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Article

Rhizosphere Microbe Affects Soil Available Nitrogen and Its Implication for the Ecological Adaptability and Rapid Growth of Dendrocalamus sinicus, the Strongest Bamboo in the World

by
Peitong Dou
1,†,
Qian Cheng
1,†,
Ning Liang
1,
Changyan Bao
1,
Zhiming Zhang
1,
Lingna Chen
2,* and
Hanqi Yang
1,3,*
1
Institute of Highland Forest Science, Chinese Academy of Forestry, Kunming 650233, China
2
College of Life Science, Xinjiang Normal University, Xinyi Road, Shayibake District, Urumqi 830054, China
3
Key Laboratory of Breeding and Utilization of Resource Insects, National Forestry and Grassland Administration, Kunming 650233, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2023, 24(19), 14665; https://doi.org/10.3390/ijms241914665
Submission received: 23 August 2023 / Revised: 16 September 2023 / Accepted: 26 September 2023 / Published: 28 September 2023
(This article belongs to the Special Issue Advanced Research in Plant-Fungi Interactions)
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Abstract

:
The interaction between soil microbes and plants has a significant effect on soil microbial structure and function, as well as plant adaptability. However, the effect of soil micro-organisms on ecological adaption and rapid growth of woody bamboos remains unclear. Here, 16S rRNA and ITS rRNA genes of rhizosphere micro-organisms were sequenced, and the soil properties of three different types of Dendrocalamus sinicus were determined at the dormancy and germination stages of rhizome buds. The result showed that each type of D. sinicus preferred to absorb ammonia nitrogen (NH4+-N) rather than nitrate nitrogen (NO3−-N) and required more NH4+-N at germination or rapid growth period than during the dormancy period. In total, nitrogen fixation capacity of soil bacteria in the straight type was significantly higher than that in the introduced straight type, while the ureolysis capacity had an opposite trend. Saprophytic fungi were the dominant fungal functional taxa in habitat soils of both straight and introduced straight type. Our findings are of great significance in understanding how soil microbes affect growth and adaptation of woody bamboos, but also for soil management of bamboo forests in red soil.

1. Introduction

Red soil is an important soil type in southern China. Due to soil parent material, high temperature, high humidity and other climatic factors, red soil is generally characterized by high Fe contents, low pH, low contents of organic carbon and soil nutrient elements, as well as strong erosion [1,2]. Nitrogen (N) is one of the major elements essential for plant growth [3]. Ammonia nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N) are the main forms of N uptake by plants, originating primarily from microbial processes of ammonification and nitrification [4,5]. Noticeably, soil N availability in terrestrial ecosystems commonly limits plant growth [6] and is influenced by the interaction between plants and rhizosphere microbes [5]. Rhizosphere is the interface between plant roots and soil [7]. As an important part of the rhizosphere system, rhizosphere micro-organisms are considered as an important part of the extended plant phenotypes, which could greatly promote the interaction between plants and the environment [8]. In general, plants recruit micro-organisms to the rhizosphere by releasing secretions (such as sugars, organic acids) [5], which will increase rhizosphere microbial abundance and activity and affect its community structure and function [9]. Conversely, rhizosphere micro-organisms also help plants absorb nutrients from the soil [10], improve plant growth and development [11], protect host plants from pathogens [12] and increase their tolerance to abiotic stresses [13,14]. Meanwhile, a growing number of studies also indicate that spatial variation in soil microbe communities may affect local adaptation patterns of plants [8,15,16]. Abiotic environmental variation, such as soil nutrients and aridity, would interact with microbe communities and affect plant fitness [17,18]. In summary, interaction among soil, plants and soil microbes plays a critical role in plant nutrition acquisition, healthy growth and geographical range margins [19,20,21,22].
Woody bamboo belongs to the bamboo subfamily of Gramineae (Poaceae), with ca. 80 genera and more than 1500 species [23]. Yunnan Province of China is a world-renowned laterite plateau and possesses more than 220 native woody bamboos from 28 genera occurring in the red soil [24]. Considering that woody bamboos are of crucial economic, ecological and cultural value in their distribution area [24], the introduction and cultivation of excellent bamboo resources have attracted increasing interest in both academia and industry in recent years [25]. The rapid growth of young culms is one of the most striking biological features of woody bamboos [26,27]. Due to low contents of organic carbon and soil nutrient in acidic red soil [1], rapidly growing bamboo plants may be more susceptible to the influence of rhizosphere micro-organisms on their nutrient absorption [11]. Furthermore, as one of the most important members of the bamboo forest ecosystem, the structure and function of soil microbial communities in bamboo rhizosphere have also received increasing attention from scientists. Recently, it was reported that rhizosphere micro-organisms were involved in carbohydrate degradation and nitrogen fixation process of woody bamboos rhizomes, which contributed to the annual shooting of Cephalostachyum pingbianense [11]. The bacterial genera Flavobacterium, Bacillus and Stenotrophomonas might affect the flowering time of Moso bamboo (Phyllostachys edulis) by regulating the effective utilization of nitrogen [28]. Supplementing azotobacter and vesicular-arbuscular mycorrhizae fungi could increase the biomass of Bambusa vulgaris [29]. These studies suggested that soil micro-organisms can affect the growth, phenology and reproduction characteristics of woody bamboos. However, the effect of micro-ecological factors, especially soil micro-organisms, on ecological adaption and rapid growth of woody bamboos remains unclear.
Remarkably, Dendrocalamus sinicus, endemic to southern and southwestern Yunnan, China, is the strongest bamboo, which has been recorded in the world, with a diameter at breast height (DBH) of 30 cm and a height of nearly 30 m. The average fresh weight of the culm is 100–150 kg, and the yield of culm timber per unit area was five to eight times higher than that of Phyllostachys edulis, the most important economic bamboo species in the world [30]. These excellent characteristics make D. sinicus one of the most promising economic bamboo species in southern China. In nature, D. sinicus has two main stable culm-shape variants: the straight type and bending type [31]. They thrive in lateritic soil and inhabit environments, which share notable similarities. However, the narrow natural distribution of D. sinicus poses a limitation to its cultivation and utilization [25]. In the previous studies, we investigated its biological characteristics, including the mating system [32] and culm development [26,31]. Furthermore, our study investigated the impact of climate factors on the distribution of D. sinicus, revealing a substantially broader potential distribution range compared to its current range [25]. To identify the potential contribution of the rhizosphere microbes in the spatial distribution and growth of D. sinicus, we performed high-throughput sequencing of ITS rRNA and 16S rRNA genes from soil samples, determined some key soil properties and investigated the DBH and bamboo shooting ratio (BSR) in different types of D. sinicus (Figure 1). This study had two aims: (1) to explore the influence of micro-ecological factors on the success of woody bamboos introduction; (2) to determine the nitrogen absorption characteristics of D. sinicus and identify the potential microbial taxa, which are conducive to its rapid growth.

2. Results

2.1. Soil Properties and Biological Characteristics of Various D. sinicus at Different Stages

The soil properties of different D. sinicus types were analyzed (Table 1). In May, the soil pH was significantly higher for each D. sinicus type compared to August (p < 0.05). The introduced straight type exhibited significantly higher soil organic carbon (SOC) content in May compared to August (p < 0.05). In each period, the SOC content ranked highest in the straight type, followed by the bending type and then the introduced straight type, with significant differences observed (p < 0.05). There was no significant difference in the soil AP content for the bending type between May and August (p > 0.05). However, the soil AP content for both the straight and introduced straight types was significantly higher in May compared to August (p < 0.05). In each period, the straight type had the highest soil available phosphorus (AP) content, followed by the introduced straight type and then the bending type, with significant differences observed (p < 0.05). The introduced straight type had significantly lower soil available potassium (AK) content compared to the bending and straight types in each stage (p < 0.05), suggesting a higher AK absorption by D. sinicus in native areas. In May, the soil NO3−-N content for the bending type was significantly higher than that in August (p < 0.05) and consistently highest at two periods (p < 0.05). Conversely, the soil NH4+-N content for all types was significantly lower in May compared to August (p < 0.05), indicating increased NH4+-N absorption during shooting and rapid growth period. The introduced straight type had significantly lower soil water content (SWC) compared to the bending and straight types in each period (p < 0.05). Apart from the straight type in August, which exhibited significantly higher SWC than that in May (p < 0.05), there were no significant differences in SWC between May and August for other types (p > 0.05). There was no significant difference in the C: N among different types during the same period (p > 0.05). However, the NH4+: NO3− of the straight type was significantly higher than that of the bending type and the introduced straight type during the same period (p < 0.05). The biological characteristics of various D. sinicus were compared as follows: the straight type had the largest DBH and bamboo stem weight (BSW), followed by the bending type and then the introduced straight type, with significant differences observed (p < 0.05). The introduced straight type showed a significantly lower BSR compared to both the bending type and the straight type.

2.2. The α Diversity and β Diversity of Soil Microbial Community

A total of 1,614,330 bacterial and 2,554,342 fungal raw reads were obtained from 30 soil samples. After the paired-end reads were spliced and filtered, clean tags for 1,383,699 bacteria and 2,307,941 fungi were obtained. These tags were classified into 2577 bacterial and 2565 fungal OTUs. One-way analysis of variance (ANOVA) was performed to compare the α diversity of microbial communities (bacterial and fungal) among the soil samples (Figure 2). The Shannon index values for bacteria in the rhizosphere soil of both bending and straight types were significantly higher in May compared to August (Figure 2C). In May, no significant difference in the α diversity of bacterial community was observed among the different soil samples (p > 0.05). However, in August, the Shannon index of bacterial community in the rhizosphere soil of the introduced straight type was significantly higher than in other types (p < 0.05). The fungal Sobs and Chao1 index values for the straight type were significantly lower in May compared to August (p < 0.05) (Figure 2B,F). In May, the fungal α diversity index in the rhizosphere soil of the bending type was significantly higher than that of the straight type (p < 0.05) (Figure 2B,D,F). However, in August, there was no significant difference in the fungal α diversity index among the different soil samples (p > 0.05).
The PCoA analysis demonstrated a clear differentiation of microbial communities in various rhizosphere soil samples. Specifically, the fungal PCoA (Figure 2H) exhibited a more distinct separation among samples compared to the bacterial PCoA (Figure 2G). Furthermore, the ANOSIM analysis indicated significant effects of the D. sinicus type and growth period on the structure of soil bacterial (r = 0.8441, p = 0.001) and fungal communities (r = 0.8646, p = 0.001) (Figure S1).

2.3. Soil Microbial Community Composition and Function

The microbial community structure and function in the rhizosphere soil varied among different types. Actinobacteria and Proteobacteria were the dominant bacterial phyla, together comprising over 50% of the bacterial communities in each soil sample (Figure 3A, Table S1). The relative abundance of Actinobacteria peaked in August for the bending type (44.19%) and reached its lowest point in May for the straight type (22.99%) (Figure 3A, Table S1). In contrast, the relative abundance of Proteobacteria peaked in May for the bending type (32.93%) and reached its lowest point in August for the introduced straight type (15.47%). The relative abundance of Actinobacteria in each type increased from May to August, while the relative abundance of Proteobacteria decreased during the same period. The dominant bacterial genera in all soil samples were Bacillus, Bradyrhizobium, Mycobacterium, Kitasatospora, Sphingomonas, RB41, Gaiella and Haliangium (Figure 3C, Table S2). As for fungi, the dominant fungal phyla were Ascomycota and Basidiomycota, accounting for over 90% of the fungal communities in each soil sample (Figure 3B, Table S1). The relative abundance of Ascomycota peaked in May for the bending type (68.57%) and reached its lowest point in May for the straight type (43.28%). Moreover, the relative abundance of Basidiomycota was highest in May for the straight type (52.09%) and lowest in May for the bending type (23.42%). The dominant fungal genera in all soil samples were Cladophialophora, Trichoderma and Penicillium (Figure 3D, Table S2). In May, the rhizosphere soil of the bending type had significantly higher abundances of Apiotrichum, Fusarium, Exophylla, Acremonium, Cordana and Neocosmospora compared to the straight type (p < 0.05) (Table S2). Conversely, Tremelodendropsis, Archaeorhizogenes, Camarophyllus and Leohumicola exhibited significantly higher abundances in the rhizosphere soil of the straight type compared to the bending type (p < 0.05). This result indicates that fungal communities beneficial to the growth of bending and straight types developed in their respective rhizospheres under natural conditions.
Functional predictions of the bacterial community indicated that chemoheterotrophy, aerobic chemoheterotrophy, nitrogen fixation and nitrate reduction were the primary soil ecological functions among the rhizosphere soil samples (Figure 4A). This result suggested that the rhizosphere bacterial community of D. sinicus hada high capacity for biological nitrogen fixation. The abundance of cellulolysis in all soil samples was notably high in August, indicating a strong carbohydrate conversion ability of the rhizosphere bacterial community during the shooting and rapid growth period. Furthermore, the introduced straight type exhibited significantly higher ureolysis abundance compared to other samples in August (p < 0.05) (Figure 4A, Table S3). The rhizosphere bacterial taxa were classified into nine phenotypes (Figure 4C), showing a wide variation in the relative abundance of different phenotypic bacteria within each sample. For instance, the relative abundance of aerobic bacteria was much higher than that of anaerobic bacteria. Notably, the relative abundance of potentially pathogenic bacteria in May was significantly higher in the straight type compared to the introduced straight type (p < 0.05) (Figure 4D).
Figure 4B shows the functional composition of fungal communities in six soil samples and three types of trophic modes: saprotroph, symbiotroph and pathoproth. Saprotrophic fungi dominated the rhizosphere soil samples, constituting over 80.93% of the community (Table S4). This group included various types, such as undefined saprotrophs, soil saprotrophs and wood saprotrophs. Pathogens comprised 4.39% to 12.46% of the community, mainly consisting of animal and plant pathogens. Symbiotrophs represented the smallest proportion, ranging from 1.22% to 14.69%. In particular, the straight type had a symbiotroph proportion of 14.69% in August (Table S4), while the introduced straight type had a symbiotroph proportion of 3.72% in August.

2.4. Soil Microbial Taxa with Significant Differences

LEfSe analysis was used to identify microbial taxa with significant abundance differences among the 30 most abundant genera in soil samples (Figure 5). This analysis revealed 26 taxonomic clades, which displayed differential abundance as bacterial biomarkers (Figure 5A, Table S5). Soil samples of the straight type in May and August exhibited the fewest bacterial taxa with significant differences, consisting of two genera each. In May, the two genera were Candidatus_Solibacter and Anaeromyxobacter, while in August, Bacillus and Bradyrhizobium were identified. In contrast, soil samples of the bending type in May displayed the most bacterial taxa, including Pedomicrobium, Solirubrobacter, Gaiella, Micromonospora, Arthrobacter, Nocardioides, Reyranella, RB41, MND1 and Haliangium.
Meanwhile, a total of 20 fungal clades with significant abundance differences were identified in this study (Figure 5B, Table S5). Specifically, soil samples of the straight type in August displayed the fewest fungal taxa, with only one genus, Pseudallescheria, showing notable variation. In contrast, soil samples of the bending type in May exhibited the most fungal taxa, including seven genera: Gonytrichum, Acremonium, Neocosmospora, Mortierella, Apiotrichum, Exophiala and Fusarium.

2.5. Soil Properties Affecting the Diversity and Structure of Microbial Community

The correlation analysis between soil properties and microbial α diversity indices revealed significant associations. Bacterial Sobs and Shannon index showed negative correlations with SWC and NH4+-N (p < 0.05), and bacterial Chao1 indices exhibited a negative correlation with SWC (p < 0.05) (Figure 6A). In fungal communities, the pH displayed a positive correlation with the Shannon index (p < 0.05), and soil AK and NH4+-N contents were positively correlated with Sobs and Chao1 indices (p < 0.05) (Figure 6B). Conversely, soil AP content was negatively correlated with all α diversity indices of fungi (p < 0.05). A positive correlation was observed between SWC and fungal Chao1 index (p < 0.05) (Figure 6B). RDA analysis revealed that the SOC, pH and NH4+-N were the primary soil properties affecting the structure of the bacterial community (r2 = 0.7487, p = 0.001 for SOC; r2 = 0.7109, p = 0.001 for pH; r2 = 0.6989, p = 0.001 for NH4+-N) (Figure 6C, Table S6). Similarly, soil AK, SOC, AP and pH were identified as the main factors affecting the structure of the fungal community (r2 = 0.8171, p = 0.001 for AK; r2 = 0.8020, p = 0.001 for SOC; r2 = 0.7794, p = 0.001 for AP; r2 = 0.7727, p = 0.001 for pH) (Figure 6D, Table S6). In particular, soil pH and SOC were found to affect the structure of both bacterial and fungal communities.

2.6. Correlations of Microbial Genera with Soil Properties and Biological Characteristics of D. sinicus

The correlation analysis between the 30 most abundant microbial genera and soil properties revealed significant associations (Figure 7). In bacterial communities, Reyranella, Paenibacillus, Micromonospora, Nocardioides, Luedemannella, Pedomicrobium, Bradyrhizobium showed positive correlations with soil NH4+-N content (p < 0.05). Meanwhile, most of these genera showed positive correlations with SWC, SOC, DBH and BSW (p < 0.05) (Figure 7A). In the fungal community, Penicillium, Entoloma, Hygrocybe, Tremellodendropsis, Archaeorhizomyces, Camarophyllus and Leohumicola were positively correlated with soil AP content (p < 0.05). Trichoderma, Mortierella, Trechispora, Apiotrichum, Sarcodon, Exophiala, Pseudallescheria, Cordana, Gonytrichum and Acremonium showed positive correlations with soil AK content (p < 0.05). Moreover, Mortierella, Trechispora, Apiotrichum, Exophiala, Tremellodendropsis exhibited positive correlations with SWC, SOC, DBH and BSW (p < 0.05). Trichoderma, Mortierella, Trechispora, Apiotrichum, Exophiala, Acremonium and Cordana displayed positive correlations with soil NH4+-N content in fungal communities (Figure 7B).

2.7. The Relationship between Selected Soil Properties and the Biological Characteristics of D. sinicus

The regression analysis revealed that soil NH4+-N content explained 52.43% of the variation in BSW (p < 0.05) (Figure 8B) and 63.44% of the variation in BSR (p < 0.05) (Figure 8F). Conversely, soil NO3−-N content explained only 7.05% of the variation in BSW (p < 0.05) (Figure 8A) and 61.27% of the variation in BSR (p < 0.05) (Figure 8E). Furthermore, the C: N and NH4+: NO3− demonstrated a lower contribution to variation in BSW and BSR compared to the soil NH4+-N. The C: N and NH4+: NO3− explained 10.82% and 31.04% of the variation in BSW (p < 0.05) (Figure 8C,D), as well as 23.73% and 34.94% of the variation in BSR (p < 0.05) (Figure 8G,H). This result indicated that the NH4+-N availability had a greater impact on the formation of biological traits of D. sinicus.

3. Discussion

3.1. Characteristics of NH4+-N Absorption by D. sinicus

Soil nitrogen availability is a critical factor limiting forest land productivity [6,33]. NH4+-N and NO3−-N are the primary nitrogen forms absorbed by plants, with plant species exhibiting an absorption preference for NH4+-N or NO3−-N [6,34,35]. This study showed that each type of D. sinicus had an absorption preference for NH4+-N, as evidenced by the higher NH4+-N content in the rhizosphere soil compared to NO3−-N during both dormancy and shooting periods of the underground rhizome. The preference was likely attributed to distinct modes of absorption for NH4+-N and NO3−-N by roots, with NH4+-N uptake relying on ion exchange and NO3−-N uptake involving an active process [36]. NH4+-N could affect the effective number of carriers for absorption of NO3−-N [37], which may reduce NO3−-N absorption in plants. Meanwhile, plants exhibited a greater efficiency in converting NH4+-N into amides or amino acids compared to NO3−-N, and the energy requirement for NH4+-N absorption and assimilation was significantly lower than that of NO3−-N in plants [36]. Additionally, during the rainy season, NO3−-N was susceptible to leaching and runoff, leading to significant loss and transport of this nitrogen compound [11,35].
The uptake of NH4+-N and NO3−-N varies across different growth stages in plants [3]. In rice (Oryza sativa L.), NH4+-N played a dominant role during the vegetative growth stage, accounting for 68.9% of the total absorbed nitrogen. The absorption ratio of the two is around one during the reproductive growth period [3]. In this study, the NH4+: NO3− of different D. sinicus types showed an increasing trend from May to August, aligning with the corresponding changes in soil NH4+-N content (Table 1). This result suggested that a higher NH4+: NO3− was more crucial for the rapid growth of D. sinicus compared to the dormancy period of the underground rhizome. Moreover, a higher NH4+: NO3− was found to enhance photosynthetic characteristics and promote root growth in bamboo plants [38,39]. The regression analysis also revealed that the NH4+: NO3− explained 31.04% of the variation in BSW (p < 0.05), as well as 34.94% of the variation in BSR (p < 0.05) (Figure 8D,H), and soil NH4+-N content exhibited the highest contribution rate to both BSW and BSR of D. sinicus. Therefore, it was recommended to apply NH4+-N during the rapid growth period of D. sinicus in production practices.
The soil C: N is an indicator of the equilibrium between soil carbon and nitrogen nutrition [40]. Typically, the soil C: N is around 25:1 [41]. In this study, the C: N in the rhizosphere soil varied between 11.39 and 15.34. A lower soil C: N enhanced the mineralization and release of N, which was available for plant uptake [42]. Soil parent material, soil type, topography and land use type are influential factors affecting the soil C: N, with minimal variation observed under similar conditions [40]. Therefore, the similar soil parent material and types in the habitats of various D. sinicus could account for the absence of a significant difference in soil C: N at the same growth stage. This finding provided valuable insights for selecting suitable planting locations for D. sinicus.

3.2. Influence of Rhizosphere Microbes on NH4+-N Availability in Red Soil

The natural distribution of D. sinicus is limited to the red soil habitat of Yunnan, China [30]. Red soil develops in warm temperate and humid climates and is characterized by low pH and soil nutrient availability [2]. In this study, the soil samples displayed a slightly acidic condition, with pH values ranging from 5.58 to 6.13. The RDA analysis confirmed that soil pH significantly affected both fungal (r2 = 0.7727, p = 0.001) and bacterial community structures (r2 = 0.7109, p = 0.001). This result showed that soil pH was a crucial factor influencing microbial community structure, which was consistent with previous studies [43]. Previous studies found that near-neutral pH soil facilitated the mineralization of carbon and nitrogen [44], providing a substrate for the microbial process [45,46]. Meanwhile, this study also showed that SOC had a significant impact on both bacterial (r2 = 0.7487, p = 0.001) and fungal communities (r2 = 0.8020, p = 0.001) (Table S6). It was easy to understand that SOC was the core of the cycling and transformation of soil nutrient [47], and soil carbon decomposition was mediated by the microbial community [45]. To sum up, near-neutral pH and increased organic C availability were associated with increased microbial biomass [43,45].
Nitrogen (N) is one of the major elements essential for plant growth [6,48]. Soil N ammoniation and nitrification, as key processes in nitrogen cycling and plant nutrition absorption, are mainly mediated by soil microbes [4,5]. Currently, many studies found that microbial nitrogen fixation and mineralization were important ways of increasing the available nitrogen content in rhizosphere soil [10,35,48]. In the case of Bambusa vulgaris, supplementation of nitrogen fixing bacteria and vesicular-arbuscular mycorrhizae fungi could significantly increase growth [29]. Moreover, the soil NH4+-N content increased during the invasion of broadleaf forests by Moso bamboo, and the presence of the fungal lcc gene explained a significant portion of variations in net ammonification rate [35]. In this study, the prediction results of bacterial functions showed dominant roles of nitrogen fixation, cellulolysis and ureolysis in the rhizosphere soil of D. sinicus, indicating a high capacity for carbohydrate conversion and biological nitrogen fixation [11]. Remarkably, the rhizosphere microbes of the straight type possessed higher nitrogen fixing capacity, which could lead to higher soil NH4+-N content compared to the introduced straight type (Table 1, Table S3) [48]. Furthermore, the FUNGuild analysis revealed a high proportion of saprotrophic fungi, which enhanced the availability of carbon and nitrogen [49,50].

3.3. Influence of Micro-Ecological Factors on the Adaptation of D. sinicus

The rhizosphere micro-ecology of plants is influenced by the secretion of secondary metabolites, the taxa of rhizosphere microbes and the physicochemical properties of the soil. The disruption of micro-ecological balance can result in soil degradation, thereby influencing plant growth [51]. Previous studies indicated that plant adaptability was influenced by soil conditions and rhizosphere microbial taxa [52,53]. In this study, although the introduced straight type had the same origin region as the straight type, the introduced straight type exhibited significantly smaller DBH, BSW and BSR (p < 0.05) (Table 1). Analysis of soil properties revealed that the rhizosphere soil of the introduced straight type had significantly lower levels of SOC, AP, AK and NH4+-N compared to the straight type at each stage (p < 0.05). This result indirectly suggested that the introduced straight type had fewer available nutrients in the rhizosphere soil, which could lead to the decrease in DBH, BSW and BSR [54]. Meanwhile, apart from a significantly higher Shannon index of bacterial community observed in August for the introduced straight type compared to the straight type, no statistically significant differences were found in other indices between the two types (Figure 2). The prediction results of soil bacterial functions showed that nitrogen fixation abundance was significantly lower in the introduced straight type compared to the straight type at each stage (Figure 4A, Table S3), which may be an important factor leading to the low soil NH4+-N content of the introduced straight type [48]. It was important to note that the rhizosphere soil of the introduced straight type exhibited a significantly higher abundance of the ureolysis function compared to the straight type in August (p < 0.05) (Figure 4A, Table S3). This increase in the ureolysis function may be a response of micro-organisms to the NH4+-N demand for introduced straight type [55]. Additionally, the introduced straight type showed a significantly lower relative abundance of potentially pathogenic bacteria in May compared to the straight type (p < 0.05) (Figure 4D). These findings suggested that the introduction site had fewer pathogens and mutualistic bacteria (e.g., nitrogen fixation). The interaction among soil, plants and soil microbes was likely to influence the adaptation of the plant, as supported by previous research [19,20].
Similarly, the edaphic condition after introduction could affect the survival and growth of soil micro-organisms, force existing micro-organisms to adapt to the new environment and promote an increase in the abundance of specific micro-organisms [19]. The rhizosphere soil of both the straight and introduced straight type exhibited distinct fungal taxa according to the LEfSe analysis (Table S5). The biomarkers for the straight type included Leohumicola, Archaeorhizomyces, Pseudallescheria, while the introduced straight type showed biomarkers such as Cladophialophora, Entoloma, Agaricus, Clavaria and Chaetomium. These microbial taxa were known to play roles in decomposing organic matter and increasing nitrogen and phosphorus availability [56,57]. These results highlighted the role of micro-organisms in increasing soil nutrient availability, which was of great significance for the successful introduction and cultivation of D. sinicus [11,58].

3.4. Potential Key Microbes Associated with Rapid Growth of D. sinicus

Hundreds of woody bamboo species occur on the red soil and are characterized by their rapid growth [30]. Previous studies showed significant upregulation of genes associated with cell elongation or division, hormone signal transduction and cell wall development during the rapid growth period of woody bamboo [26,31,59]. However, there were few studies on the relationship between red soil micro-organisms and rapid growth of woody bamboos. Red soil was characterized by low nutrient availability [2], but D. sinicus growing on the red soil exhibited a substantial aboveground biomass [30]. It was therefore of interest to see how the barren red soil provided sufficient available nutrients for D. sinicus during its rapid growth period. This study revealed that the NH4+-N contents in the rhizosphere soil of all types were significantly higher in August than in May (p < 0.05) (Table 1), indicating substantial NH4+-N absorption by D. sinicus during the shooting and rapid growth period, which was consistent with other bamboo species [35]. The correlation analysis highlighted a positive association between soil NH4+-N content and bacterial genera Reyranella, Paenibacillus, Micromonospora, Nocardioides, Luedemannella, Pedomicrobium, Bradyrhizobium, as well as fungal genera Trichoderma, Mortierella, Trechispora, Apiotrichum, Exophiala, Acremonium, Cordana (p < 0.05). Among them, the taxa associated with N fixation, such as Bradyrhizobium, Paenibacillus and Trichoderma, may contribute to increased soil NH4+-N availability [12,14,60,61], which could facilitate the rapid growth of D. sinicus.

4. Materials and Methods

4.1. Soil Microbes Associated with Rapid Growth of D. sinicus

The study examined three types of D. sinicus: bending, straight and introduced straight type. The habitat conditions for these types are presented in Table 2. Monthly precipitation data for the three locations were obtained from the WorldClim website (https://www.worldclim.org/data/worldclim21.html, accessed on 27 February 2022) (Figure S2). The introduced straight type in Xinping County originated from the straight type in Ximeng County in 2010, and the seedlings were cultivated following the methods of asexual reproduction, i.e., stem cutting and divided clumps. A close-to-nature management approach was adopted for the cultivation of bamboo forest. The sample plot under investigation represented the largest surviving population subsequent to the introduction of the straight type.

4.2. Soil Sample Collection and Investigation of Bamboo Biological Characteristics

Soil sampling was conducted in May and August 2022, corresponding to the dormancy and shooting/rapid growth periods of the underground rhizome, respectively. Five quadrats (40 × 40 m) were established for each type of D. sinicus. Five healthy bamboo clumps were selected within each quadrat for the study, and the DBH of adult bamboos was measured. In August, the shooting rate was assessed by enumerating the number of adult bamboos and young shoots within each cluster. For each sampling event, five healthy bamboo clumps were excavated. After the loosely bound soil was shaken off, the tightly adhered soils were collected and used as rhizosphere soil. The collected fresh soils from each quadrat were sieved through a 2 mm mesh size and homogenized to create mixed samples. These mixed soil samples were divided into three parts. The first part was stored in sterilized centrifuge tubes in dry ice during transportation, then kept in an ultra-low-temperature refrigerator (−80 °C) at the laboratory for subsequent microbial diversity sequencing. The second part was stored in a portable refrigerator and stored at −20 °C for soil chemical property analysis after being transported to the laboratory. The third part of the soil sample (ca. 20 g) was promptly packed into aluminum boxes, weighed and transported back to the laboratory for moisture content determination [11].

4.3. The Measurement of Soil Properties

Soil pH was measured using a pH meter (FE20K, Mettler-Toledo, Switzerland) at a ratio of 2.5:1 (water:soil). SOC was quantified using an automatic analyzer (Shimadzu, Kyoto, Japan). Total phosphorus (TP) was determined via molybdenum-antimony colorimetry. AP was extracted using the hydrochloric acid–sulfuric acid method. Total potassium (TK) and AK were measured using the atomic absorption photometry method. SWC was determined by drying the samples at 105 °C until constant weight [62]. Total nitrogen (TN), NH4+-N and NO3−-N were measured using the SEAL AutoAnalyzer 3 (Seal Analytical, Hamburg, Germany).

4.4. DNA Extraction, Amplification and Sequencing

Total DNA was extracted from 0.5 g of homogenized fresh soil samples using the PowerSoil DNA Isolation Kit (Mo Bio Laboratories Inc., Carlsbad, CA, USA). The quality and concentration of the DNA were examined using a NanoDrop ND-2000 spectrophotometer (Thermo Scientific, Wilmington, DE, USA). The extracted DNA was stored at −20 °C prior to analysis. To identify the characteristics of soil bacterial communities, the V3-V4 variable region of the 16S rRNA gene was amplified. The following primers were used: 338F (5′-ACTCCTACGGGAGGCAGCAG-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′) [63]. The PCR reaction system had a volume of 20 μL, consisting of 4 μL of 5 × FastPfu buffer, 2 μL of 2.5 mM dNTPs, 0.8 μL of each primer (5 μM), 0.4 μL of FastPfu Polymerase, 0.2 μL of BSA and 10 ng of Template DNA, with the rest being ddH2O. Meanwhile, fungal communities were characterized by amplifying the internal transcribed spacer 1 (ITS1) region using the universal eukaryotic primers ITS1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) and ITS2R (5′-GCTGCGTTCTTCATCGATGC-3′) [62]. The PCR reaction system (20 μL) included 2 μL of 10 × Buffer, 2 μL of 2.5 mM dNTPs, 0.8 μL of each primer (5 μM), 0.2 μL of rTaq Polymerase, 0.2 μL of BSA and 10 ng of Template DNA. PCR amplification was performed using the GeneAmp PCR System 9700 (Applied Biosystems, Foster City, CA, USA) under the following thermal cycling conditions: 95 °C for 3 min, 35 cycles at 95 °C for 30 s, 55 °C for 30 s, 72 °C for 45 s and a final extension at 72 °C for 10 min. Sequencing was performed on an Illumina MiSeqPE300 Platform (Illumina, San Diego, CA, USA) by Majorbio Bio-pharm Technology Co., Ltd. (Shanghai, China). The raw sequencing data were deposited in the NCBI Sequence Reading Archive (SRA), with the BioProject number PRJNA980898 for bacterial diversity and PRJNA980913 for fungal diversity.

4.5. Data Analyses

The FLASH (v1.2.11) software was utilized for merging raw paired-end sequences [64], and the fastp software (v0.19.6) was utilized for quality control [65]. Operational taxonomic units (OTUs) were classified using the Uparse software (v7.0) with a 97% similarity criterion [66]. The taxonomic assignment of representative OTUs was performed by the RDP classifier [67] based on the Silva database (https://www.arb-silva.de/, accessed on 9 December 2022) and the Unite database (https://unite.ut.ee/, accessed on 9 December 2022). Soil microbial community α diversity was evaluated using the Sob, Shannon and Chao1 indices. To analyze the β diversity of the microbial community, principal coordinate analysis (PCoA) based on the abund-jaccard distance algorithm was conducted. Within-group and between-group similarity comparisons were assessed using the analysis of similarity (ANOSIM).
The composition of the microbial community was analyzed at the phylum and genus levels using taxonomic information. The LEfSe tool was used to determine the significant differences among samples [68], and the LDA was set to 4. The trophic modes of the fungal community were discerned based on FUNGuild [69]. The bacterial ecological functions were predicted using FAPROTAX [70], and bacterial phenotypes were predicted using the BugBase tool. The predicted results among groups were analyzed using the Kruskal–Wallis rank test. Soil properties with low multicollinearity, determined through the variance inflation factor (VIF) analysis, were retained. To explore the relationship between the microbial community and retained soil properties, the redundancy analysis (RDA) was conducted. The correlation between microbial taxa at the genus level and soil properties was assessed using the Spearman correlation coefficient. The calculation method for the bamboo stem weight (BSW) was as follows: BSW = 0.4531 × DBH1.7961 [30]. Statistical significance among samples was calculated using Duncan’s multiple comparison test. All statistical analyses were performed using R version 4.2.3.

5. Conclusions

Based on amplification sequencing and measurements of soil properties in different types of D. sinicus at the rapid growth and dormancy periods of rhizosphere soil, this study suggested that D. sinicus exhibited an absorption preference for NH4+-N, particularly during the shooting and following the rapid growth period. Moreover, compared with the native habitat of the straight type, the soil bacterial functions of the introduced straight type exhibited a significant decrease in nitrogen fixation, and the dominant microbial function was associated with ureolysis. Saprophytic fungi were the dominant fungal functional taxa in both straight and introduced straight type soils. This may reflect the fact that bacterial communities were more susceptible to soil conditions compared to fungal communities. This paper constitutes one of the initial research works exploring the effects of rhizosphere micro-organisms in woody bamboo on its adaptability and rapid growth. When introducing and cultivating woody bamboo, it is imperative to not only select superior seed sources but to also consider the influence of microbes on the bamboo forest in order to enhance adaptation and growth.

Supplementary Materials

The supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms241914665/s1.

Author Contributions

Conceptualization, H.Y., N.L. and L.C.; methodology and investigation, P.D., Q.C., C.B., N.L. and Z.Z.; data curation, P.D. and Q.C.; writing—original draft preparation, P.D.; writing—review and editing, H.Y., L.C. and P.D.; supervision and project administration, H.Y. and L.C.; funding acquisition, H.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Fundamental Research Funds of the Chinese Academy of Forestry, grant number CAFYBB2021SZ001; the National Natural Science Foundation of China, grant number 31870574; the Department of Sciences and Technology of Xizang Autonomous Region, grant number XZ201801-GA-11; and Yunnan Forestry Technological College, grant number KY(TD)202202.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data supporting the findings of this study are available on request from the corresponding author.

Acknowledgments

We would like to thank the editor and reviewers for their constructive comments on this manuscript, Wei Mao (Southwest Forestry University) for improving this paper, Lushuang Li for her assistance in analyzing data, the Forestry Bureau of Xinping County for their help in investigation of the introduced straight type in Xinping, Yunnan, China.

Conflicts of Interest

The authors declare no conflict of interest.

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Ijms 24 14665 g001
Figure 1. Morphological characteristics of bending type (A), straight type (B) and introduced straight type (C). Photographs by Peitong Dou.
Figure 1. Morphological characteristics of bending type (A), straight type (B) and introduced straight type (C). Photographs by Peitong Dou.
Ijms 24 14665 g001
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Figure 2. Rhizosphere microbial community α and β diversity in different soil samples. (A,B) Sobs of bacterial (A) and fungal (B) communities. (C,D) Shannon indexes of bacterial (C) and fungal (D) communities. (E,F) Chao1 indexes of bacterial (E) and fungal (F) communities. (G,H) Principal coordinate analysis (PCoA) of bacterial (G) and fungal (H) communities based on the abund-jaccard distance algorithm. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August. Different letters in the same line indicate significant differences (p < 0.05).
Figure 2. Rhizosphere microbial community α and β diversity in different soil samples. (A,B) Sobs of bacterial (A) and fungal (B) communities. (C,D) Shannon indexes of bacterial (C) and fungal (D) communities. (E,F) Chao1 indexes of bacterial (E) and fungal (F) communities. (G,H) Principal coordinate analysis (PCoA) of bacterial (G) and fungal (H) communities based on the abund-jaccard distance algorithm. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August. Different letters in the same line indicate significant differences (p < 0.05).
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Figure 3. Microbial community composition in rhizosphere soil samples. Abundances of main bacterial (A) and fungal (B) community phyla. Heatmaps showing the top 30 abundant bacterial (C) and fungal (D) genera. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
Figure 3. Microbial community composition in rhizosphere soil samples. Abundances of main bacterial (A) and fungal (B) community phyla. Heatmaps showing the top 30 abundant bacterial (C) and fungal (D) genera. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
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Figure 4. Functional prediction of bacteria (A) and fungi (B) in six rhizosphere soil samples. Significant difference test among groups in bacterial phenotypes (C). Kruskal−Wallis H−test for potentially pathogenic (D). W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August. * Significant differences at p < 0.05 level, ** Significant differences at p < 0.01 level, *** Significant differences at p < 0.001 level.
Figure 4. Functional prediction of bacteria (A) and fungi (B) in six rhizosphere soil samples. Significant difference test among groups in bacterial phenotypes (C). Kruskal−Wallis H−test for potentially pathogenic (D). W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August. * Significant differences at p < 0.05 level, ** Significant differences at p < 0.01 level, *** Significant differences at p < 0.001 level.
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Figure 5. LEfSe analysis of microbial abundance in six rhizosphere soil samples. Cladogram showing taxa with different abundance values of bacterial (A) and fungal (B) community. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
Figure 5. LEfSe analysis of microbial abundance in six rhizosphere soil samples. Cladogram showing taxa with different abundance values of bacterial (A) and fungal (B) community. W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
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Figure 6. Correlations of selected soil properties with bacterial (A) or fungal (B) α diversity indices. Redundancy analysis of soil properties and bacterial (C) or fungal (D) community in rhizosphere of D. sinicus. Color depth represented the magnitude of correlation R value. * 0.01  < p ≤ 0.05; ** 0.001 < p ≤ 0.01. SWC, soil water content; SOC, soil organic carbon; AP, available phosphorus; AK, available potassium; NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+:NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
Figure 6. Correlations of selected soil properties with bacterial (A) or fungal (B) α diversity indices. Redundancy analysis of soil properties and bacterial (C) or fungal (D) community in rhizosphere of D. sinicus. Color depth represented the magnitude of correlation R value. * 0.01  < p ≤ 0.05; ** 0.001 < p ≤ 0.01. SWC, soil water content; SOC, soil organic carbon; AP, available phosphorus; AK, available potassium; NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+:NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August.
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Figure 7. Heatmaps showing correlations between soil factors, biological characteristics and the first 30 genera of bacteria (A) and fungi (B). Color depth represented the magnitude of correlation R value. * 0.01  < p ≤ 0.05; ** 0.001 < p ≤ 0.01; *** p ≤ 0.001. SWC, soil water content; SOC, soil organic carbon; AP, available phosphorus; AK, available potassium; NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+: NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; DBH, diameter at breast height; BSW, bamboo stem weight.
Figure 7. Heatmaps showing correlations between soil factors, biological characteristics and the first 30 genera of bacteria (A) and fungi (B). Color depth represented the magnitude of correlation R value. * 0.01  < p ≤ 0.05; ** 0.001 < p ≤ 0.01; *** p ≤ 0.001. SWC, soil water content; SOC, soil organic carbon; AP, available phosphorus; AK, available potassium; NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+: NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; DBH, diameter at breast height; BSW, bamboo stem weight.
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Figure 8. The regression relation between selected soil properties and the biological characteristics of D. sinicus. Regression analysis between BSW and soil NO3−-N content (A), NH4+-N content (B), C: N (C), and NH4+: NO3− (D). Regression analysis between BSR and soil NO3−-N content (E), NH4+-N content (F), C: N (G), and NH4+: NO3− (H). NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+: NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; BSW, bamboo stem weight; BSR, bamboo shooting ratio.
Figure 8. The regression relation between selected soil properties and the biological characteristics of D. sinicus. Regression analysis between BSW and soil NO3−-N content (A), NH4+-N content (B), C: N (C), and NH4+: NO3− (D). Regression analysis between BSR and soil NO3−-N content (E), NH4+-N content (F), C: N (G), and NH4+: NO3− (H). NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+: NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; BSW, bamboo stem weight; BSR, bamboo shooting ratio.
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Table 1. Soil properties and biological characteristics of each D. sinicus type in different periods.
Table 1. Soil properties and biological characteristics of each D. sinicus type in different periods.
W1T1X1W2T2X2
pH6.13 ± 0.0231 a5.66 ± 0.0182 d5.74 ± 0.0130 c6.02 ± 0.0114 b5.58 ± 0.0180 e5.62 ± 0.0100 de
SOC (g·kg−1)24.88 ± 1.7468 c30.40 ± 1.4859 ab15.30 ± 1.3172 d26.64 ± 1.6675 bc32.06 ± 1.5740 a10.31 ± 0.7668 e
AP (mg·kg−1)4.38 ± 0.4409 d13.94 ± 1.0245 a9.12 ± 0.3652 b4.82 ± 0.5472 d8.68 ± 0.6967 b6.76 ± 0.4336 c
TP (g·kg−1)1.29 ± 0.1118 a1.28 ± 0.2034 a0.44 ± 0.0089 b1.28 ± 0.1660 a1.19 ± 0.1282 a0.59 ± 0.0551 b
AK (mg·kg−1)297.0 ± 6.9498 a167.6 ± 7.8333 c58.8 ± 3.2465 d225.2 ± 16.7404 b289.2 ± 26.0776 a78.0 ± 7.2732 d
TK (g·kg−1)5.60 ± 0.2074 c11.78 ± 0.2177 a7.34 ± 0.1568 b5.30 ± 0.3795 c11.22 ± 0.2311 a7.00 ± 0.3521 b
TN (g·kg−1)1.85 ± 0.2517 b1.99 ± 0.1316 ab1.04 ± 0.0592 c2.34 ± 0.3391 ab2.49 ± 0.1058 a0.92 ± 0.0496 c
NO3−-N (mg·kg−1)11.69 ± 0.7936 a1.67 ± 0.1309 cd1.88 ± 0.1541 c9.04 ± 0.3649 b0.72 ± 0.0611 d2.16 ± 0.1548 c
NH4+-N (mg·kg−1)22.32 ± 1.7144 bc19.85 ± 1.1401 cd5.89 ± 0.8136 e29.83 ± 3.5011 a28.10 ± 4.1165 ab14.46 ± 0.4222 d
SWC (%)25.79 ± 0.9174 b26.29 ± 1.7114 b15.55 ± 0.5985 c30.30 ± 2.0609 ab33.17 ± 2.5209 a20.01 ± 0.6092 c
C: N14.19 ± 1.4521 ab15.34 ± 0.5688 a14.90 ± 1.4384 ab12.33 ± 1.6959 ab12.88 ± 0.2239 ab11.39 ± 1.1213 b
NH4+: NO3−1.94 ± 0.1736 c12.22 ± 1.3341 b3.24 ± 0.5697 c3.37 ± 0.4578 c39.52 ± 5.5597 a6.85 ± 0.5630 bc
DBH (cm)17.90 ± 0.6058 b20.79 ± 0.7266 a7.99 ± 0.3923 c17.34 ± 1.1352 b21.61 ± 0.5640 a8.18 ± 0.8046 c
BSW (kg)80.90 ± 4.9101 b105.81 ± 6.5896 a19.06 ± 1.6011 c77.09 ± 8.9063 b113.33 ± 5.1874 a20.30 ± 3.5416 c
BSR (%)---71.05 ± 2.9599 a77.98 ± 3.2459 a44.07 ± 1.3003 b
Values are means ± SE; Different letters in the same line indicate significant differences (p < 0.05); W1, rhizosphere soil sample of bending type in May; W2, rhizosphere soil sample of bending type in August; T1, rhizosphere soil sample of straight type in May; T2, rhizosphere soil sample of straight type in August; X1, rhizosphere soil sample of introduced straight type in May; X2, rhizosphere soil sample of introduced straight type in August. SOC, soil organic carbon; AP, available phosphorus; TP, soil total phosphorus; AK, available potassium; TK, soil total potassium; TN, soil total nitrogen; NO3−-N, nitrate nitrogen; NH4+-N, ammonia nitrogen; SWC, soil water content; C: N, the ratio between soil organic carbon and soil total nitrogen; NH4+: NO3−, the ratio between ammonia nitrogen and nitrate nitrogen; DBH, diameter at breast height. BSW, bamboo stem weight; BSR, bamboo shooting ratio.
Table 2. The habitat conditions of different types of D. sinicus.
Table 2. The habitat conditions of different types of D. sinicus.
The Type of D. sinicusStudy SiteAltitude/mClimate TypeAnnual Average Temperature/°CAnnual Precipitation/mmFrost-Free Period/DaySoil Type
Bending typeMenglian County, YN (22.20 N, 99.33 E)1040south subtropical climate19.71363.6300lateritic red soil
Straight typeXimeng County, YN (22.63 N, 99.62 E)1122subtropical mountain humid monsoon climate19.11629.2362lateritic red soil
Introduced straight typeYuxi County, YN (24.12 N, 102.63 E)878subtropical semi-humid plateau monsoon climate19.0950.0315red soil
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MDPI and ACS Style

Dou, P.; Cheng, Q.; Liang, N.; Bao, C.; Zhang, Z.; Chen, L.; Yang, H. Rhizosphere Microbe Affects Soil Available Nitrogen and Its Implication for the Ecological Adaptability and Rapid Growth of Dendrocalamus sinicus, the Strongest Bamboo in the World. Int. J. Mol. Sci. 2023, 24, 14665. https://doi.org/10.3390/ijms241914665

AMA Style

Dou P, Cheng Q, Liang N, Bao C, Zhang Z, Chen L, Yang H. Rhizosphere Microbe Affects Soil Available Nitrogen and Its Implication for the Ecological Adaptability and Rapid Growth of Dendrocalamus sinicus, the Strongest Bamboo in the World. International Journal of Molecular Sciences. 2023; 24(19):14665. https://doi.org/10.3390/ijms241914665

Chicago/Turabian Style

Dou, Peitong, Qian Cheng, Ning Liang, Changyan Bao, Zhiming Zhang, Lingna Chen, and Hanqi Yang. 2023. "Rhizosphere Microbe Affects Soil Available Nitrogen and Its Implication for the Ecological Adaptability and Rapid Growth of Dendrocalamus sinicus, the Strongest Bamboo in the World" International Journal of Molecular Sciences 24, no. 19: 14665. https://doi.org/10.3390/ijms241914665

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