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Unraveling fertilization effects on the dynamics of arbuscular mycorrhizal fungal community in the Qinghai-Tibet Alpine Meadow |
Longfei Liu1,2,3, Yi Ren2, Shuo Sun2, Chen Liu2, Kairui Ding2, Rong Li2, Pengfei Zhang1,4(), Biao Shen2, Mohammadhossein Ravanbakhsh5, Wu Xiong2,3(), Qirong Shen2 |
1. College of Ecology, Lanzhou University, Lanzhou 730000, China 2. Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Joint International Research Laboratory of Soil Health, Nanjing Agricultural University, Nanjing 210095, China 3. The Sanya Institute of Nanjing Agricultural University, Sanya 572000, China 4. Department of Ecology, Evolution, and Behavior, University of Minnesota, 1475 Gortner Ave, St. Paul, MN 55108, USA 5. Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands |
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Abstract ● Community structure and composition of AMF shifted under different fertilization. ● Soil physicochemical properties played important roles in contributing plant diversity and biomass. ● Fertilization affected plant and AMF communities through changing soil abiotic properties. ● Acaulospora and Diversispora were highly linked with plant communities. Arbuscular mycorrhizal fungi (AMF) represent a crucial component of soil microorganisms, playing pivotal roles in promoting plant growth by enhancing nutrient availability. However, the responses of AMF communities to different fertilization regimes and their correlations with plant communities in the context of anthropogenic disturbances in alpine meadow ecosystems remain largely unexplored. In this study, we investigated the effects of nitrogen, phosphorus, and combined nitrogen-phosphorus fertilization on AMF communities and their interconnections with plant diversity and biomass based on a seven-year long-term experiment conducted on the Qinghai-Tibet Plateau. Our results showed significant shifts in AMF community structure and composition under different fertilization treatments, while the richness of AMF exhibited no remarkable alterations. Notably, soil pH decreased, and electrical conductivity increased with the increasing nitrogen fertilizer application, emerging as pivotal abiotic factors in predicting plant richness and biomass. Fascinatingly, Acaulospora exhibited a positive correlation with plant richness, serving as an important bioindicator of plant richness, while Diversispora emerged as the primary bioindicator of plant biomass. Our findings shed light on potential correlations between AMF community composition and both plant and soil abiotic factors, driven by nitrogen and phosphorus fertilization. We advocate for the critical significance of balanced fertilization in sustaining beneficial plant–soil–AMF interactions in natural ecosystems as well as agricultural soils.
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Keywords
biodiversity
arbuscular mycorrhizal fungi
nitrogen and phosphorus fertilizer
Qinghai-Tibet Plateau
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Corresponding Author(s):
Pengfei Zhang,Wu Xiong
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Issue Date: 06 May 2024
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|
1 |
M.S., Beauregard, C., Hamel, St-Arnaud, M., Atul-Nayyar, 2010. Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in Alfalfa. Microbial Ecology59, 379–389.
https://doi.org/10.1007/s00248-009-9583-z
|
2 |
N., Begum, C., Qin, M.A., Ahanger, S., Raza, M.I., Khan, M., Ashraf, N., Ahmed, L.X., Zhang, 2019. Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science10, 1068.
https://doi.org/10.3389/fpls.2019.01068
|
3 |
F., Breuillin, J., Schramm, M., Hajirezaei, A., Ahkami, P., Favre, U., Druege, B., Hause, M., Bucher, T., Kretzschmar, E., Bossolini, C., Kuhlemeier, E., Martinoia, P., Franken, U., Scholz, D., Reinhardt, 2010. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. The Plant Journal64, 1002–1017.
https://doi.org/10.1111/j.1365-313X.2010.04385.x
|
4 |
C.L., Chang, F., Nasir, L.N., Ma, C.J., Tian, 2017. Molecular Communication and Nutrient Transfer of Arbuscular Mycorrhizal Fungi, Symbiotic Nitrogen-fixing Bacteria, and Host Plant in Tripartite Symbiosis. In: Sulieman, S., Tran, L.S.P., eds. Legume Nitrogen Fixation in Soils with Low Phosphorus Availability: Adaptation and Regulatory Implication. Cham: Springer International Publishing, 169–183
|
5 |
S.C., Chen, H.J., Zhao, C.C., Zou, Y.S., Li, Y.F., Chen, Z.H., Wang, Y., Jiang, A.R., Liu, P.Y., Zhao, M.M., Wang, G.J., Ahammed, 2017a. Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Frontiers in Microbiology8, 2516.
https://doi.org/10.3389/fmicb.2017.02516
|
6 |
Y.L., Chen, Z.W., Xu, T.L., Xu, S.D., Veresoglou, G.W., Yang, B.D., Chen, 2017b. Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biology and Biochemistry115, 233–242.
https://doi.org/10.1016/j.soilbio.2017.08.024
|
7 |
Y.L., Chen, X., Zhang, J.S., Ye, H.Y., Han, S.Q., Wan, B.D., Chen, 2014. Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia. Soil Biology and Biochemistry69, 371–381.
https://doi.org/10.1016/j.soilbio.2013.11.020
|
8 |
L.J., Dai, J.S., Ge, L.Q., Wang, Q., Zhang, T., Liang, N., Bolan, G., Lischeid, J., Rinklebe, 2022. Influence of soil properties, topography, and land cover on soil organic carbon and total nitrogen concentration: a case study in Qinghai-Tibet Plateau based on random forest regression and structural equation modeling. Science of the Total Environment821, 153440.
https://doi.org/10.1016/j.scitotenv.2022.153440
|
9 |
J.F., Dueñas, T., Camenzind, J., Roy, S., Hempel, J., Homeier, J.P., Suárez, M.C., Rillig, 2020. Moderate phosphorus additions consistently affect community composition of arbuscular mycorrhizal fungi in tropical montane forests in southern Ecuador. New Phytologist227, 1505–1518.
https://doi.org/10.1111/nph.16641
|
10 |
R.C., Edgar, 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics26, 2460–2461.
https://doi.org/10.1093/bioinformatics/btq461
|
11 |
A.F., Fall, G., Nakabonge, J., Ssekandi, H., Founoune-Mboup, S.O., Apori, A., Ndiaye, A., Badji, K., Ngom, 2022. Roles of arbuscular mycorrhizal fungi on soil fertility: contribution in the improvement of physical, chemical, and biological properties of the soil. Frontiers in Fungal Biology3, 723892.
https://doi.org/10.3389/ffunb.2022.723892
|
12 |
M., Fayiah, S.K., Dong, Y., Li, Y.D., Xu, X.X., Gao, S., Li, H., Shen, J.N., Xiao, Y.F., Yang, K., Wessell, 2019. The relationships between plant diversity, plant cover, plant biomass and soil fertility vary with grassland type on Qinghai-Tibetan Plateau. Agriculture, Ecosystems & Environment286, 106659.
|
13 |
S., García, F., Pezzani, A., Rodríguez-Blanco, 2017. Long-term phosphorus fertilization effects on arbuscular mycorrhizal fungal diversity in Uruguayan grasses. Journal of Soil Science and Plant Nutrition17, 1013–1027.
https://doi.org/10.4067/S0718-95162017000400013
|
14 |
X., Guo, Z., Wang, J., Zhang, P., Wang, Y.M., Li, B.M., Ji, 2021. Host-specific effects of arbuscular mycorrhizal fungi on two Caragana species in desert grassland. Journal of Fungi7, 1077.
https://doi.org/10.3390/jof7121077
|
15 |
N., Hijikata, M., Murase, C., Tani, R., Ohtomo, M., Osaki, T., Ezawa, 2010. Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytologist186, 285–289.
https://doi.org/10.1111/j.1469-8137.2009.03168.x
|
16 |
A., Hodge, K., Storer, 2015. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil386, 1–19.
https://doi.org/10.1007/s11104-014-2162-1
|
17 |
H., Huang, 2021. LinkET: everything is linkable. R Package Version 0.0.2.4
|
18 |
J., Jansa, S.T., Forczek, M., Rozmoš, D., Püschel, P., Bukovská, H., Hršelová, 2019. Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chemical and Biological Technologies in Agriculture6, 10.
https://doi.org/10.1186/s40538-019-0147-2
|
19 |
S.J., Jiang, Y.J., Liu, J.J., Luo, M.S., Qin, N.C., Johnson, M., Öpik, M., Vasar, Y.X., Chai, X.L., Zhou, L., Mao, G.Z., Du, L.Z., An, H.Y., Feng, 2018. Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytologist220, 1222–1235.
https://doi.org/10.1111/nph.15112
|
20 |
R.T., Koide, Z., Kabir, 2000. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytologist148, 511–517.
https://doi.org/10.1046/j.1469-8137.2000.00776.x
|
21 |
M., Lang, C.Y., Zhang, W.H., Su, X.X., Chen, C.Q., Zou, X.P., Chen, 2022. Long-term P fertilization significantly altered the diversity, composition and mycorrhizal traits of arbuscular mycorrhizal fungal communities in a wheat-maize rotation. Applied Soil Ecology170, 104261.
https://doi.org/10.1016/j.apsoil.2021.104261
|
22 |
Y., Lekberg, M., Vasar, L.S., Bullington, S.K., Sepp, P.M., Antunes, R., Bunn, B.G., Larkin, M. Öpik, , 2018. More bang for the buck? Can arbuscular mycorrhizal fungal communities be characterized adequately alongside other fungi using general fungal primers? New Phytologist 220, 971–976
|
23 |
C.Y., Li, W.T., Zhang, Y., Wang, Y., Miao, S., Chang, Z.Y., Kou, Q.X., Li, T.H., Dang, 2022. Long-term nitrogen and phosphorus additions change community diversity of arbuscular mycorrhizal fungi and crop yield are mainly determined by Glomus and Paraglomus in the Loess Plateau. DOI:10.21203/rs.3.rs-1557001/v1
|
24 |
J.J., Li, C., Yang, X.L., Liu, X.Q., Shao, 2019. Inconsistent stoichiometry response of grasses and forbs to nitrogen and water additions in an alpine meadow of the Qinghai-Tibet Plateau. Agriculture, Ecosystems & Environment279, 178–186.
|
25 |
A., Liaw, M., Wiener, 2002. Classification and regression by random forest. R News2, 18–22.
|
26 |
C.Y., Lin, Y.X., Wang, M.H., Liu, Q., Li, W.F., Xiao, X.Z., Song, 2020. Effects of nitrogen deposition and phosphorus addition on arbuscular mycorrhizal fungi of Chinese fir (Cunninghamia lanceolata). Scientific Reports10, 12260.
https://doi.org/10.1038/s41598-020-69213-6
|
27 |
X.G., Lin, Y.Z., Feng, H.Y., Zhang, R.R., Chen, J.H., Wang, J.B., Zhang, H.Y., Chu, 2012. Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environmental Science & Technology46, 5764–5771.
|
28 |
M.H., Liu, Y.K., Shen, Q., Li, W.F., Xiao, X.Z., Song, 2021. Arbuscular mycorrhizal fungal colonization and soil pH induced by nitrogen and phosphorus additions affects leaf C:N:P stoichiometry in Chinese fir (Cunninghamia lanceolata) forests. Plant and Soil461, 421–440.
https://doi.org/10.1007/s11104-021-04831-1
|
29 |
L.H., Luginbuehl, G.N., Menard, S., Kurup, H., Van Erp, G.V., Radhakrishnan, A., Breakspear, G.E. D., Oldroyd, P.J., Eastmond, 2017. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science356, 1175–1178.
https://doi.org/10.1126/science.aan0081
|
30 |
M.Y., Ma, Y.J., Zhu, Y.Y., Wei, N.N., Zhao, 2021a. Soil nutrient and vegetation diversity patterns of alpine wetlands on the Qinghai-Tibetan Plateau. Sustainability13, 6221.
https://doi.org/10.3390/su13116221
|
31 |
X.C., Ma, Q.H., Geng, H.G., Zhang, C.Y., Bian, H.Y.H., Chen, D.L., Jiang, X., Xu, 2021b. Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytologist229, 2957–2969.
https://doi.org/10.1111/nph.17077
|
32 |
D., Mahanta, R.K., Rai, S., Dhar, E., Varghese, A., Raja, T.J., Purakayastha, 2018. Modification of root properties with phosphate solubilizing bacteria and arbuscular mycorrhiza to reduce rock phosphate application in soybean-wheat cropping system. Ecological Engineering111, 31–43.
https://doi.org/10.1016/j.ecoleng.2017.11.008
|
33 |
K., Nopphakat, P., Runsaeng, L., Klinnawee, 2022. Acaulospora as the dominant arbuscular mycorrhizal fungi in organic lowland rice paddies improves phosphorus availability in soils. Sustainability14, 31.
|
34 |
J., Oksanen, F.G., Blanchet, M., Friendly, R., Kindt, P., Legendre, D., McGlinn, P.R., Minchin, R.B., O’hara, G.L., Simpson, P., Solymos, 2019. Package ‘vegan’. Community Ecology Package, Version 2
|
35 |
S.R., Olsen, 1954. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. Washington: U.S. Department of Agriculture
|
36 |
P.A., Olsson, J., Rahm, N., Aliasgharzad, 2010. Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiology Ecology72, 125–131.
https://doi.org/10.1111/j.1574-6941.2009.00833.x
|
37 |
M., Öpik, A., Vanatoa, E., Vanatoa, M., Moora, J., Davison, J.M., Kalwij, Ü., Reier, M., Zobel, 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist188, 223–241.
https://doi.org/10.1111/j.1469-8137.2010.03334.x
|
38 |
R., Prasad, D., Bhola, K., Akdi, C., Cruz, S., Kvss, N., Tuteja, A., Varma, 2017. Introduction to mycorrhiza: historical development. In: Varma, A., Prasad, R., Tuteja, N., eds. Mycorrhiza - Function, Diversity, State of the Art. Cham: Springer International Publishing, 1–7
|
39 |
V., Řezáčová, R., Slavíková, T., Konvalinková, L., Zemková, M., Řezáč, M., Gryndler, P., Šmilauer, H., Gryndlerová, H., Hršelová, P., Bukovská, J., Jansa, 2019. Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows. Mycorrhiza29, 567–579.
https://doi.org/10.1007/s00572-019-00921-2
|
40 |
A., Saboor, M.A., Ali, S., Husain, M.S., Tahir, M., Irfan, M., Bilal, K.S., Baig, R., Datta, N., Ahmed, S., Danish, B.R., Glick, 2021. Regulation of phosphorus and zinc uptake in relation to arbuscular mycorrhizal fungi for better maize growth. Agronomy11, 2322.
https://doi.org/10.3390/agronomy11112322
|
41 |
P., Sáez-Plaza, M.J., Navas, S., Wybraniec, T., Michałowski, A.G., Asuero, 2013. An overview of the Kjeldahl method of nitrogen determination. Part II. Sample preparation, working scale, instrumental finish, and quality control. Critical Reviews in Analytical Chemistry43, 224–272.
|
42 |
K., Sato, Y., Suyama, M., Saito, K., Sugawara, 2005. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassland Science51, 179–181.
https://doi.org/10.1111/j.1744-697X.2005.00023.x
|
43 |
J.L., Schroder, H.L., Zhang, K., Girma, W.R., Raun, C.J., Penn, M.E., Payton, 2011. Soil acidification from long-term use of nitrogen fertilizers on winter wheat. Soil Science Society of America Journal75, 957–964.
https://doi.org/10.2136/sssaj2010.0187
|
44 |
G.X., Shi, B.Q., Yao, Y.J., Liu, S.J., Jiang, W.Y., Wang, J.B., Pan, X.Q., Zhao, H.Y., Feng, H.K., Zhou, 2017. The phylogenetic structure of AMF communities shifts in response to gradient warming with and without winter grazing on the Qinghai–Tibet Plateau. Applied Soil Ecology121, 31–40.
https://doi.org/10.1016/j.apsoil.2017.09.010
|
45 |
M.H., Song, F.H., Yu, 2015. Reduced compensatory effects explain the nitrogen-mediated reduction in stability of an alpine meadow on the Tibetan Plateau. New Phytologist207, 70–77.
https://doi.org/10.1111/nph.13329
|
46 |
Y., Song, L., Jin, H.B., Wang, 2018. Vegetation changes along the Qinghai-Tibet Plateau engineering corridor since 2000 induced by climate change and human activities. Remote Sensing10, 95.
https://doi.org/10.3390/rs10010095
|
47 |
S.L., Stürmer, J.D., Bever, J.B., Morton, 2018. Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns. Mycorrhiza28, 587–603.
https://doi.org/10.1007/s00572-018-0864-6
|
48 |
M.G.A., Van Der Heijden, 2002. Arbuscular Mycorrhizal Fungi as a Determinant of Plant Diversity: in Search of Underlying Mechanisms and General Principles. In: van der Heijden, M.G.A., Sanders, I.R., eds. Mycorrhizal Ecology. Berlin, Heidelberg: Springer, 243–265
|
49 |
C., Wang, P.J., White, C.J., Li, 2017. Colonization and community structure of arbuscular mycorrhizal fungi in maize roots at different depths in the soil profile respond differently to phosphorus inputs on a long-term experimental site. Mycorrhiza27, 369–381.
https://doi.org/10.1007/s00572-016-0757-5
|
50 |
Q.F., Wang, M.C., Ma, X., Jiang, D.W., Guan, D., Wei, F.M., Cao, Y.W., Kang, C.B., Chu, S.H., Wu, J., Li, 2020. Influence of 37 years of nitrogen and phosphorus fertilization on composition of rhizosphere arbuscular mycorrhizal fungi communities in black soil of Northeast China. Frontiers in Microbiology11, 539669.
https://doi.org/10.3389/fmicb.2020.539669
|
51 |
Z.H., Wen, H.B., Li, Q., Shen, X.M., Tang, C.Y., Xiong, H.G., Li, J.Y., Pang, M.H., Ryan, H., Lambers, J.B., Shen, 2019. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus‐acquisition strategies of 16 crop species. New Phytologist223, 882–895.
https://doi.org/10.1111/nph.15833
|
52 |
H., Wickham, W., Chang, M.H., Wickham, 2016. Package ‘ggplot2’. Create Elegant Data Visualisations Using the Grammar of Graphics. Version 2, 1–189
|
53 |
H., Wu, J.J., Yang, W., Fu, M.C., Rillig, Z.J., Cao, A.H., Zhao, Z.P., Hao, X., Zhang, B.D., Chen, X.G., Han, 2023. Identifying thresholds of nitrogen enrichment for substantial shifts in arbuscular mycorrhizal fungal community metrics in a temperate grassland of northern China. New Phytologist237, 279–294.
https://doi.org/10.1111/nph.18516
|
54 |
X.J., Xiang, S.M., Gibbons, J.S., He, C., Wang, D., He, Q., Li, Y.Y., Ni, H.Y., Chu, 2016. Rapid response of arbuscular mycorrhizal fungal communities to short-term fertilization in an alpine grassland on the Qinghai-Tibet Plateau. PeerJ4, e2226.
https://doi.org/10.7717/peerj.2226
|
55 |
D., Xiao, R.X., Che, X., Liu, Y.J., Tan, R., Yang, W., Zhang, X.Y., He, Z.H., Xu, K.L., Wang, 2019. Arbuscular mycorrhizal fungi abundance was sensitive to nitrogen addition but diversity was sensitive to phosphorus addition in karst ecosystems. Biology and Fertility of Soils55, 457–469.
https://doi.org/10.1007/s00374-019-01362-x
|
56 |
W., Xiong, A., Jousset, R., Li, M., Delgado-Baquerizo, M., Bahram, R., Logares, B., Wilden, G.A., de Groot, N., Amacker, G.A., Kowalchuk, Q.R., Shen, S., Geisen, 2021. A global overview of the trophic structure within microbiomes across ecosystems. Environment International151, 106438.
https://doi.org/10.1016/j.envint.2021.106438
|
57 |
W., Xiong, Y.Q., Song, K.M., Yang, Y.A., Gu, Z., Wei, G.A., Kowalchuk, Y.C., Xu, A., Jousset, Q.R., Shen, S., Geisen, 2020. Rhizosphere protists are key determinants of plant health. Microbiome8, 27.
https://doi.org/10.1186/s40168-020-00799-9
|
58 |
B., Xu, J.N., Wang, N., Wu, Y., Wu, F.S., Shi, 2018. Seasonal and interannual dynamics of soil microbial biomass and available nitrogen in an alpine meadow in the eastern part of Qinghai–Tibet Plateau, China. Biogeosciences15, 567–579.
https://doi.org/10.5194/bg-15-567-2018
|
59 |
L., Yu, W.T., Zhang, Y.Y., Geng, K.S., Liu, X.Q., Shao, 2022. Cooperation with arbuscular mycorrhizal fungi increases plant nutrient uptake and improves defenses against insects. Frontiers in Ecology and Evolution10, 833389.
https://doi.org/10.3389/fevo.2022.833389
|
60 |
L., Zhang, N., Shi, J.Q., Fan, F., Wang, T.S., George, G., Feng, 2018. Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environmental Microbiology20, 2639–2651.
https://doi.org/10.1111/1462-2920.14289
|
61 |
P.F., Zhang, E.T., Borer, E.W., Seabloom, M.B., Soons, M.M., Hefting, G.A., Kowalchuk, P.B., Adler, C.J., Chu, X.L., Zhou, C.S., Brown, Z., Guo, X.H., Zhou, Z.G., Zhao, G.Z., Du, Y., Hautier, 2023. Space resource utilization of dominant species integrates abundance‐ and functional‐based processes for better predictions of plant diversity dynamics. Oikos2023, e09519.
https://doi.org/10.1111/oik.09519
|
62 |
P.F., Zhang, X.L., Zhou, J.Y., Li, Z., Guo, G.Z., Du, 2015a. Space resource utilisation: a novel indicator to quantify species competitive ability for light. Scientific Reports5, 16832.
https://doi.org/10.1038/srep16832
|
63 |
R.Z., Zhang, Y., Mu, X.R., Li, S.M., Li, P., Sang, X.R., Wang, H.L., Wu, N., Xu, 2020. Response of the arbuscular mycorrhizal fungi diversity and community in maize and soybean rhizosphere soil and roots to intercropping systems with different nitrogen application rates. Science of the Total Environment740, 139810.
https://doi.org/10.1016/j.scitotenv.2020.139810
|
64 |
Y., Zhang, Q.Z., Gao, S.K., Dong, S.L., Liu, X.X., Wang, X.K., Su, Y.Y., Li, L., Tang, X.Y., Wu, H.D., Zhao, 2015b. Effects of grazing and climate warming on plant diversity, productivity and living state in the alpine rangelands and cultivated grasslands of the Qinghai-Tibetan Plateau. The Rangeland Journal37, 57–65.
https://doi.org/10.1071/RJ14080
|
65 |
Y.J., Zhang, C., Ye, Y.W., Su, W.C., Peng, R., Lu, Y.X., Liu, H.C., Huang, X.H., He, M., Yang, S.S., Zhu, 2022. Soil Acidification caused by excessive application of nitrogen fertilizer aggravates soil-borne diseases: Evidence from literature review and field trials. Agriculture, Ecosystems & Environment340, 108176.
|
66 |
H., Zhou, D.G., Zhang, Z.H., Jiang, P., Sun, H.L., Xiao, W., Yuxin, J.G., Chen, 2019. Changes in the soil microbial communities of alpine steppe at Qinghai-Tibetan Plateau under different degradation levels. Science of the Total Environment651, 2281–2291.
https://doi.org/10.1016/j.scitotenv.2018.09.336
|
67 |
X.C., Zhu, W.Y., Yang, F.B., Song, X.N., Li, 2020. Diversity and composition of arbuscular mycorrhizal fungal communities in the cropland black soils of China. Global Ecology and Conservation22, e00964.
https://doi.org/10.1016/j.gecco.2020.e00964
|
68 |
N., Zong, G.S., Zhao, P.L., Shi, 2019. Different sensitivity and threshold in response to nitrogen addition in four alpine grasslands along a precipitation transect on the northern Tibetan Plateau. Ecology and Evolution9, 9782–9793.
https://doi.org/10.1002/ece3.5514
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