantly affected by precipitation exclusion was the levels of easily extractable glomalin (Figure 5). The control group had significantly less easily extractable glomalin in the summer but the precipitation exclusion group had no significant change between seasons. Total glomalin did not differ significantly by treatment or season.

3.4. Factors Controlling the Response of Fine Root and Arbuscular Mycorrhizal Fungi to Drought

The diameters of the primary and secondary roots positively correlated with soil water content, whereas soil water content had negative effects on the tissue density of the primary and secondary roots (Figure 6a,b). The soil DOC positively correlated with root diameter, specific root length and specific root surface area but negatively impacted root tissue density (Figure 6a,b). Soil water content had a positive effect on the amounts of spores; the soil DOC positively correlated with spore amounts and hyphal density (Figure 6c). Random forest and redundancy analyses showed that the soil dissolved organic carbon and nitrogen were the key factors affecting the AMF (Figure 7). The diameters of primary and secondary roots positively correlated with soil water content, whereas soil water content had negative effects on the tissue density of primary and secondary roots (Figure 6a,b). Soil DOC positively correlated with the root diameter, specific root length and specific root surface area, but negatively impacted root tissue density (Figure 6a,b). Soil water content had a positive effect on the amounts of spores; soil DOC positively correlated with spore amounts and hyphal density (Figure 6c). Random forest and redundancy analyses showed that soil dissolved organic carbon and nitrogen were the key factors that might affect the AMF (Figure 7).

4. Discussion

It has been clearly evidenced that annual precipitation is declining during the long-term period in tropical and subtropical regions and thus amplifies the seasonal drought effect in our study area [44]. Plant roots and mycorrhizal fungi are the main channels for material exchange between plants and soils. When soil moisture decreases, plants will invest more carbon below ground to the roots and mycorrhizae [55]. Plants may adapt to environmental stressors by making resource investment trade-offs for roots and arbuscular mycorrhizal fungi [56]. There are many criteria for the comprehensive measurement of root quality, including fine root production, fine root diameter, specific root length, specific surface area, tissue density and production. These can reflect how plants adapt to stressors. For example, under drought conditions, plants can change their investment in roots to regulate their nutrient absorption efficiency [57,58]. The results of this study showed that under normal conditions, the diameters of primary and secondary roots of Chinese fir were significantly higher in summer than in winter, but there were no significant seasonal differences under the precipitation exclusion treatment (Figure 3a). On the other hand, there was only a significant increase in the specific surface area of secondary roots in the summer under the precipitation exclusion condition, with no change observed in the control group. These results allowed us to make a postulate that in summer droughts, Chinese fir responds to drought stress by decreasing the diameter and tissue density of primary and secondary roots, while increasing the specific surface area of secondary roots.
Studies have shown that a functional complementation strategy exists between plant roots and mycorrhizae, but the degree of complementarity between the two changes as environmental conditions change [59,60]. It has been found that plants dominated by fine roots tend to obtain nutrients through roots, whereas species dominated by coarse roots rely more on mycorrhizal fungi [61,62]. As a fine root-dominated plant, Chinese firs usually obtain nutrients and moisture from roots. In the control group, the diameters of primary and secondary roots were significantly smaller in the winter than in the summer (p < 0.05), while in the precipitation exclusion treatment, there was no seasonal difference in root diameters between winter and summer (Figure 3a). Furthermore, there were significant interactions between the season and treatment (p = 0.048; Table 3), indicating that precipitation exclusion reduced the seasonal difference in root diameter. Therefore, we concluded that drought decreased the root diameter of the Chinese fir, indicating that drought may make Chinese fir more dependent on the nutrient function of Chinese fir roots. However, some studies believe that most tree species will change their root nutrient acquisition in the face of adversity; i.e., they may collaborate with the low-cost production of mycorrhizal fungal hyphae to obtain nutrients and moisture [63]. This study found that drought significantly changed the functional characteristics of the AMF from a Chinese fir plantation and the effects were seasonal. In summer, precipitation exclusion significantly decreased the AMF infection rate and increased hyphal density; on the other hand, precipitation exclusion in winter had no significant effect on the AMF infection rate, hyphal density or spore number. These results indicated that Chinese fir responded to drought by increasing its hyphal density and not its mycorrhizal infection rate. Chinese fir may adapt to drought conditions by increasing low-cost mycorrhizal fungal hyphae to maintain plant growth and physiological function.
The decrease in the mycorrhizal infection rate of Chinese fir during a drought may be due to the high sensitivity of AMF physiology in response to water conditions. Because AMF is an aerobic fungus that develops best in moderate soil moisture, excessively humid and dry soil environments may adversely affect AMF infection and symbiosis [22]. High summer temperatures and reduced rainfall can exacerbate soil moisture shortages and lead to extreme drought conditions, especially in tropical and subtropical regions. The AMF infection rate of plant roots decreases as drought stress is prolonged [64]. This reflects the cost–benefit theory that under stress, plants minimize the cost of obtaining soil resources while maximizing their use of fine roots and mycorrhizae to increase the nutrient acquisition benefits [17]. A low mycorrhizal infection rate does not necessarily represent a low mycorrhizal absorption efficiency, since the number of mycorrhizal hyphae present to absorb nutrients may still vary considerably [9]. Under stress, plants may “select” to inhibit AMF growth [65,66,67], leaving nutrient absorption to be carried out using only the mycorrhizae that can directly obtain carbon from soil organic matter [68]. In this study, the Chinese fir enhanced soil occupation by increasing its hyphal density, absorption area and accessibility while decreasing its mycorrhizal infection rate. According to our RDA result, we can partly conclude that the functional characteristics of the AMF might be influenced by the availability of carbon sources and organic nitrogen in the soil (Figure 7). Drought reduced the resource consumption of the Chinese fir from mycorrhizal infection but enhanced the complementary strategy of resource acquisition from the roots and mycorrhizal fungi by increasing the low-cost investments of the hyphae and the root’s resource acquisition ability. This helped the Chinese fir to cope with drought stress and better maintain normal growth.

5. Conclusions

Simulated drought did not significantly affect the root production of the Chinese fir, but it significantly decreased the root diameter and increased the specific surface area of the roots. This might have improved the Chinese fir roots’ ability to absorb moisture under drought conditions. Drought also had a great effect on the AMF of the Chinese fir. Summer drought significantly decreased the AMF infection rate and increased hyphal density, which indicated that drought may reduce the investment consumption of mycorrhizae and expand the nutrient acquisition area of hyphae. Therefore, under drought conditions, the Chinese fir might increase the moisture absorption capacity of its roots by decreasing its root diameter and increasing its specific surface area; at the same time, mycorrhizae might increase their low-cost soil occupation to maintain their absorption of moisture and nutrients. Therefore, it is crucial to understand the carbon and nutrient cycles of ecosystems. We postulate that drought might enhance the cooperative strategy of nutrient and moisture absorption by the roots and mycorrhizae of the Chinese fir and improve the resistance of Chinese fir growth to drought.

Author Contributions

J.D., Y.J., M.L. and W.L. wrote the manuscript; M.L. and J.X. designed and supervised the experiment; G.C., Y.Y. and J.X. improved the manuscript; J.D., Y.J., X.L., X.X., C.C. and Z.Y. carried out the measurements following the field incubation and collected and analyzed the data. 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 (No. 32001169), the National Key Research and Development Program of China (Nos. 2016YFD0600204 and 2021YFD220040303) and the Public Welfare Projects Foundation of Fujian Province, China (2021R1002004).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank Jiayu Li, Shiliang Zhang, Chaoyue Ruan, Anni Cao and Haohao Su for helping with the laboratory and field work. We would like to thank Joseph Elliot at the University of Kansas for his assistance in the English language and grammatical editing of the manuscript.

Conflicts of Interest

The authors declare that they have no competing interests.

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Figure 1. Overview of rainfall exclusion experimental plots. (a) Aerial view of the study plots, (b) precipitation reduction plots (PR, −50% of precipitation) and (c) control plots (CT).
Figure 1. Overview of rainfall exclusion experimental plots. (a) Aerial view of the study plots, (b) precipitation reduction plots (PR, −50% of precipitation) and (c) control plots (CT).
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Figure 2. Changes in the (a) soil temperature and (b) moisture of the Chinese fir plantation. The red line represents the control plots (CT); the black line represents the precipitation reduction plots (PR).
Figure 2. Changes in the (a) soil temperature and (b) moisture of the Chinese fir plantation. The red line represents the control plots (CT); the black line represents the precipitation reduction plots (PR).
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Figure 3. Effects of precipitation exclusion on fine root morphological characteristics. (a) Fine root diameter, (b) specific root length, (c) specific root surface area and (d) root tissue density. The right and left panels represent primary and secondary roots, respectively. Values are presented as the mean ± standard deviation (n = 4). Different uppercase letters indicate a significant difference between winter and summer within the control (CT) or precipitation reduction (PR) treatments; different lowercase letters indicate a significant difference between the CT and PR treatments within the same season (p < 0.05).
Figure 3. Effects of precipitation exclusion on fine root morphological characteristics. (a) Fine root diameter, (b) specific root length, (c) specific root surface area and (d) root tissue density. The right and left panels represent primary and secondary roots, respectively. Values are presented as the mean ± standard deviation (n = 4). Different uppercase letters indicate a significant difference between winter and summer within the control (CT) or precipitation reduction (PR) treatments; different lowercase letters indicate a significant difference between the CT and PR treatments within the same season (p < 0.05).
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Figure 4. Effects of precipitation exclusion on (a) hyphal density, (b) spore density and (c) infection rate. Different uppercase letters indicate a significant difference between the control (CT) and precipitation reduction (PR) treatments within the same season; different lowercase letters indicate a significant difference between the dry and wet seasons within the same treatment (p < 0.05).
Figure 4. Effects of precipitation exclusion on (a) hyphal density, (b) spore density and (c) infection rate. Different uppercase letters indicate a significant difference between the control (CT) and precipitation reduction (PR) treatments within the same season; different lowercase letters indicate a significant difference between the dry and wet seasons within the same treatment (p < 0.05).
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Figure 5. Effects of precipitation exclusion on (a) easily extractable glomalin (EE-GRSP) and (b) total glomalin (T-GRSP). Different uppercase letters indicate a significant difference between the control (CT) and precipitation reduction (PR) treatments within the same season; different lowercase letters indicate a significant difference between the dry and wet seasons within the same treatment (p < 0.05).
Figure 5. Effects of precipitation exclusion on (a) easily extractable glomalin (EE-GRSP) and (b) total glomalin (T-GRSP). Different uppercase letters indicate a significant difference between the control (CT) and precipitation reduction (PR) treatments within the same season; different lowercase letters indicate a significant difference between the dry and wet seasons within the same treatment (p < 0.05).
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Figure 6. Correlations between the (a) primary root, (b) secondary root and (c) arbuscular mycorrhiza and soil properties. SWC: soil water content; DOC: dissolved organic carbon; DON: dissolved organic nitrogen; AP: available phosphate; NH4+: ammonium nitrogen; NO3−: nitrate nitrogen; MN: mineral nitrogen; MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; MBP: microbial biomass phosphate. * p < 0.05; ** p < 0.01; *** p < 0.001.
Figure 6. Correlations between the (a) primary root, (b) secondary root and (c) arbuscular mycorrhiza and soil properties. SWC: soil water content; DOC: dissolved organic carbon; DON: dissolved organic nitrogen; AP: available phosphate; NH4+: ammonium nitrogen; NO3−: nitrate nitrogen; MN: mineral nitrogen; MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; MBP: microbial biomass phosphate. * p < 0.05; ** p < 0.01; *** p < 0.001.
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Figure 7. Redundancy analysis of arbuscular mycorrhizal fungi and environmental factors. SWC: soil water content; DOC: dissolved organic carbon; DON: dissolved organic nitrogen; NH4+: ammonium nitrogen; CT: control; PR: precipitation reduction.
Figure 7. Redundancy analysis of arbuscular mycorrhizal fungi and environmental factors. SWC: soil water content; DOC: dissolved organic carbon; DON: dissolved organic nitrogen; NH4+: ammonium nitrogen; CT: control; PR: precipitation reduction.
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Table
Table 1. Effects of precipitation exclusion on soil physical and chemical properties.
Table 1. Effects of precipitation exclusion on soil physical and chemical properties.
WinterSummerTreatmentSeasonInteraction
CTPRCTPRFPFPFP
Moisture11.08
± 1.86 Ab		9.69
± 0.91 Ab		20.07
± 1.98 Aa		17.47
± 1.75 Aa		5.660.03599.88 0.0000.52 0.486
pH4.25
± 0.05 Ab		4.30
± 0.06 Aa		4.36
± 0.05 Aa		4.37
± 0.03 Aa		1.41 0.259 14.84 0.0020.62 0.445
DOC
(mg kg−1)		20.91
± 1.15 Ab		22.06
± 1.43 Ab		38.43
± 4.97 Aa		40.08
± 5.16 Aa		0.570.465 92.30 0.0000.02 0.896
DON
(mg kg−1)		0.98
± 0.13 Ab		0.89
± 0.09 Ab		4.20
± 0.39 Aa		2.90
± 1.17 Ba		4.99 0.04570.58 0.0003.82 0.013
AP
(mg kg−1)		1.31
± 0.19 Aa		1.02
± 0.21 Aa		0.88
± 0.1 Ab		1.17
± 0.26 Aa		0.002 0.967 1.94 0.189 8.49 0.075
NH4+
(mg kg−1)		3.00
± 0.92 Bb		4.64
± 0.86 Aa		5.96
± 0.4 Aa		5.88
± 0.68 Aa		4.38 0.058 31.81 0.0005.32 0.040
NO3−
(mg kg−1)		3.79
± 0.53 Aa		3.83
± 0.38 Aa		3.97
± 0.48 Aa		3.90
± 0.63 Aa		0.01 0.940 0.22 0.647 0.04 0.837
MN
(mg kg−1)		6.24
± 1.55 Bb		8.47
± 1.05 Aa		9.93
± 0.82 Aa		9.78
± 0.38 Aa		3.97 0.070 23.07 0.0005.23 0.041
MBC
(mg kg−1)		464.51
± 60.23 Aa		451.33
± 66.31 Aa		445.45
± 46.33 Aa		383.0
± 19.47 Bb		2.17 0.167 2.900.115 0.920.356
MBN
(mg kg−1)		44.38
± 3.56 Aa		50.77
± 9.87 Aa		46.25
± 6.96 Aa		41.31
± 5.54 Aa		0.04 0.837 1.22 0.292 2.72 0.125
MBP
(mg kg−1)		13.20
± 1.75 Ab		12.25
± 1.89 Ab		18.27
± 0.84 Aa		16.76
± 1.40 Aa		2.590.13339.42 0.0000.140.718
DOC: dissolved organic carbon; DON: dissolved organic nitrogen; AP: available phosphate; MN: mineral nitrogen; MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; MBP: microbial biomass phosphate. Different uppercase letters indicate a significant difference between the control (CT) and precipitation reduction (PR) treatments within the same season; different lowercase letters indicate a significant difference between seasons within the same treatment (p < 0.05).
Table
Table 2. Effects of precipitation exclusion on fine root production between the control (CT) and precipitation reduction (PR) treatments. Values are presented as the means ± standard deviation (n = 4).
Table 2. Effects of precipitation exclusion on fine root production between the control (CT) and precipitation reduction (PR) treatments. Values are presented as the means ± standard deviation (n = 4).
Root Ordinal TreatmentFine Root Production
Primary rootCT1.28 ± 0.25
PR1.37 ± 0.38
Secondary rootCT1.25 ± 0.58
PR1.03 ± 0.9
Table
Table 3. Multi-factor analysis of variance for testing the effect of precipitation exclusion, season and their interaction on fine root morphological characteristics. Bold type means significance.
Table 3. Multi-factor analysis of variance for testing the effect of precipitation exclusion, season and their interaction on fine root morphological characteristics. Bold type means significance.
Fine Root DiameterSpecific Root LengthSpecific Root Surface AreaRoot
Density
Treatment (T)F-value0.6620.8140.0203.489
p-value0.4240.3760.8880.074
Diameter class (D)F-value27.94627.4524.1409.551
p-value<0.001<0.0010.0530.005
Season (S)F-value18.2264.76648.20185.990
p-value<0.0010.039<0.001<0.001
T × DF-value0.0030.6160.9270.055
p-value0.9580.4400.3450.816
T × SF-value4.3305.1753.9811.203
p-value0.0480.0320.0570.284
D × SF-value0.2470.7850.0162.036
p-value0.6240.3840.8990.166
T × D × SF-value0.0041.8282.6631.254
p-value0.9500.1890.1160.274
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Dong, J.; Jiang, Y.; Lyu, M.; Cao, C.; Li, X.; Xiong, X.; Lin, W.; Yang, Z.; Chen, G.; Yang, Y.; et al. Drought Changes the Trade-Off Strategy of Root and Arbuscular Mycorrhizal Fungi Growth in a Subtropical Chinese Fir Plantation. Forests 2023, 14, 114. https://doi.org/10.3390/f14010114

AMA Style

Dong J, Jiang Y, Lyu M, Cao C, Li X, Xiong X, Lin W, Yang Z, Chen G, Yang Y, et al. Drought Changes the Trade-Off Strategy of Root and Arbuscular Mycorrhizal Fungi Growth in a Subtropical Chinese Fir Plantation. Forests. 2023; 14(1):114. https://doi.org/10.3390/f14010114

Chicago/Turabian Style

Dong, Jie, Yongmeng Jiang, Maokui Lyu, Cong Cao, Xiaojie Li, Xiaoling Xiong, Weisheng Lin, Zhijie Yang, Guangshui Chen, Yusheng Yang, and et al. 2023. "Drought Changes the Trade-Off Strategy of Root and Arbuscular Mycorrhizal Fungi Growth in a Subtropical Chinese Fir Plantation" Forests 14, no. 1: 114. https://doi.org/10.3390/f14010114

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