Seasonal variations of arbuscular mycorrhizal fungal community in greenhouse soil under different rotation systems

doi:10.13287/j.1001-9332.202111.033

Abstract

Abstract: Soil samples were collected at the fallow period, flowering stage, and fruiting stage of tomato under tomato-melon (TM) and tomato-bean (TB) systems. Illumina MiSeq high-throughput pyrosequencing was performed to analyze the differences in AM fungal community between the two rotation systems. We further analyzed the key factors driving the changes in AM fungal diversity and community composition. Results showed that rotation with legume significantly altered the α-diversity of AM fungi. Shannon diversity and Pielou evenness of AM fungi under the TB system were 24.9% and 24.0% lower than that under TM system, respectively. Compared to the fallow period, richness, Shannon diversity, and phylogenetic diversity of AM fungi at the tomato flowering and fruiting stages decreased significantly by 55.6%-67.5%, 49.6%-51.5%, and 21.4%-23.7%, respectively. Rotation with legume (the TB system) promoted the relative abundance of Glomus in all the three sampling times, but reduced the relative abundance of Paraglomus and Archaeospora at the flowering and fruiting stages. Claroideoglomus was more abundant in soils under the TM system than that under the TB system at the fallow period, but the pattern was the opposite at the flowering stage. Ambispora, Diversispora, and Scutellospora were detected only in soil under the TB system. Results of permutational multivariate analysis of variance (PERMANOVA) and non-metric multidimensional scaling (NMDS) analysis showed that both rotation system and growing stage significantly affected the structure of AM fungal community. Soil moisture, pH, and Olsen-P were the predominant factors controlling the variations in the diversity and composition of AM fungal community. Results of structural equation modeling (SEM) further indicated that rotation system and growing stage affected the variations in AM fungal diversity and community structure indirectly via changing soil pH.

Key words: arbuscular mycorrhiza fungi, high-throughput pyrosequencing, rotation with legumes, structural equation model, tomato.

LIU Lei, XU Meng, ZHANG Guo-yin, WANG Ling, SUN Shi-you, RU Shu-hua, XIAO Guang-min, GAO Jing, LI Pin, MA Li-min. 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.

References 58

[1]	Wagg C, Jansa J, Stadler M, et al. Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology, 2011, 92: 1303-1313
[2]	Chen S, Zhao H, Zou C, et al. Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Frontiers in Microbiology, 2017, 8: 2516, doi: 10.3389/fmicb.2017.02516
[3]	Mardhiah U, Caruso T, Gurnell A, et al. Arbuscular mycorrhizal fungal hyphae reduce soil erosion by surface water flow in a greenhouse experiment. Applied Soil Eco-logy, 2016, 99: 137-140
[4]	Carrara JE, Walter CA, Hawkins JS, et al. Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization. Global Change Biology, 2018, 24: 2721-2734
[5]	任志雨, 贺超兴, 李树和, 等. 丛枝菌根真菌对有机栽培黄瓜生长、产量和品质的影响. 华北农学报, 2008, 23(6): 135-138 [Ren Z-Y, He C-X, Li S-H, et al. Effects of arbuscular mycorrhizal fungi on growth, yield and quality of cucumber in organic culture. Acta Agriculturea Boreali-Sinica, 2008, 23(6): 135-138]
[6]	Wu M, Yan Y, Wang Y, et al. Arbuscular mycorrhizal fungi for vegetable (VT) enhance resistance to Rhizoctonia solani in watermelon by alleviating oxidative stress. Biological Control, 2021, 152, doi: 10.1016/j.biocontrol.2020.104433
[7]	Giri B, Mukerji KG. Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: Evidence for reduced sodium and improved magnesium uptake. Mycorrhiza, 2004, 14: 307-312
[8]	Kapoulas N, Ili ZS, Koukounaras A, et al. Application of arbuscular mycorrhizal inoculum in greenhouse soil with manure induced salinity for organic pepper production. Acta Scientiarum Polonorum-Hortorum Cultus, 2019, 18: 129-139
[9]	Liu RJ, Li Y, Diao ZK, et al. Effects of soil depth and season variation on community structure of arbuscular mycorrhizal fungi in greenhouse soils planted with watermelon. Pedosphere, 2013, 23: 350-358
[10]	杨秀丽, 闫伟. 呼和浩特市保护地蔬菜丛枝菌根真菌初步研究. 华北农学报, 2010, 25(4): 206-208 [Yang X-L, Yan W. A preliminary survey of arbuscular mycorrhizal fungi on greenhouse vegetables in Huhhot District of Inner Mongolia. Acta Agriculturea Boreali-Sinica, 2010, 25(4): 206-208]
[11]	行园园. 设施菜地丛枝菌根真菌的群落特征及对番茄的生长效应. 硕士论文. 太谷: 山西农业大学, 2014 [Xing Y-Y. Infectivity and Community Structure of Arbuscular Mycorrhizal Fungi in the Vegetable Greenhouse and Their Effects on the Tomato Growth. Master Thesis. Taigu: Shanxi Agricultural University, 2014]
[12]	蒋雨含. 长期不同施肥处理对设施番茄生长及丛枝菌根真菌群落的影响. 博士论文. 沈阳: 沈阳农业大学, 2019 [Jiang Y-H. Effects of Long-term Fertilization on Tomato Growth and Arbuscular Mycorrhizal Fungal Communities in Intensive Agroecosystems. PhD Thesis. Shenyang: Shenyang Agricultural University, 2019]
[13]	刘蕾, 王凌, 徐万强, 等. 设施土壤磷素淋失环境阈值及防控措施. 华北农学报, 2019, 34(suppl.1): 197-203 [Liu L, Wang L, Xu W-Q, et al. Environmental threshold and prevention of soil phosphorus leaching in greenhouse soils. Acta Agriculturae Boreali-Sinica, 2019, 34(suppl.1): 197-203]
[14]	于慧颖. 轮作方式对黄瓜根际细菌多样性及产量的影响. 博士论文. 哈尔滨: 东北农业大学, 2008 [Yu H-Y. Study on Cucumber Rhizosphere Bacteria Diversity and Yield of Begetable Crops Rotation. PhD Thesis. Harbin: Northeast Agricultural University, 2008]
[15]	曹明锋, 宁尚辉, 祝利, 等. 烟草-早熟食用豆轮作模式研究. 湖南农业科学, 2019(12): 26-29 [Cao M-F, Ning S-H, Zhu L, et al. Study on rotation mode of tobacco and early maturing edible bean. Hunan Agricultural Siences, 2019(12): 26-29]
[16]	鲍士旦. 土壤农化分析. 第三版. 北京: 中国农业出版社, 2000 [Bao S-D. Soil and Agrochemistry Analysis. 3rd Ed. Beijing: China Agriculture Press, 2000]
[17]	Lee J, Lee S, Young JPW. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology, 2008, 65: 339-349
[18]	Sato K, Suyama Y, Saito M, et al. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction denature gradient gel electrophoresis. Grassland Science, 2005, 51: 179-181
[19]	Chai Y, Jiang S, Guo W, et al. The effect of slope aspect on the phylogenetic structure of arbuscular mycorrhizal fungal communities in an alpine ecosystem. Soil Biology and Biochemistry, 2018, 126: 103-113
[20]	Oksanen J, Blanchet FG, Kindt R, et al. Vegan: Community Ecology Package. R package Version 2.2-1 [EB/OL]. (2015-05-16) [2020-02-08]. http://CRAN.R-project.org/package=vegan
[21]	Kembel SW, Cowan PD, Helmus MR, et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 2010, 26: 1463-1464
[22]	Higo M, Takahashi Y, Gunji K, et al. How are arbuscular mycorrhizal associations related to maize growth performance during short-term cover crop rotation? Journal of the Science of Food and Agriculture, 2018, 98: 1388-1396
[23]	Antoninka A, Johnson RNC. Seven years of carbon dio-xide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytologist, 2011, 192: 200-214
[24]	李聪聪, 周亚星, 谷强, 等. 三江源区典型高寒草地丛枝菌根真菌多样性及构建机制. 草业学报, 2021, 30(1): 46-58 [Li C-C, Zhou Y-X, Gu Q, et al. The species diversity and community assembly of arbuscular mycorrhizal fungi in typical alpine grassland in Sanjiang-yuan region. Acta Prataculturae Sinica, 2021, 30(1): 46-58]
[25]	Kadian N, Yadav K, Aggarwal A. Interactive effect of arbuscular mycorrhizal fungi and potassium on growth and yield in Cyamopsis tetragonoloba (L.) under water stress. Researcher, 2014, 6: 86-91
[26]	朱晨. 不同施肥制度对主要农作物土壤中AMF群落结构的影响. 硕士论文. 南京: 南京农业大学, 2016 [Zhu C. Effects of Different Fertilization on Community Structure of AMF in Major Farmland Crops Soils. Master Thesis. Nanjing: Nanjing Agricultural University, 2016]
[27]	马建辉. 膜下滴灌对设施土壤团聚体稳定性及其AM真菌群落结构的影响. 博士论文. 沈阳: 沈阳农业大学, 2018 [Ma J-H. Effects of Drip Irrigation under Plastic Film on Soil Aggregate Stability and Arbuscular Mycorrhizal Fungi Communities in Soil Aggregate. PhD Thesis. Shenyang: Shenyang Agricultural University, 2018]
[28]	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. 应用生态学报, 2019, 30(8): 228-238 [Ma K, Song L-L, Wang M-G, et al. Effects of maize straw returning on arbuscular mycorrhizal fungal community structure in soil. Chinese Journal of Applied Ecology, 2019, 30(8): 2746-2756]
[29]	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. 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. Scientia Agricultura Sinica, 2018, 51(17): 3315-3324]
[30]	Bainard LD, Bainard JD, Hamel C, et al. Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semiarid prairie agroecosystem. FEMS Microbio-logy Ecology, 2014, 88: 333-344
[31]	Tiemann LK, Grandy AS, Atkinson EE, et al. Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecology Letters, 2015, 18: 761-771
[32]	Ai C, Zhang S, Zhang X, et al. Distinct responses of soil bacterial and fungal communities to changes in fertilization regime and crop rotation. Geoderma, 2018, 319: 156-166
[33]	Mathimaran N, Ruh R, Jama B, et al. Impact of agricultural management on arbuscular mycorrhizal fungal communities in Kenyan ferralsol. Agriculture, Ecosystems and Environment, 2007, 119: 22-32
[34]	Lekberg Y, Koide RT, Twomlow SJ. Effect of agricultural management practices on arbuscular mycorrhizal fungal abundance in low-input cropping systems of southern Africa: A case study from Zimbabwe. Biology and Fertility of Soils, 2008, 44: 917-923
[35]	Tian H, Drijber RA, NIiu XS, et al. Spatio-temporal dynamics of an indigenous arbuscular mycorrhizal fungal community in an intensively managed maize agroecosystem in North China. Applied Soil Ecology, 2011, 47: 141-152
[36]	Pontes JSD, Oehl F, Pereira CD, et al. Diversity of arbuscular mycorrhizal fungi in the Brazilian’s Cerrado and in soybean under conservation and conventional tillage. Applied Soil Ecology, 2017, 117: 178-189
[37]	Rasmussen PU, Hugerth LW, Blanchet FG, et al. Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root-associated soil of a wild perennial herb. New Phytologist, 2018, 220: 1248-1261
[38]	张美庆, 王幼珊, 邢礼军. 环境因子和AM真菌分布的关系. 菌物系统, 1999, 18(1): 25-29 [Zhang M-Q, Wang Y-S, Xing L-J. The relationship between the distribution of AM fungi and environmental factors. Mycosystema, 1999, 18(1): 25-29]
[39]	Carballar-Hernández S, Hernández-Cuevas LV, Montao NM, et al. Native communities of arbuscular mycorrhizal fungi associated with Capsicum annuum L. respond to soil properties and agronomic management under field conditions. Agriculture, Ecosystems and Environment, 2017, 245: 43-51
[40]	冯曾威, 王宁, 朱红惠, 等. 低pH影响丛枝菌根真菌丛枝发育和磷的吸收. 菌物学报, 2017, 36(7): 950-962 [Feng Z-W, Wang N, Zhu H-H, et al. Influences of low pH on the arbuscule development and phosphorus uptake of Rhizophagus intraradices. Mycosystema, 2017, 36(7): 950-962]
[41]	Aarle IMV, Soderstrom B, Olsson PA . Growth and interactions of arbuscular mycorrhizal fungi in soils from limestone and acid rock habitats. Soil Biology and Biochemistry, 2003, 35: 1557-1564
[42]	Řezá čová V, Slavíková R, Konvalinková T, et al. Geo-graphy and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows. Mycorrhiza, 2019, 29: 567-579
[43]	Lekberg Y, Meadow J, Rohr JR, et al. Importance of dispersal and thermal environment for mycorrhizal communities: Lessons from Yellowstone National Park. Eco-logy, 2011, 92: 1292-1302
[44]	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. 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. Journal of Plant Nutrition and Fertilizer, 2017, 23(3): 649-657]
[45]	唐蕊. 柴河流域富磷区优势植物AMF多样性及其对根际土壤磷、氮的影响. 硕士论文. 昆明: 云南大学, 2019 [Tang R. Diversity of AMF and Their Effects on Rhizospheric Phosphorus and Nitrogen of Dominant Plant in Phosphorus Enriched Area at Chaihe Basin. Master Thesis. Kunming: Yunnan University, 2019]
[46]	Anastasiia Z. 气温变化和土地利用方式改变对AMF多样性的影响. 硕士论文. 长春: 东北师范大学, 2018 [Anastasiia Z. Effects of Temperature Change and Land Use Type on Diversity and Structure of AMF Communities. Master Thesis. Changchun: Northeast Normal University, 2018]
[47]	李素美, 王银桥, 刘润进. 特殊生境中丛枝菌根真菌多样性. 应用生态学报, 2013, 24(11): 3325-3332 [Li S-M, Wang Y-Q, Liu R-J. Diversity of arbuscular mycorrhizal fungi in special habitats: A review. Chinese Journal of Applied Ecology, 2013, 24(11): 3325-3332]
[48]	Guzman A, Montes M, Hutchins L, et al. Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytologist, 2021, 231, doi: 10.1111/NPH.17306
[49]	Johnson NC, Wilsen GW, Wilsen JA, et al. Mycorrhizal phenotypes and the law of the minimum. New Phytologist, 2015, 205: 1473-1484
[50]	Bever JD, Morton JB, Antonovics J, et al. Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. Journal of Ecology, 1996, 84: 71-82
[51]	Chen B, Xiao X, Zhu YG, et al. The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Science of the Total Environment, 2007, 379: 226-234
[52]	范洁群, 冯固, 李晓林. 有机磷杀虫剂——灭克磷对丛枝菌根真菌Glomus mosseae生长的效应. 菌物学报, 2006, 25(1): 125-130 [Fan J-Q, Feng G, Li X-L. The impact of ethoprophos, an organic-pesticide, on arbuscular mycorrhizal fungus. Mycosystema, 2006, 25(1): 125-130]
[53]	Jansa J, Mozafar A, Anken T, et al. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza, 2002, 12: 225-234
[54]	Hijri I, Sákorový Z,Oehl F, et al. Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Molecular Ecology, 2010, 15: 2277-2289
[55]	Rosendahl S, McGee P, Morton J. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Molecular Ecology, 2009, 18: 4316-4329
[56]	Daniell T, Husband R, Fitter A, et al. Molecular diversity of arbuscular mycorrhizal fungi colonizing arable crops. FEMS Microbiology Ecology, 2011, 36: 203-209
[57]	Oehl F, Sieverding E, Ineichen K, et al. Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agriculture, Ecosystems and Environment, 2009, 134: 257-268
[58]	赵爱花, 刘蕾, 付伟, 等. 施氮对森林生态系统AM真菌群落组成及多样性的影响. 生态学报, 2020, 40(21): 7576-7587 [Zhao A-H, Liu L, Fu W, et al. Can understory nitrogen addition overestimate the effects of nitrogen deposition on arbuscular mycorrhizal fungal community? Acta Ecologica Sinica, 2020, 40(21): 7576-7587]