Response of arbuscular mycorrhiza fungi to long-term organic and inorganic fertilization in agricultural soils in dry farming regions

TIAN Xia; WANG Yuan; ZHANG Yu; GUO Rong; MA Kun

doi:10.12357/cjea.20230304

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TIAN X, WANG Y, ZHANG Y, GUO R, MA K. Response of arbuscular mycorrhiza fungi to long-term organic and inorganic fertilization in agricultural soils in dry farming regions[J]. Chinese Journal of Eco-Agriculture, 2023, 31(0): 1−12 doi: 10.12357/cjea.20230304

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Response of arbuscular mycorrhiza fungi to long-term organic and inorganic fertilization in agricultural soils in dry farming regions

doi: 10.12357/cjea.20230304

Key Laboratory of Restoration and Reconstruction of Degraded Ecosystems in Northwest China / Incubation Base of the State Key Laboratory of Land Degradation and Ecological Restoration in Northwest China, Ningxia University, Yinchuan 750021, China

Funds: This study was funded by the Key Research and Development Program of Ningxia Hui Autonomous Region (2018BBF03002, 2019BBF03011) and the National Natural Science Foundation of China (31660132).

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Corresponding author: E-mail: makun0411@163.com
Received Date: 2023-04-27
Accepted Date: 2023-09-28
Rev Recd Date: 2023-10-09

Available Online: 2023-10-15

Abstract

Abstract

The dynamics of arbuscular mycorrhiza (AM) fungal communities are important for effective, long-term soil ecosystem management. To reveal the response mechanisms of soil AM fungi to long-term combined applicatoin of organic and inorganic fertilizers in dryland farming regions, the effects of no fertilizer application (T0), long-term chemical fertilizer application (T1), long-term combined applicatoin of chemical fertilizer and cow manure organic fertilizer (T2), and long-term combined applicatoin of chemical fertilizer and sheep manure organic fertilizer (T3) on soil were investigated using a one-way randomized group design based on 11 consecutive years of locality testing and high-throughput sequencing methods. Differences in the composition and diversity of soil AM fungal communities were compared, and the factors affecting the soil environment and interaction effects that drive changes in soil AM fungal community composition and diversity were investigated. The results indicated that the soil total nitrogen and organic matter contents significantly increased, whereas the pH significantly decreased (P<0.05) under the T2 and T3 treatments compared to those under T0. Furthermore, compared with eight years of fertilization, 11 years of fertilization significantly decreased the total phosphorus and available potassium contents of the soil in the T0, T1, and T3 treatments. The dominant genera of soil AM fungi under organic and inorganic fertilization were Glomus and Paraglomus, respectively. However, the relative abundance of Claroideoglomus decreased significantly and changed from dominant to non-dominant. In contrast, the relative abundance of Claroideoglomus was more susceptible to long-term fertilization than that of Glomus and Paraglomus. After a period of eight years of combined applicaiton of organic and inorganic fertilizers, the relative abundance of AM fungi, specifically Claroideoglomus and Ambispora, in soils under T2 and T3 treatments was significantly different from that of T0 (P<0.05). Over the 11-years fertilization period, the relative abundances of Claroideoglomus and Ambispora under T2 and T3 treatments were not significantly different from those under T0. With the extension of fertilization time, differences in the α diversity of soil AM fungal communities disappeared between treatments. NMDS analysis showed that long-term fertilization changed the β diversity of the soil AM fungal community, but the soil AM fungal community was more similar between the T2 and T3 treatments. During the continuous application of fertilizer, significant changes were observed in the structural composition and diversity of the soil AM fungal community. Moreover, the soil environmental factors influencing changes in the AM fungal community shifted from soil total nitrogen and pH to soil total phosphorus. Long-term combined applicatoin of organic and inorganic fertilizers did not simultaneously improve the main physicochemical properties of soil, such as total phosphorus and available potassium. As the number of years of fertilization increased, the soil factors that drove changes in the structure and diversity of the soil AM fungal communities were significantly altered. The AM fungal community is more easily influenced by sensitive driving factors with changes in all soil environments.
- Arbuscular mycorrhiza fungus,
- Diversity,
- Community composition,
- Combined application of organic and inorganic fertilizers,
- Dry farming regions

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References(55)

References

[1]	KRAUSS M, BERNER A, PERROCHET F, et al. Enhanced soil quality with reduced tillage and solid manures in organic farming — A synthesis of 15 years[J]. Scientific Reports, 2020, 10: 4403 doi: 10.1038/s41598-020-61320-8
[2]	GOSLING P, OZAKI A, JONES J, et al. Organic management of tilled agricultural soils results in a rapid increase in colonisation potential and spore populations of arbuscular mycorrhizal fungi[J]. Agriculture, Ecosystems and Environment, 2010, 139(1/2): 273−279
[3]	王博, 张茹, 刘静, 等. 翻埋与覆盖林木枝条对干旱区沙化土壤及紫花苜蓿根系丛枝菌根真菌的影响[J]. 草业学报, 2023, 32(2): 15−25 WANG B, ZHANG R, LIU J, et al. Effects of incorporated and mulchedtree branches on arbuscular mycorrhizal fungi in the desertified soil and root of alfalfa in arid areas[J]. Acta Prataculturae Sinica, 2023, 32(2): 15−25
[4]	MA M C, ONGENA M, WANG Q F, et al. Chronic fertilization of 37 years alters the phylogenetic structure of soil arbuscular mycorrhizal fungi in Chinese Mollisols[J]. AMB Express, 2018, 8(1): 57 doi: 10.1186/s13568-018-0587-2
[5]	CHEN Y L, ZHANG X, YE J S, et al. Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia[J]. Soil Biology and Biochemistry, 2014, 69: 371−381 doi: 10.1016/j.soilbio.2013.11.020
[6]	ZENG H L, YU L L, LIU P, et al. Nitrogen fertilization has a stronger influence than cropping pattern on AMF community in maize/soybean strip intercropping systems[J]. Applied Soil Ecology, 2021, 167: 104034 doi: 10.1016/j.apsoil.2021.104034
[7]	LIU Y J, SHI G X, MAO L, et al. Direct and indirect influences of 8-yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem[J]. New Phytologist, 2012, 194(2): 523−535 doi: 10.1111/j.1469-8137.2012.04050.x
[8]	王庆峰, 姜昕, 马鸣超, 等. 长期施用氮肥和磷肥对东北黑土丛枝菌根真菌群落组成的影响[J]. 中国农业科学, 2018, 51(17): 3315−3324 WANG Q F, JIANG X, MA M C, et al. Influence of long-term nitrogen and phosphorus fertilization on arbuscular mycorrhizal fungi community in mollisols of northeast China[J]. Scientia Agricultura Sinica, 2018, 51(17): 3315−3324
[9]	CHENG Y, ISHIMOTO K, KURIYAMA Y, et al. Ninety-year-, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities[J]. Plant and Soil, 2013, 365(1): 397−407
[10]	YANG W, GU S Y, XIN Y, et al. Compost addition enhanced hyphal growth and sporulation of arbuscular mycorrhizal fungi without affecting their community composition in the soil[J]. Frontiers in Microbiology, 2018, 9: 169 doi: 10.3389/fmicb.2018.00169
[11]	OEHL F, SIEVERDING E, MÄDER P, et al. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi[J]. Oecologia, 2004, 138(4): 574−583 doi: 10.1007/s00442-003-1458-2
[12]	WU F S, DONG M X, LIU Y J, et al. Effects of long-term fertilization on AM fungal community structure and glomalin-related soil protein in the Loess Plateau of China[J]. Plant and Soil, 2011, 342(1): 233−247
[13]	WANG F Y, HU J L, LIN X G, et al. Arbuscular mycorrhizal fungal community structure and diversity in response to long-term fertilization: a field case from China[J]. World Journal of Microbiology and Biotechnology, 2011, 27(1): 67−74 doi: 10.1007/s11274-010-0427-2
[14]	QIN H, LU K P, STRONG P J, et al. Long-term fertilizer application effects on the soil, root arbuscular mycorrhizal fungi and community composition in rotation agriculture[J]. Applied Soil Ecology, 2015, 89: 35−43 doi: 10.1016/j.apsoil.2015.01.008
[15]	LUO X, SHI S M, LIU Y N, et al. Arbuscular mycorrhizal fungal communities of topsoil and subsoil of an annual maize-wheat rotation after 15-years of differential mineral and organic fertilization[J]. Agriculture, Ecosystems & Environment, 2021, 315: 107442
[16]	鲍士旦. 土壤农化分析[M]. 北京: 中国农业出版社, 2000: 1–329 BAO S D. Soil and Agricultural Chemistry Analysis[M]. Beijing: China Agriculture Press, 2000: 1–329
[17]	马琨, 宋丽丽, 王明国, 等. 玉米秸秆还田对土壤丛枝菌根真菌群落的影响[J]. 应用生态学报, 2019, 30(8): 2746−2756 MA K, SONG L L, WANG M G, et al. Effects of maize straw returning on arbuscular mycorrhizal fungal community structure in soil[J]. Chinese Journal of Applied Ecology, 2019, 30(8): 2746−2756
[18]	马桂秀, 林治安, 李志杰, 等. 有机物料与化肥配施改良盐碱耕地的效果研究[J]. 中国土壤与肥料, 2019(3): 69−75 MA G X, LIN Z A, LI Z J, et al. Effect of combination of organic material and chemical fertilizer on the improvement of saline soil[J]. Soil and Fertilizer Sciences in China, 2019(3): 69−75
[19]	ALEKSEEV I, KRAEV G, SHEIN A, et al. Soil organic matter in soils of suburban landscapes of Yamal region: humification degree and mineralizing risks[J]. Energies, 2022, 15(6): 2301 doi: 10.3390/en15062301
[20]	李成亮, 孔宏敏, 何园球. 施肥结构对旱地红壤有机质和物理性质的影响[J]. 水土保持学报, 2004, 18(6): 116−119 LI C L, KONG H M, HE Y Q. Effect of fertilization structures on soil organic matter and physical properties of upland field in red soil area[J]. Journal of Soil Water Conservation, 2004, 18(6): 116−119
[21]	李娟, 赵秉强, 李秀英, 等. 长期有机无机肥料配施对土壤微生物学特性及土壤肥力的影响[J]. 中国农业科学, 2008, 41(1): 144−152 LI J, ZHAO B Q, LI X Y, et al. Effects of long-term combined application of organic and mineral fertilizers on soil microbiological properties and soil fertility[J]. Scientia Agricultura Sinica, 2008, 41(1): 144−152
[22]	方凯, 孙丽丽, 周昌敏, 等. 长期秸秆还田对双季稻土壤有机碳组分及碳库管理指数的影响[J]. 福建农业学报, 2022, 37(9): 1216−1224 FANG K, SUN L L, ZHOU C M, et al. Effects of long-term spent straw incorporation on organic carbons in soil and carbon pool management at two-crop rice fields[J]. Fujian Journal of Agricultural Sciences, 2022, 37(9): 1216−1224
[23]	赵伟东, 郭宝玲, 郑祥洲, 等. 烟-稻轮作不同施肥土壤N₂O排放对水分的响应[J]. 农业环境科学学报, 2023, 42(7): 1655−1665 ZHAO W D, GUO B L, ZHENG X Z, et al. Effects of moisture content on N₂O emissions in different fertilized soils under tobacco-rice rotation[J]. Journal of Agro-Environment Science, 2023, 42(7): 1655−1665
[24]	朱建华, 李俊良, 李晓林, 等. 几种复合肥施用对蔬菜保护地土壤环境质量的影响[J]. 农业环境保护, 2002, 21(1): 5−8 ZHU J H, LI J L, LI X L, et al. Effects of compound fertilizers utilized on soil environmental quality in protected vegetable field[J]. Agro-Environmental Protection, 2002, 21(1): 5−8
[25]	唐贤, 梁丰, 徐明岗, 等. 长期施用化肥对农田土壤pH影响的整合分析[J]. 吉林农业大学学报, 2020, 42(3): 316−321 TANG X, LIANG F, XU M G, et al. A meta-analysis of effects of long-term application of chemical fertilizer on pH of farmland soil[J]. Journal of Jilin Agricultural University, 2020, 42(3): 316−321
[26]	刘灿, 秦鱼生, 赵秀兰. 长期不同施肥对钙质紫色水稻土重金属累积及有效性的影响[J]. 农业环境科学学报, 2020, 39(7): 1494−1502 LIU C, QIN Y S, ZHAO X L. Long-term effect of fertilization on accumulation and availability of heavy metal in a calcareous paddy soil[J]. Journal of Agro-Environment Science, 2020, 39(7): 1494−1502
[27]	黄福珍, 白志坚, 张与真, 等. 黄土区生土的特性及熟化中肥力变化的研究[J]. 中国农业科学, 1980, 13(1): 52−60 HUANG F Z, BAI Z J, ZHANG Y Z, et al. A study on the characteristics of exposed subsoil and increment of its fertility in mellow process in loess area[J]. Scientia Agricultura Sinica, 1980, 13(1): 52−60
[28]	樊红柱, 陈庆瑞, 秦鱼生, 等. 长期施肥紫色水稻土磷素累积与迁移特征[J]. 中国农业科学, 2016, 49(8): 1520−1529 FAN H Z, CHEN Q R, QIN Y S, et al. Characteristics of phosphorus accumulation and movement in a calcareous purple paddy soil profile as affected by long-term fertilization[J]. Scientia Agricultura Sinica, 2016, 49(8): 1520−1529
[29]	王西和, 吕金岭, 刘骅. 灰漠土小麦-玉米-棉花轮作体系钾平衡与钾肥利用率[J]. 土壤学报, 2016, 53(1): 213−223 WANG X H, LYU J L, LIU H. Potassium balance and use efficiency in grey desert soil under continuous wheat-maize-cotton crop rotation system[J]. Acta Pedologica Sinica, 2016, 53(1): 213−223
[30]	夏颖, 刘冬碧, 张富林, 等. 湖北省主要种植制度农田生态系统钾平衡状况[J]. 生态学杂志, 2014, 33(9): 2395−2401 XIA Y, LIU D B, ZHANG F L, et al. Potassium balance in the agroecosystem of the main cropping systems in Hubei Province[J]. Chinese Journal of Ecology, 2014, 33(9): 2395−2401
[31]	王箫璇, 张敏, 张鑫尧, 等. 不同磷肥对砂姜黑土和红壤磷库转化及冬小麦磷素吸收利用的影响[J]. 中国农业科学, 2023, 56(6): 1113−1126 WANG X X, ZHANG M, ZHANG X Y, et al. Effects of different varieties of phosphate fertilizer application on soil phosphorus transformation and phosphorus uptake and utilization of winter wheat[J]. Scientia Agricultura Sinica, 2023, 56(6): 1113−1126
[32]	SHARPLEY A N, MCDOWELL R W, KLEINMAN P J A. Amounts, forms, and solubility of phosphorus in soils receiving manure[J]. Soil Science Society of America Journal, 2004, 68(6): 2048−2057 doi: 10.2136/sssaj2004.2048
[33]	HUO W G, CHAI X F, WANG X H, et al. Indigenous arbuscular mycorrhizal fungi play a role in phosphorus depletion in organic manure amended high fertility soil[J]. Journal of Integrative Agriculture, 2022, 21(10): 3051−3066 doi: 10.1016/j.jia.2022.07.045
[34]	XUE J F, PU C, LIU S L, et al. Effects of tillage systems on soil organic carbon and total nitrogen in a double paddy cropping system in Southern China[J]. Soil and Tillage Research, 2015, 153: 161−168 doi: 10.1016/j.still.2015.06.008
[35]	何炜. 南山植物园主要观赏园AM真菌多样性研究[D]. 重庆: 西南大学, 2009 HE W. AM fungi diversity in the main ornamental gardens of Chongqing Nanshan Botanical Park[D]. Chongqing: Southwest University, 2009
[36]	BEHIE S W, BIDOCHKA M J. Nutrient transfer in plant-fungal symbioses[J]. Trends in Plant Science, 2014, 19(11): 734−740 doi: 10.1016/j.tplants.2014.06.007
[37]	刘蕾, 徐梦, 张国印, 等. 不同轮作模式下设施土壤丛枝菌根真菌群落结构的季相变化[J]. 应用生态学报, 2021, 32(11): 4095−4106 LIU L, XU M, ZHANG G Y, et al. Seasonal variations of arbuscular mycorrhizal fungal community in greenhouse soil under different rotation systems[J]. Chinese Journal of Applied Ecology, 2021, 32(11): 4095−4106
[38]	徐如玉, 左明雪, 袁银龙, 等. 增施摩西管柄囊霉对甜玉米氮肥增效及土壤丛枝菌根真菌多样性的影响[J]. 福建农业学报, 2020, 35(4): 379−391 XU R Y, ZUO M X, YUAN Y L, et al. Effects of Funneliformis mosseae application on nitrogen utilization by sweet corn and AM fungi diversity in soil[J]. Fujian Journal of Agricultural Sciences, 2020, 35(4): 379−391
[39]	SHENG M, CHEN X D, ZHANG X L, et al. Changes in arbuscular mycorrhizal fungal attributes along a chronosequence of black locust (Robinia pseudoacacia) plantations can be attributed to the plantation-induced variation in soil properties[J]. Science of the Total Environment, 2017, 599/600: 273−283 doi: 10.1016/j.scitotenv.2017.04.199
[40]	张淑彬, 王幼珊, 殷晓芳, 等. 不同施磷水平下AM真菌发育及其对玉米氮磷吸收的影响[J]. 植物营养与肥料学报, 2017, 23(3): 649−657 ZHANG S B, WANG Y S, YIN X F, et al. Development of arbuscular mycorrhizal (AM) fungi and their influences on the absorption of N and P of maize at different soil phosphorus application levels[J]. Journal of Plant Nutrition and Fertilizer, 2017, 23(3): 649−657
[41]	刘文科, 冯固, 李晓林. 磷素形态对AM真菌生长及接种效应的影响[J]. 农业环境科学学报, 2004, 23(5): 968−971 LIU W K, FENG G, LI X L. Effects of applying different forms of phosphorus on maize growth and inoculation of arbuscular mycorrhizal fungi for maize symbiosis[J]. Journal of Agro-Environmental Science, 2004, 23(5): 968−971
[42]	韦素贞, 张好强, 胡文涛, 等. AM真菌和施钾对宁夏枸杞响应干旱胁迫的交互影响[J]. 西北林学院学报, 2016, 31(5): 165−170,260 WEI S Z, ZHANG H Q, HU W T, et al. Interactive effects of arbuscular mycorrhizal fungus and potassium application on response of Lycium barbarum to drought stress[J]. Journal of Northwest Forestry University, 2016, 31(5): 165−170,260
[43]	ŘEZÁČOVÁ V, SLAVÍKOVÁ R, KONVALINKOVÁ T, et al. Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows[J]. Mycorrhiza, 2019, 29(6): 567−579 doi: 10.1007/s00572-019-00921-2
[44]	WANG J C, SONG Y, MA T F, et al. Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil[J]. Applied Soil Ecology, 2017, 112: 42−50 doi: 10.1016/j.apsoil.2017.01.005
[45]	蔡艳, 郝明德, 臧逸飞, 等. 不同轮作制下长期施肥旱地土壤微生物多样性特征[J]. 核农学报, 2015, 29(2): 344−350 doi: 10.11869/j.issn.100-8551.2015.02.0344 CAI Y, HAO M D, ZANG Y F, et al. Effect of long-term fertilization on microbial diversity of black loessial soil based on 454 sequencing technology[J]. Journal of Nuclear Agricultural Sciences, 2015, 29(2): 344−350 doi: 10.11869/j.issn.100-8551.2015.02.0344
[46]	WILLIAMS A, MANOHARAN L, ROSENSTOCK N P, et al. Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange[J]. New Phytologist, 2017, 213(2): 874−885 doi: 10.1111/nph.14196
[47]	HERRMANN L, LESUEUR D, BRÄU L, et al. Diversity of root-associated arbuscular mycorrhizal fungal communities in a rubber tree plantation chronosequence in Northeast Thailand[J]. Mycorrhiza, 2016, 26(8): 863−877 doi: 10.1007/s00572-016-0720-5
[48]	VERBRUGGEN E, RÖLING W F M, GAMPER H A, et al. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils[J]. New Phytologist, 2010, 186(4): 968−979 doi: 10.1111/j.1469-8137.2010.03230.x
[49]	WANG Y, ZHANG W T, LI C Y, et al. Long-term nitrogen and/or phosphorus additions lead to a shift in the diversity of soil arbuscular mycorrhizal fungi and improve rainfed crop yield on the Chinese Loess Plateau[J]. Pedosphere, 2023, https://doi.org/10.1016/j.pedsph.2023.01.009
[50]	NGO H T T, WATTS-WILLIAMS S J, PANAGARIS A, et al. Development of an organomineral fertiliser formulation that improves tomato growth and sustains arbuscular mycorrhizal colonisation[J]. The Science of the Total Environment, 2022, 815: 151977 doi: 10.1016/j.scitotenv.2021.151977
[51]	XIAO D, CHE R X, LIU X, et al. Arbuscular mycorrhizal fungi abundance was sensitive to nitrogen addition but diversity was sensitive to phosphorus addition in Karst ecosystems[J]. Biology and Fertility of Soils, 2019, 55(5): 457−469 doi: 10.1007/s00374-019-01362-x
[52]	XU Z Y, LYU Y C, FANG M J, et al. Diverse and abundant arbuscular mycorrhizal fungi in ecological floating beds used to treat eutrophic water[J]. Applied Microbiology and Biotechnology, 2021, 105(18): 6959−6975 doi: 10.1007/s00253-021-11470-0
[53]	王发园, 刘润进. 环境因子对AM真菌多样性的影响[J]. 生物多样性, 2001, 9(3): 301−305 doi: 10.3321/j.issn:1005-0094.2001.03.015 WANG F Y, LIU R J. Effects of environmental factors on the diversity of arbuscular mycorrhizal fungi[J]. Chinese Biodiversity, 2001, 9(3): 301−305 doi: 10.3321/j.issn:1005-0094.2001.03.015
[54]	YONEYAMA K, XIE X, KUSUMOTO D, et al. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites[J]. Planta, 2007, 227(1): 125−132 doi: 10.1007/s00425-007-0600-5
[55]	BRADLEY K, DRIJBER R A, KNOPS J. Increased N availability in grassland soils modifies their microbial communities and decreases the abundance of arbuscular mycorrhizal fungi[J]. Soil Biology and Biochemistry, 2006, 38(7): 1583−1595 doi: 10.1016/j.soilbio.2005.11.011