Response mechanisms of rhizosphere bacterial community diversity and functional group composition of dominant plants in typical grasslands to long-term grazing

doi:10.17521/cjpe.2024.0428

Abstract

Abstract:

Aims Long-term grazing profoundly affects the external environment for plant growth and development in grassland ecosystems, and plants adapt to environmental changes through interactions with rhizosphere microbes. However, there is limited research on how grazing affects the rhizosphere microbial diversity of plants with different survival strategies in grasslands.
Methods In this study, based on a long-term grazing experiment on typical grasslands in Nei Mongol, we selected the dominant plant species Stipa grandis and Cleistogenes squarrosa as research subjects. Using high-throughput sequencing technology, we investigated the changes in rhizosphere bacterial diversity under different grazing intensities (control, light: 1.5 sheep·hm^-2, moderate: 4.5 sheep·hm^-2, and heavy: 7.5 sheep·hm^-2), and analyzed the differences in the responses of two dominant plant rhizospheric bacteria and their intrinsic connection with plant functional traits.
Important findings The results showed that: (1) Heavy grazing significantly reduced the rhizosphere bacterial richness (8.97%) and Chao1 index (9.48%) for Stipa grandis, but had no significant effect on the rhizosphere bacterial α-diversity of Cleistogenes squarrosa. Additionally, the α-diversity of Stipa grandis was significantly lower than that of Cleistogenes squarrosa. Moreover, heavy grazing significantly altered the bacterial community composition of both plant species, with the change being more pronounced in Stipa grandis than in Cleistogenes squarrosa. (2) As grazing intensity increased, Stipa grandiswas enriched with both plant growth promoting rhizobacteria and biocontrol agents, whereas Cleistogenes squarrosa was primarily enriched with plant growth promoting rhizobacteria. (3) Changes in the diversity and relative abundance of rhizosphere bacterial communities in Stipa grandiswere significantly correlated with its larger root diameter, lower specific leaf area, and lower specific root length, which reflect grazing avoidance and resource-conserving strategies. In contrast, changes in the bacterial communities of Cleistogenes squarrosa were significantly correlated with its higher carbon to nitrogen ratio in aboveground biomass and larger specific leaf area, which reflect grazing tolerance and resource-consuming strategies. In conclusion, this study demonstrated that the responses of rhizosphere bacterial communities of different dominant plant species to grazing pressure are closely related to their survival strategies, enriching our understanding of the synergistic adaptations between plants and rhizosphere microbial communities in the context of long-term grazing.

Key words: grazing intensity, dominant plants, rhizosphere bacteria, plant functional traits, microbial functional groups

CUI Dong-Qing, TIAN Chen, SONG Hui-Min, LU Xiao-Ming, SA Qi-Ri, XU Guo-Qing, YANG Pei-Zhi, BAI Yong-Fei, TIAN Jian-Qing. Response mechanisms of rhizosphere bacterial community diversity and functional group composition of dominant plants in typical grasslands to long-term grazing[J]. Chin J Plant Ecol, 2025, 49(7): 1163-1176.

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Figures/Tables 7

Fig. 1 Difference of plant functional traits of Stipa grandis and Cleistogenes squarrosa, and the effect of different grazing intensity on functional traits of the two species (mean ± SE). ACNR, aboveground biomass carbon to nitrogen ratio; AGB, aboveground biomass; AGBP, aboveground biomass phosphorus content; ARD, average root diameter; BGB, belowground biomass; RCNR, root carbon to nitrogen ratio; RP, root phosphorus content; RTD, root tissue density; RTSR, root-to-shoot ratio; SLA, specific leaf area; SRL, specific root length. CK, L, M and H represent the control, light grazing, moderate grazing and heavy grazing intensity, respectively. Different upper- and lower-case letters indicate significant differences (p < 0.05) in the effects of grazing intensities on plant functional traits of Stipa grandis and Cleistogenes squarrosa.

Fig 2 Alpha diversity index of rhizosphere bacteria of Stipa grandis and Cleistogenes squarrosa under different grazing intensities. *, p < 0.05; **, p < 0.01; ns, p ≥ 0.05. CK, L, M and H represent the control, light grazing, moderate grazing and heavy grazing intensity, respectively. Different upper- and lower-case letters indicate significant differences (p < 0.05) in the effects of rhizosphere bacterial alpha diversity of Stipa grandis and Cleistogenes squarrosa.

Table 1 Differences in rhizobacterial community composition of Stipa grandis and Cleistogenes squarrosa between grazing and control treatments

物种名称 Species	CK vs. L	CK vs. M	CK vs. H
大针茅 Stipa grandis	0.194 6^**	0.224 9^**	0.238 7^**
糙隐子草 Cleistogenes squarrosa	0.146 0^**	0.156 5^**	0.163 2^**

Table 2 Effects of plant functional traits on rhizosphere soil bacterial richness and community composition of Stipa grandis and Cleistogenes squarrosa

大针茅 Stipa grandis			糙隐子草 Cleistogenes squarrosa
植物性状 Plant traits	r	Variance (%)	植物性状 Plant trait	r	Variance (%)
AGB	0.093	43.89^***	AGB	0.063	29.02^*
SLA	0.039	26.37	SLA	0.154	28.45^*
ACNR	0.028	27.72	ACNR	0.162^*	38.07^***
SRL	-0.112	36.17^**	SRL	0.062	25.32
ARD	0.154^*	30.71^**	RTD	0.036	27.95
RTD	-0.015	27.56^*	RCNR	0.061	28.06

Table 3 Functional group classification of rhizosphere-enriched bacterial genera in Stipa grandis and Cleistogenes squarrosa

	属名 Genus	参考文献 Reference
根际促生菌Plant growth- promoting rhizobacteria (PGPR)	浅野氏菌属、硝化螺旋菌属、类诺卡氏菌属、RB41菌属(未正式命名)、红色杆菌属、土壤红色杆菌属、鞘氨醇单胞菌属、苔藓杆菌属、芽单胞菌属、克罗斯氏菌属、根瘤杆菌属、候选乌达杆菌属 Asanoa, Nitrospira, Nocardioides, RB41, Rubrobacter, Solirubrobacter, Sphingomonas, Bryobacter, Gemmatimonas, Crossiella, Rhizobacter, Candidatus Udaeobacter	Chen et al., 2004; Foesel et al., 2013; Hu et al., 2020; Willms et al, 2020; Xun et al., 2021; Jia et al., 2022; Yu et al., 2022; Zhou et al., 2022; Ortiz-López et al., 2023; Wei et al., 2023; Xu et al., 2024
生物防治菌Biocontrol agents (BCAs)	游动放线菌属、芽孢杆菌属、盖氏菌属、莱氏菌属、小单孢菌属、连接杆菌属 Bacillus, Gaiella, Lechevalieria, Micromonospora, Conexibacter, Actinoplanes	Cui et al., 2019; Deng et al., 2021; Yu et al., 2021; Revillini et al., 2023; Xia et al., 2024

Fig. 3 Heatmaps of rhizobacterial genera with increased relative abundance (A, B) and linear regression of functional group relative abundance (C, D) for Stipa grandis and Cleistogenes squarrosa under different grazing intensities. Different lowercase letters indicate significant differences (p < 0.05) in the relative abundance of genera influenced by varying grazing intensities in A and B. CK, L, M, and H represent control, light grazing, moderate grazing, and heavy grazing, respectively. RA denotes the average relative abundance of the genus under the four grazing intensities. Error bars in C and D represent mean ± SE. *, p < 0.05; ***, p < 0.001; ns, p ≥ 0.05.

Fig. 4 Redundancy analysis (RDA) results and correlation heatmaps of rhizosphere enriched bacterial genera with plant functional traits of Stipa grandis (A, C) and Cleistogenes squarrosa (B, D) under different grazing intensities. *, p < 0.05; **, p < 0.01; ***, p < 0.001。AGB, aboveground biomass; SLA, specific leaf area; ACNR, aboveground biomass carbon to nitrogen ratio; SRL, specific root length; ARD, average root diameter; RTD, root tissue density; RCNR, root carbon to nitrogen ratio.

References 88

[1]	Ahkami AH, White III RA, Handakumbura PP, Jansson C (2017). Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere, 3, 233-243.
[2]	An JY, Li XL, Ding Y, Li F, Guo FH, Ma HL, Gao SB, Li YH (2021). Effects of different grazing intensities on functional traits of Cleistogenes squarrosa. Chinese Journal of Grassland, 43(1), 50-57.
	[安景源, 李西良, 丁勇, 李芳, 郭丰辉, 马晖玲, 高韶勃, 李元恒 (2021). 不同放牧强度对糙隐子草功能性状的影响. 中国草地学报, 43(1), 50-57.]
[3]	Anderson MJ (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
[4]	Bai B, Liu WD, Qiu XY, Zhang J, Zhang JY, Bai Y (2022). The root microbiome: community assembly and its contributions to plant fitness. Journal of Integrative Plant Biology, 64, 230-243. DOI
[5]	Bai YF, Cotrufo MF (2022). Grassland soil carbon sequestration: current understanding, challenges, and solutions. Science, 377, 603-608. DOI PMID
[6]	Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010). Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from Inner Mongolia grasslands. Global Change Biology, 16, 358-372.
[7]	Bardgett RD, Mommer L, de Vries FT (2014). Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692-699.
[8]	Berendsen RL, Pieterse CM, Bakker PA (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478-486. DOI PMID
[9]	Blee K, Hein J, Wolfe GV (2013). Molecular Microbial Ecology of the Rhizosphere. Wiley-Blackwell, Hoboken, USA.
[10]	Bradford MA, Wieder WR, Bonan GB, Fierer N, Raymond PA, Crowther TW (2016). Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change, 6, 751-758.
[11]	Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, Knights D, Gajer P, Ravel J, Fierer N, Gordon JI, Knight R (2011). Moving pictures of the human microbiome. Genome Biology, 12, R50. DOI: 10.1186/gb-2011-12-5-r50.
[12]	Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wirén N (2011). Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition and Soil Science, 174, 3-11.
[13]	Chai JL, Xu CL, Zhang DG, Xiao H, Pan TT, Yu XJ (2019). Effects of simulated trampling and rainfall on soil nutrients and enzyme activity in an alpine meadow. Acta Ecologica Sinica, 39, 333-344.
	[柴锦隆, 徐长林, 张德罡, 肖红, 潘涛涛, 鱼小军 (2019). 模拟践踏和降水对高寒草甸土壤养分和酶活性的影响. 生态学报, 39, 333-344.]
[14]	Chen LL, Wang KX, Baoyin TGT (2021). Effects of grazing and mowing on vertical distribution of soil nutrients and their stoichiometry (C:N:P) in a semi-arid grassland of North China. Catena, 206, 105507. DOI: 10.1016/j.catena.2021.105507.
[15]	Chen MY, Wu SH, Lin GH, Lu CP, Lin YT, Chang WC, Tsay SS (2004). Rubrobacter taiwanensis sp. nov., a novel thermophilic, radiation-resistant species isolated from hot springs. International Journal of Systematic and Evolutionary Microbiology, 54, 1849-1855.
[16]	Cheng JH, Chu PF, Chen DM, Bai YF (2015). Functional correlations between specific leaf area and specific root length along a regional environmental gradient in Inner Mongolia grasslands. Functional Ecology, 30, 985-997.
[17]	Cole DN (1995). Experimental trampling of vegetation. II. Predictors of resistance and resilience. Journal of Applied Ecology, 32, 215-224.
[18]	Cui L, Guo F, Zhang JL, Yang S, Wang JG, Meng JJ, Geng Y, Li XG, Wan SB (2019). Improvement of continuous microbial environment in peanut rhizosphere soil by Funneliformis mosseae. Chinese Journal of Plant Ecology, 43, 718-728.
	[崔利, 郭峰, 张佳蕾, 杨莎, 王建国, 孟静静, 耿耘, 李新国, 万书波 (2019). 摩西斗管囊霉改善连作花生根际土壤的微环境. 植物生态学报, 43, 718-728.] DOI
[19]	Delgado-Baquerizo M, Guerra CA, Cano-Díaz C, Egidi E, Wang JT, Eisenhauer N, Singh BK, Maestre FT (2020). The proportion of soil-borne pathogens increases with warming at the global scale. Nature Climate Change, 10, 550-554.
[20]	Deng Y, Yu LY, Zhang YQ (2021). Research progress on the family Micromonosporaceae. Biotic Resources, 43, 583-596.
	[邓阳, 余利岩, 张玉琴 (2021). 小单孢菌科放线菌的研究进展. 生物资源, 43, 583-596.]
[21]	Deng ZY, Wang YC, Xiao CC, Zhang DX, Feng G, Long WX (2022). Effects of plant fine root functional traits and soil nutrients on the diversity of rhizosphere microbial communities in tropical cloud forests in a dry season. Forests, 13, 421. DOI: 10.3390/f13030421.
[22]	Dhungana I, Kantar MB, Nguyen NH (2023). Root exudate composition from different plant species influences the growth of rhizosphere bacteria. Rhizosphere, 25, 100645. DOI: 10.1016/j.rhisph.2022.100645.
[23]	Díaz S, Noy-Meir I, Cabido M (2001). Can grazing response of herbaceous plants be predicted from simple vegetative traits? Journal of Applied Ecology, 38, 497-508.
[24]	Dwivedi D, Riley WJ, Torn MS, Spycher N, Maggi F, Tang JY (2017). Mineral properties, microbes, transport, and plant-input profiles control vertical distribution and age of soil carbon stocks. Soil Biology & Biochemistry, 107, 244-259.
[25]	Foesel BU, Rohde M, Overmann J (2013). Blastocatella fastidiosa gen. nov., sp. nov., isolated from semiarid savanna soil—The first described species of Acidobacteria subdivision 4. Systematic and Applied Microbiology, 36, 82-89.
[26]	Garbeva P, van Elsas JD, van Veen JA (2008). Rhizosphere microbial community and its response to plant species and soil history. Plant and Soil, 302, 19-32.
[27]	He PC, Ye Q (2019). Plant functional traits: from individual plant to global scale. Journal of Tropical and Subtropical Botany, 27, 523-533.
	[贺鹏程, 叶清 (2019). 基于植物功能性状的生态学研究进展: 从个体水平到全球尺度. 热带亚热带植物学报, 27, 523-533.]
[28]	Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016). Root endophyte colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell, 165, 464-474. DOI PMID
[29]	Hu HT, Zhu ZG, Yang JZ, Cao AC, Yan DD (2020). Effect of treatments on bacterial wilt of ginger at high mountain area and soil bacterial community. Microbiology China, 47, 1763-1775.
	[胡洪涛, 朱志刚, 杨靖钟, 曹坳程, 颜冬冬 (2020). 不同处理对高山凤头姜姜瘟病的防效及土壤细菌群落结构和功能的影响. 微生物学通报, 47, 1763-1775.]
[30]	Hu JP, Zhang MX, Lü ZL, He YY, Yang XX, Khan A, Xiong YC, Fang XL, Dong QM, Zhang JL (2023). Grazing practices affect phyllosphere and rhizosphere bacterial communities of Kobresia humilis by altering their network stability. Science of the Total Environment, 900, 165814. DOI: 10.1016/j.scitotenv.2023.165814.
[31]	Huang XF, Chaparro JM, Reardon KF, Zhang RF, Shen QR, Vivanco JM (2014). Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany, 92, 267-275.
[32]	Hufkens K, Keenan TF, Flanagan LB, Scott RL, Bernacchi CJ, Joo E, Brunsell NA, Verfaillie J, Richardson AD (2016). Productivity of North American grasslands is increased under future climate scenarios despite rising aridity. Nature Climate Change, 6, 710-714. DOI
[33]	Jia LJ, Wang Z, Ji L, de Neve S, Struik PC, Yao YQ, Lv JJ, Zhou T, Jin K (2022). Keystone microbiome in the rhizosphere soil reveals the effect of long-term conservation tillage on crop growth in the Chinese Loess Plateau. Plant and Soil, 473, 457-472.
[34]	Jiao S, Xu YQ, Zhang J, Hao X, Lu YH (2019). Core microbiota in agricultural soils and their potential associations with nutrient cycling. mSystems, 4, e00313-18. DOI: 10.1128/mSystems.00313-18.
[35]	Jiménez S, Ollat N, Deborde C, Maucourt M, Rellán-Álvarez R, Moreno MÁ, Gogorcena Y (2011). Metabolic response in roots of Prunus rootstocks submitted to iron chlorosis. Journal of Plant Physiology, 168, 415-423. DOI PMID
[36]	Jing JY, Bezemer TM, van der Putten WH (2015). Complementarity and selection effects in early and mid-successional plant communities are differentially affected by plant-soil feedback. Journal of Ecology, 103, 641-647.
[37]	Kaštovská E, Edwards K, Picek T, Šantrůčková H (2015). A larger investment into exudation by competitive versus conservative plants is connected to more coupled plant-microbe N cycling. Biogeochemistry, 122, 47-59.
[38]	Kaźmierczak M, Błońska E, Kempf M, Zarek M, Lasota J (2024). Rhizosphere effect: microbial and enzymatic dynamics in the rhizosphere of various shrub species. Plant and Soil, 511, 245-262.
[39]	Lan ZC, Bai YF (2012). Testing mechanisms of N-enrichment-induced species loss in a semiarid Inner Mongolia grassland: critical thresholds and implications for long-term ecosystem responses. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 3125-3134.
[40]	Li Q, Zhao CZ, Zhao LC, Wang JW, Wen J (2019). The correlation analysis between specific leaf area and photosynthetic efficiency of Phragmites australis in salt marshes of Qinwangchuan. Acta Ecologica Sinica, 39, 7124-7133.
	[李群, 赵成章, 赵连春, 王继伟, 文军 (2019). 秦王川盐沼湿地芦苇叶片比叶面积与光合效率的关联分析. 生态学报, 39, 7124-7133.]
[41]	Li WH, Zheng SX, Bai YF (2014). Effects of grazing intensity and topography on species abundance distribution in a typical steppe of Inner Mongolia. Chinese Journal of Plant Ecology, 38, 178-187.
	[李文怀, 郑淑霞, 白永飞 (2014). 放牧强度和地形对内蒙古典型草原物种多度分布的影响. 植物生态学报, 38, 178-187.] DOI
[42]	Lin QH, Tian D, Gao F, Ge XF, Ding YH, Ma SH, Hong JM, Ren D (2022). Effects of returning farmland to forest and grassland on soil bacteria: a case study in Bashang area, China. Soils, 54, 307-313.
	[林权虹, 田地, 高菲, 葛星霏, 丁月泓, 马素辉, 洪剑明, 任东 (2022). 坝上地区退耕还林还草措施对土壤细菌的影响. 土壤, 54, 307-313.]
[43]	Ling N, Wang TT, Kuzyakov Y (2022). Rhizosphere bacteriome structure and functions. Nature Communications, 13, 836. DOI: 10.1038/s41467-022-28448-9.
[44]	Lucke M, Correa MG, Levy A (2020). The role of secretion systems, effectors, and secondary metabolites of beneficial rhizobacteria in interactions with plants and microbes. Frontiers in Plant Science, 11, 589416. DOI: 10.3389/fpls.2020.589416.
[45]	Lv B, Ding L, Guo C, Chen F, Zhou HP, Wang XS, Dong XL, Xiang FY (2024). Effects of compound microbial fertilizer on soil nutrients and rhizosphere bacterial community in cotton field. Crops, 40(4), 209-215.
	[吕博, 丁亮, 过聪, 陈锋, 周海平, 汪雪松, 董小林, 向发云 (2024). 复合微生物肥对棉田土壤养分及根际细菌群落的影响. 作物杂志, 40(4), 209-215.]
[46]	Ma XD (2023). Assembly, Turnover and Function of Rhizosphere Microbial Communities of Seven Zonal Stipa species in Inner Mongolia Steppe. PhD dissertation, Inner Mongolia University, Hohhot. 54-67.
	[马晓丹 (2023). 内蒙古草原7种地带性针茅根际微生物群落的构建、更替及功能探究. 博士学位论文, 内蒙古大学, 呼和浩特. 54-67.]
[47]	Maitra P, Hrynkiewicz K, Szuba A, Jagodziński AM, Al-Rashid J, Mandal D, Mucha J (2024). Metabolic niches in the rhizosphere microbiome: dependence on soil horizons, root traits and climate variables in forest ecosystems. Frontiers in Plant Science, 15, 1344205. DOI: 10.3389/fpls.2024.1344205.
[48]	Meier IC, Tuckmantel T, Heitkotter J, Muller K, Preusser S, Wrobel TJ, Kandeler E, Marschner B, Leuschner C (2020). Root exudation of mature beech forests across a nutrient availability gradient: the role of root morphology and fungal activity. New Phytologist, 226, 583-594. DOI PMID
[49]	Molefe RR, Amoo AE, Babalola OO (2023). Communication between plant roots and the soil microbiome; involvement in plant growth and development. Symbiosis, 90, 231-239.
[50]	Moreau D, Pivato B, Bru D, Busset H, Deau F, Faivre C, Matejicek A, Strbik F, Philippot L, Mougel C (2015). Plant traits related to nitrogen uptake influence plant-microbe competition. Ecology, 96, 2300-2310. PMID
[51]	Muscarella SM, Alduina R, Badalucco L, Capri FC, Di Leto Y, Gallo G, Laudicina VA, Paliaga S, Mannina G (2024). Water reuse of treated domestic wastewater in agriculture: Effects on tomato plants, soil nutrient availability and microbial community structure. Science of the Total Environment, 928, 172259. DOI: 10.1016/j.scitotenv.2024.172259.
[52]	Nabais C, Labuto G, Gonçalves S, Buscardo E, Semensatto D, Nogueira ARA, Freitas H (2011). Effect of root age on the allocation of metals, amino acids and sugars in different cell fractions of the perennial grass Paspalum notatum (bahiagrass). Plant Physiology and Biochemistry, 49, 1442-1447.
[53]	Nan J, Chao LM, Ma XD, Xu DL, Mo L, Zhang XD, Zhao XP, Bao YY (2020). Microbial diversity in the rhizosphere soils of three Stipa species from the eastern Inner Mongolian grasslands. Global Ecology and Conservation, 22, e00992. DOI: 10.1016/j.gecco.2020.e00992.
[54]	Ortiz-López FJ, Oves-Costales D, Carretero-Molina D, Martín J, Díaz C, de la Cruz M, Román-Hurtado F, Álvarez-Arévalo M, Jørgensen TS, Reyes F, Weber T, Genilloud O (2023). Crossiellidines A-F, unprecedented pyrazine-alkylguanidine metabolites with broad-spectrum antibacterial activity from Crossiella sp. Organic Letters, 25, 3502-3507. DOI PMID
[55]	Rathore N, Hanzelková V, Dostálek T, Semerád J, Schnablová R, Cajthaml T, Münzbergová Z (2023). Species phylogeny, ecology, and root traits as predictors of root exudate composition. New Phytologist, 239, 1212-1224. DOI PMID
[56]	Revillini D, David AS, Reyes AL, Knecht LD, Vigo C, Allen P, Searcy CA, Afkhami ME (2023). Allelopathy-selected microbiomes mitigate chemical inhibition of plant performance. New Phytologist, 240, 2007-2019.
[57]	Saeed Q, Wang XK, Haider FU, Kučerik J, Mumtaz MZ, Holatko J, Naseem M, Kintl A, Ejaz M, Naveed M, Brtnicky M, Mustafa A (2021). Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. International Journal of Molecular Sciences, 22, 10529. DOI: 10.3390/ijms221910529.
[58]	Sivaram AK, Subashchandrabose SR, Logeshwaran P, Lockington R, Naidu R, Megharaj M (2020). Rhizodegradation of PAHs differentially altered by C₃ and C₄ plants. Scientific Reports, 10, 16109. DOI: 10.1038/s41598-020-72844-4.
[59]	Sparks DL, Page AL, Loeppert PA, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (1996). Methods of Soil Analysis Part 3: Chemical Methods. Soil Science Society of America and American Society of Agronomy, Madison.
[60]	Sweeney CJ, de Vries FT, van Dongen BE, Bardgett RD (2021). Root traits explain rhizosphere fungal community composition among temperate grassland plant species. New Phytologist, 229, 1492-1507.
[61]	Wan HW, Bai YF, Schönbach P, Gierus M, Taube F (2011). Effects of grazing management system on plant community structure and functioning in a semiarid steppe: scaling from species to community. Plant and Soil, 340, 215-226.
[62]	Wang CN, Li X, Lu XM, Wang Y, Bai YF (2023). Intraspecific trait variation governs grazing-induced shifts in plant community above- and below-ground functional trait composition. Agriculture, Ecosystems & Environment, 346, 108357. DOI: 10.1016/j.agee.2023.108357.
[63]	Wang SW, Li WH, Li YL, Yan H, Li YH (2022). Effects of different livestock types on plant diversity and community structure of a typical steppe in Nei Mongol, China. Chinese Journal of Plant Ecology, 46, 941-950.
	[王姝文, 李文怀, 李艳龙, 严慧, 李永宏 (2022). 放牧家畜类型对内蒙古典型草原植物多样性和群落结构的影响. 植物生态学报, 46, 941-950.] DOI
[64]	Wang Z (2021). Effects of Different Grazing Types on Functional Traits of Dominant Species in Typical Steppe of Inner Mongolia. Master degree dissertation, Inner Mongolia University, Hohhot.
	[王铮 (2021). 不同放牧方式对内蒙古典型草原优势种植物功能性状的影响. 硕士学位论文, 内蒙古大学, 呼和浩特.]
[65]	Wei CF, Liu ST, Li Q, He J, Sun ZJ, Pan XY (2023). Diversity analysis of vineyards soil bacterial community in different planting years at eastern foot of Helan Mountain, Ningxia. Rhizosphere, 25, 100650. DOI: 10.1016/j.rhisph.2022.100650.
[66]	Wen T, Zhao ML, Yuan J, Kowalchuk GA, Shen QR (2021). Root exudates mediate plant defense against foliar pathogens by recruiting beneficial microbes. Soil Ecology Letters, 3, 42-51. DOI
[67]	Willms IM, Rudolph AY, Göschel I, Bolz SH, Schneider D, Penone C, Poehlein A, Schöning I, Nacke H (2020). Globally abundant “Candidatus Udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging. mSphere, 5, e00186-20. DOI: 10.1128/mSphere.00186-20.
[68]	Wu LK, Lin XM, Lin WX (2014). Advances and perspective in research on plant-soil-microbe interactions mediated by root exudates. Chinese Journal of Plant Ecology, 38, 298-310. DOI
	[吴林坤, 林向民, 林文雄 (2014). 根系分泌物介导下植物-土壤-微生物互作关系研究进展与展望. 植物生态学报, 38, 298-310.] DOI
[69]	Wu SY, Baoyin T, Xu HB, Zhang L (2021). Effects of grazing intensities on functional traits of Cleistogenes squarrosa in a typical grassland of Inner Mongolia, China. Chinese Journal of Applied Ecology, 32, 392-398.
	[吴思雨, 宝音陶格涛, 许宏斌, 张璐 (2021). 放牧强度对内蒙古典型草原糙隐子草功能性状的影响. 应用生态学报, 32, 392-398.] DOI
[70]	Xia XY, Wei QH, Wu HX, Chen XY, Xiao CX, Ye YP, Liu CT, Yu HY, Guo YW, Sun WX, Liu WD (2024). Bacillus species are core microbiota of resistant maize cultivars that induce host metabolic defense against corn stalk rot. Microbiome, 12, 156. DOI: 10.1186/s40168-024-01887-w.
[71]	Xiao T, Li P, Fei WB, Wang JD (2024). Effects of vegetation roots on the structure and hydraulic properties of soils: a perspective review. Science of the Total Environment, 906, 167524. DOI: 10.1016/j.scitotenv.2023.167524.
[72]	Xu K, Lu JH, Li X, Zhang JD, Luo JF, Zheng XR (2024). Composition and functions of soil bacterial communities of wild Glycyrrhiza uralensis Fisch. in habitats with different degrees of salinization. Acta Microbiologica Sinica, 64, 1550-1566.
	[徐可, 陆嘉惠, 李新, 张迦得, 罗加粉, 郑雪荣 (2024). 不同盐渍化生境野生乌拉尔甘草土壤细菌群落结构及功能预测分析. 微生物学报, 64, 1550-1566.]
[73]	Xun WB, Liu YP, Li W, Ren Y, Xiong W, Xu ZH, Zhang N, Miao YZ, Shen QR, Zhang RF (2021). Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome, 9, 35. DOI: 10.1186/s40168-020-00985-9.
[74]	Yang CB, Zhang XP, Ni HJ, Gai X, Huang ZC, Du XH, Zhong ZK (2021). Soil carbon and associated bacterial community shifts driven by fine root traits along a chronosequence of Moso bamboo (Phyllostachys edulis) plantations in subtropical China. Science of the Total Environment, 752, 142333. DOI: 10.1016/j.scitotenv.2020.142333.
[75]	Yang Y, Zhang H, Liu W, Sun JM, Zhao ML, Han GD, Pan QM (2023). Effects of grazing intensity on diversity and composition of rhizosphere and non-rhizosphere microbial communities in a desert grassland. Ecology and Evolution, 13, e10300. DOI: 10.1002/ece3.10300.
[76]	Yu FM, Jayawardena RS, Thongklang N, Lv ML, Zhu XT, Zhao Q (2022). Morel production associated with soil nitrogen-fixing and nitrifying microorganisms. Journal of Fungi, 8, 299. DOI: 10.3390/jof8030299.
[77]	Yu ZY, Yan YJ, Liu CX, Huang JP, Xiang WS, Huang SX (2021). Secondary metabolites and genetic system of the rare actinobacteria Lechevalieria rhizosphaerae NEAU-A2. Microbiology China, 48, 2318-2328.
	[余志银, 颜一军, 刘重喜, 黄建萍, 向文胜, 黄胜雄 (2021). 稀有放线菌Lechevalieria rhizosphaerae NEAU-A2的次级代谢产物研究及遗传操作系统的建立. 微生物学通报, 48, 2318-2328.]
[78]	Yuan J, Zhao J, Wen T, Zhao ML, Li R, Goossens P, Huang QW, Bai Y, Vivanco JM, Kowalchuk GA, Berendsen RL, Shen QR (2018). Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome, 6, 156. DOI: 10.1186/s40168-018-0537-x. PMID
[79]	Zeng WA, Wang ZH, Xiao YS, Teng K, Cao ZH, Cai HL, Liu YJ, Yin HQ, Cao PJ, Tao JM (2022). Insights into the interactions between root phenotypic traits and the rhizosphere bacterial community. Current Microbiology, 79, 176. DOI: 10.1007/s00284-022-02870-0.
[80]	Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi SJ, Cho H, Karaoz U, Loqué D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018). Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nature Microbiology, 3, 470-480. DOI PMID
[81]	Zhang JH, He NP, Liu CC, Xu L, Chen Z, Li Y, Wang RM, Yu GR, Sun W, Xiao CW, Chen HYH, Reich PB (2020a). Variation and evolution of C:N ratio among different organs enable plants to adapt to N-limited environments. Global Change Biology, 26, 2534-2543.
[82]	Zhang JY, Liu YX, Zhang N, Hu B, Jin T, Xu HR, Qin Y, Yan PX, Zhang XN, Guo XX, Hui J, Cao SY, Wang X, Wang C, Wang H, et al. (2019). NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology, 37, 676-684.
[83]	Zhang YT, Gao XL, Hao XY, Alexander TW, Shi XJ, Jin L, Thomas BW (2020b). Heavy grazing over 64 years reduced soil bacterial diversity in the foothills of the Rocky Mountains, Canada. Applied Soil Ecology, 147, 103361. DOI: 10.1016/j.apsoil.2019.09.011.
[84]	Zhang ZW, Gao B, Lin CC, Wang Q, Liu JL, Yang N, Su DR, Ping XY (2021). Effects of grazing intensity on biomass allocation patterns of six plant species in a typical grassland. Acta Agrestia Sinica, 29, 149-155.
	[张紫薇, 高斌, 林长存, 王青, 刘佳乐, 杨娜, 苏德荣, 平晓燕 (2021). 放牧强度对典型草原6个物种生物量分配格局的影响. 草地学报, 29, 149-155.] DOI
[85]	Zhao K, Han GD (2023). Responses of the functional traits of dominant species to different grazing intensities in desert steppe. Acta Agrestia Sinica, 31, 649-656. DOI
	[赵坤, 韩国栋 (2023). 荒漠草原优势种功能性状对不同放牧强度的响应. 草地学报, 31, 649-656.] DOI
[86]	Zhao Y, Peth S, Reszkowska A, Gan L, Krümmelbein J, Peng XH, Horn R (2011). Response of soil moisture and temperature to grazing intensity in a Leymus chinensis steppe, Inner Mongolia. Plant and Soil, 340, 89-102.
[87]	Zheng SX, Li WH, Lan ZC, Ren HY, Wang KB (2015). Functional trait responses to grazing are mediated by soil moisture and plant functional group identity. Scientific Reports, 5, 18163. DOI: 10.1038/srep18163.
[88]	Zhou YX, Chen J, Li Y, Hou ZA, Min W (2022). Effects of cotton stalk returning on soil enzyme activity and bacterial community structure diversity in cotton field with long-term saline water irrigation. Environmental Science, 43, 2192-2203.
	[周永学, 陈静, 李远, 侯振安, 闵伟 (2022). 棉秆还田对咸水滴灌棉田土壤酶活性和细菌群落结构多样性的影响. 环境科学, 43, 2192-2203.]