Biodiversity Science ›› 2016, Vol. 24 ›› Issue (8): 907-915.doi: 10.17520/biods.2016100

• Orginal Article • Previous Article     Next Article

Effects of soil biota influenced by long-term organic and chemical fertilizers on rice growth and resistance to insects

Linhui Jiang1, Ling Luo1, Zhenggao Xiao1, Daming Li2, Xiaoyun Chen1, Manqiang Liu1, *(), Feng Hu1   

  1. 1 Soil Ecology Laboratory, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095
    2 Jiangxi Institute of Red Soil, Nanchang 331717
  • Received:2016-04-08 Accepted:2016-05-19 Online:2016-09-02
  • Liu Manqiang

Fertilization plays an important role in soil quality, food supply and security. Although promoting soil biological development is considered as one of the most critical components that organic fertilizers exert on soil compared with chemical fertilization, less attention has been paid to the fertilization-derived influence on crop growth and insect-resistance via soil biota. Understanding the role of soil biota in crop growth and resistance to insects would not only help explain the biological mechanisms of the fertilization effects on soil functions, but also help identify integrative management techniques for soils and crops. Soil suspension was extracted from long-term organically fertilized soils and chemically fertilized soils. Then, the soil suspension was sterilized or non-sterilized to investigate the soil biota’s effects on rice growth and insect-resistance through a soil-free cultured method. Results showed that soil biota and fertilization significantly affected soil nutrient status (P < 0.01). Soil biota decreased soil ammonium content, rice biomass, shoot nitrogen content and the biomass of Nilaparvata lugens, but increased soil nitrate content, rice root-shoot ratio and the contents of root nitrogen, soluble sugar and phenolics (P < 0.05). Meanwhile, soil biota from organically fertilized soils promoted the synthesis of shoot soluble sugar and shoot phenolics. With the addition of Nilaparvata lugens, soil biota significantly reduced rice nitrogen uptake and promoted phenolic synthesis (P < 0.05). Collectively, soil biota, especially from organically fertilized soils, promoted rice resistance traits by altering the nutrient allocation of rice between aboveground and belowground, and by increasing the root-shoot ratio and the synthesis of phenols.

Key words: soil biota, fertilization, aboveground-belowground, herbivory, nutrient allocation, insect-resistance

Table 1

Physicochemical properties of original and sterilized soils (mean ± SD, n = 4)"

对照 Non-sterilized 灭活 Sterilized
化肥 Chemical fertilizer 有机肥 Organic fertilizer 化肥 Chemical fertilizer 有机肥 Organic fertilizer
铵态氮 NH4+-N (mg/kg) 4.34 ± 0.73 2.19 ± 0.53 18.36 ± 0.63 27.35 ± 0.38
硝态氮 NO3--N (mg/kg) 75.97 ± 9.73 147.13 ± 3.53 73.12 ± 3.65 143.23 ± 2.65
可溶性有机碳 DOC (mg/kg) 43.86 ± 11.90 34.27 ± 5.56 712.86 ± 4.71 1,074.73 ± 21.17
速效磷 AP (mg/kg) 135.34 ± 1.26 101.01 ± 0.68 21.88 ± 0.00 10.02 ± 0.39
速效钾 AK (mg/kg) 21.03 ± 0.00 34.96 ± 1.51 38.68 ± 1.38 67.00 ± 2.57
pH (H2O) 6.01 ± 0.21 6.25 ± 0.26 5.77 ± 0.22 5.93 ± 0.23

Table 2

ANOVA results showing the effects of soil biological factor (non-sterilized vs. sterilized), fertilization management (chemical vs. organic fertilizer) and brown planthopper (with vs. without planthoppers) on content of soil NH4+-N, NO3--N, dissolved organic carbon (DOC), pH, shoot mass, root mass, R/S ratio."

自由度 铵态氮 硝态氮 可溶性有机碳 pH 茎叶重 根系重 根冠比
df NH4+-N NO3--N DOC (H2O) Shoot mass Root mass R/S ratio
灭活 Sterilization (S) 1 427.12** 62.10** 108.76** 60.98** 151.95** 47.66** 28.22**
施肥 Fertilization (F) 1 11.48** 16.70** 22.65** 27.48** 9.28** 0.10NS 1.24NS
飞虱 Planthopper (P) 1 2.08NS 7.89** 0.05NS 0.07NS 210.59** 10.66** 101.71**
灭活×施肥 Sterilization × Fertilization (S × F) 1 7.16* 0.28NS 11.46** 0.94NS 9.44** 3.77NS 8.18**
灭活×飞虱 Sterilization × Planthopper (S × P) 1 0.25NS 3.60NS 0.17NS 6.05* 20.62** 2.39NS 0.30NS
施肥×飞虱 Fertilization × Planthopper (F × P) 1 1.13NS 2.51NS 0.60NS 0.17NS 1.89NS 5.06* 1.51NS
Sterilization × Fertilization × Planthopper (S × F × P)
1 0.19NS 1.66NS 1.52NS 1.41NS 1.99NS 2.53NS 2.74NS
Error 24

Fig. 1

Effects of soil biological factor (non-sterilized vs. sterilized), fertilization management (chemical vs. organic fertilizer) and brown planthopper (with vs. without planthoppers) on the content of soil NH4+-N、NO3--N、DOC and pH. Different letters among the treatments mean significant differences, P < 0.05."

Fig. 2

Effects of soil biological factor (non-sterilized vs. sterilized), fertilization management (chemical vs. organic fertilizer) and brown planthopper (with vs. without planthoppers) on shoot mass, root mass and root to shoot ratio. Different letters among the treatments mean significant differences, P < 0.05."

Table 3

ANOVA results showing the effects of soil biological factor (non-sterilized vs. sterilized), fertilization management (chemical vs. organic fertilizer) and brown planthopper (with vs. without planthoppers) on the content of nitrogen, soluble sugar, phenolic in shoot and root, respectively."

Shoot N
Root N
Shoot sugar
Root sugar
Shoot phenolic
Root phenolic
灭活 Sterilization (S) 1 151.95** 35.50** 9.56** 39.27** 20.41** 15.22**
施肥 Fertilization (F) 1 9.28** 27.93** 31.76** 0.39NS 7.71* 10.49**
飞虱 Planthopper (P) 1 210.59** 72.93** 83.24** 2.73NS 1.59NS 0.57NS
灭活×施肥 Sterilization × Fertilization (S × F) 1 9.44** 50.35** 0.02NS 0.023NS 0.62NS 10.82**
灭活×飞虱 Sterilization × Planthopper (S × P) 1 20.62** 2.00NS 11.45** 0.42NS 5.31* 0.53NS
施肥×飞虱 Fertilization × Planthopper (F × P) 1 1.89NS 5.42* 3.18NS 2.65NS 0.30NS 2.06NS
Sterilization × Fertilization × Planthopper (S × F × P)
1 1.99NS 6.18* 0.06NS 12.86** 4.68* 0.73NS
Error 24

Fig. 3

Effects of soil biological factor (non-sterilized vs. sterilized), fertilization management (chemical vs. organic fertilizer) and brown planthopper (with vs. without planthoppers) on the content of shoot total nitrogen, root total nitrogen, shoot soluble sugar, root soluble sugar, shoot phenolics and root phenolics. Different letters among the treatments mean significant differences, P < 0.05."

Fig. 4

Effects of soil biological factor (non-sterilized vs. sterilized) and fertilization management (chemical vs. organic fertilizer) on planthopper mass. Different letters among the treatments mean significant differences, P < 0.05."

Fig. 5

Principle component analysis (PCA) of plant and soil properties affected by soil biological factor, fertilization management and planthopper.□ plant metabolome and soil physicochemical property; ● different treatments."

[1] Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols, 2, 875-877.
[2] Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil and Tillage Research, 72, 203-211.
[3] Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM (2013) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytologist, 198, 264-273.
[4] Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant and Soil, 360, 1-13.
[5] Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology, 84, 2258-2268.
[6] Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature, 515, 505-511.
[7] Bardgett RD, Wardle D (2010) Biotic interactions in soil as drivers of ecosystem properties. In: Aboveground- Belowground Linkages, Biotic Interactions, Ecosystem Processes, and Global Change (eds Bardgett RD, Wardle D), pp.15-61. Oxford University Press, New York.
[8] Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478-486.
[9] Bissett A, Brown MV, Siciliano SD, Thrall PH (2013) Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecology Letters, 16, 128-139.
[10] Cohen MB, Alam SN, Medina EB, Bernal CC (1997) Brown planthopper, Nilaparvata lugens, resistance in rice cultivar IR64: mechanism and role in successful N. lugens management in Central Luzon, Philippines. Entomologia Experimentalis et Applicata, 85, 221-229.
[11] D’Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TC (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell & Environment, 37, 813-826.
[12] Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350-356.
[13] Erb M (2012) The role of roots in plant defence. In: Plant Defence: Biological Control (eds Mérillon JM, Ramawat KG), pp. 291-309. Springer Netherlands Press, Berlin.
[14] Fu SL (2007) A review and perspective on soil biodiversity research. Biodiversity Science, 15, 109-115. (in Chinese with English abstract)
[傅声雷 (2007) 土壤生物多样性的研究概况与发展趋势. 生物多样性, 15, 109-115.]
[15] Gu YF, Zhang XP, Tu SH, Sun XF (2008) Effect of long-term fertilization on nitrification and nitrobacteria community in a purple paddy soil under rice-wheat rotations. Acta Ecologica Sinica, 28, 2123-2130. (in Chinese with English abstract)
[辜运富, 张小平, 涂仕华, 孙锡发 (2008) 长期定位施肥对紫色水稻土硝化作用及硝化细菌群落结构的影响. 生态学报, 28, 2123-2130.]
[16] Jiang T, Zhao JL, Cheng JJ, Xu S, Su W, Bao SW, Liu F (2011) Effects of rice varieties and nitrogen fertilizer application rates on the occurrence of the brown planthopper, Nilaparvata lugens under field conditions. Chinese Journal of Applied Entomology, 48, 1359-1368. (in Chinese with English abstract)
[江涛, 赵俊玲, 程建军, 徐帅, 苏文, 包善微, 刘芳 (2011) 水稻品种与氮肥施用水平对田间褐飞虱发生的影响. 应用昆虫学报, 48, 1359-1368.]
[17] Jiang ZG, Qin HN, Liu YN, Ji LQ, Ma KP (2015) Protecting biodiversity and promoting sustainable development: in memory of the releasing of Catalogue of Life China 2015 and China Biodiversity Red List on the International Day for Biological Diversity 2015. Biodiversity Science, 23, 433-434. (in Chinese)
[蒋志刚, 覃海宁, 刘忆南, 纪力强, 马克平 (2015) 保护生物多样性, 促进可持续发展——纪念《中国生物物种名录》和《中国生物多样性红色名录》发布. 生物多样性, 23, 433-434.]
[18] Kenmore PE (1980) Ecology and Outbreaks of a Tropical Insects Pest of the Green Revolution, the Rice Brown Planthopper, Nilaparvata lugens (Stal). PhD dissertation, University of California, Berkeley.
[19] Lazcano C, Gómez-Brandón M, Revilla P, Domínguez J (2013) Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function. Biology and Fertility of Soils, 49, 723-733.
[20] Liu M, Bjørnlund L, Rønn R, Christensen S, Ekelund F (2012) Disturbance promotes non-indigenous bacterial invasion in soil microcosms: analysis of the roles of resource availability and community structure. PLoS ONE, 7, e45306.
[21] Liu MQ, Huang JH, Chen XY, Wang F, Ge C, Su Y, Shao B, Tang Y, Li HX, Hu F (2009) Aboveground herbivory by the brown planthopper (Nilaparvata lugens) affects soil nematode communities under different rice varieties. Biodiversity Science, 17, 431-439. (in Chinese with English abstract)
[刘满强, 黄菁华, 陈小云, 王峰, 葛成, 苏昱, 邵波, 汤英, 李辉信, 胡锋 (2009) 地上部植食者褐飞虱对不同水稻品种土壤线虫群落的影响. 生物多样性, 17, 431-439.]
[22] Lu RK (2000) Analysis Method of Soil Agricultural Chemistry. China Agricultural Science and Technology Press, Beijing.
(in Chinese) [鲁如坤 (2000) 土壤农业化学分析方法. 中国农业科技出版社, 北京.]
[23] Martinuz A, Schouten A, Menjivar RD, Sikora RA (2012) Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biological Control, 62, 206-212.
[24] Megali L, Schlau B, Rasmann S (2015) Soil microbial inoculation increases corn yield and insect attack. Agronomy for Sustainable Development, 35, 1511-1519.
[25] Phelan PL, Mason JF, Stinner BR (1995) Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hübner), on Zea mays L.: a comparison of organic and conventional chemical farming. Agriculture, Ecosystems & Environment, 56, 1-8.
[26] Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. The ISME Journal, 7, 1609-1619.
[27] Pineda A, Zheng SJ, van Loon JJA, Dicke M (2012) Rhizobacteria modify plant-aphid interactions: a case of induced systemic susceptibility. Plant Biology, 14, 83-90.
[28] Roger A, Getaz M, Rasmann S, Sanders IR (2013) Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference. Ecological Entomology, 38, 330-338.
[29] Senthil-Nathan S, Choi MY, Paik CH, Seo HY, Kalaivani K (2009) Toxicity and physiological effects of neem pesticides applied to rice on the Nilaparvata lugens, the brown planthopper. Ecotoxicology and Environmental Safety, 72, 1707-1713.
[30] Shavit R, Ofek-Lalzar M, Burdman S, Morin S (2013) Inoculation of tomato plants with rhizobacteria enhances the performance of the phloem-feeding insect Bemisia tabaci. Frontiers in Plant Science, 4, 1-12.
[31] Shi LL, Fu SL (2014) Review of soil biodiversity research: history, current status and future challenges. Chinese Science Bulletin, 59, 493-509. (in Chinese)
[时雷雷, 傅声雷 (2014) 土壤生物多样性研究: 历史, 现状与挑战. 科学通报, 59, 493-509.]
[32] Soler R, van der Putten WH, Harvey JA, Vet LE, Dicke M, Bezemer TM (2012) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. Journal of Chemical Ecology, 38, 755-767.
[33] Su T, Xu HX, Han HL, Yang YJ, Wang GY, Zheng XS, Lü ZX (2014) Soil microbe quantities and enzyme activities in rhizosphere of different rice varieties fed by brown planthoppers. Chinese Journal of Rice Science, 28, 322-326. (in Chinese with English abstract)
[苏婷, 徐红星, 韩海亮, 杨亚军, 王桂跃, 郑许松, 吕仲贤 (2014) 褐飞虱胁迫对不同抗性水稻品种根际土壤酶活性和微生物含量的影响. 中国水稻科学, 28, 322-326.]
[34] Tang Y, Liu MQ, Wang F, Chen FJ, Shao B, Su Y, Ge C, Huang JH, Li HX, Hu F (2010) Herbivory by the brown planthopper (Nilaparvata lugens) affects rice seeding growth and belowground soil labile erganic carbon and nitrogen fractions. Acta Ecologica Sinica, 30, 2890-2898. (in Chinese with English abstract)
[汤英, 刘满强, 王峰, 陈法军, 邵波, 苏昱, 葛成, 黄菁华, 李辉信, 胡锋 (2010) 褐飞虱对水稻苗期生长及地下部土壤活性碳氮的影响. 生态学报, 30, 2890-2898.]
[35] Wang J, Zhu B, Zhang J, Müller C, Cai Z (2015) Mechanisms of soil N dynamics following long-term application of organic fertilizers to subtropical rain-fed purple soil in China. Soil Biology and Biochemistry, 91, 222-231.
[36] Zha Y, Wu XP, Zhang HM, Cai DX, Zhu P, Gao HJ (2015) Effects of long-term organic and inorganic fertilization on enhancing soil organic carbon and basic soil productivity in black soil. Scientia Agricultura Sinica, 48, 4649-4659. (in Chinese with English abstract)
[查燕, 武雪萍, 张会民, 蔡典雄, 朱平, 高洪军 (2015) 长期有机无机配施黑土土壤有机碳对农田基础地力提升的影响. 中国农业科学, 48, 4649-4659.]
[37] Zhu Q, Riley WJ, Tang J, Koven CD (2016) Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests. Biogeosciences, 13, 341-363.
[1] Zhu Baijing, Xue Jingrong, Xia Rong, Jin Miaomiao, Wu You, Tian Shanyi, Chen Xiaoyun, Liu Manqiang, Hu Feng. (2019) Effect of soil nematode functional guilds on plant growth and aboveground herbivores . Biodiv Sci, 27(4): 409-418.
[2] Yu Wensheng, Guo Yaolin, Jiang Jiajia, Sun Keke, Ju Ruiting. (2019) Comparison of the life history of a native insect Laelia coenosa with a native plant Phragmites australis and an invasive plant Spartina alterniflora . Biodiv Sci, 27(4): 433-438.
[3] Zhuang Ping. (2019) Progress on the fertility of Rhododendron . Biodiv Sci, 27(3): 327-338.
[4] Zhengjun Guan,Shunbao Lu,Yanlin Huo,Haoyong Hao,Jianbin Cao,Wei Wei,Biao Liu. (2018) Effects of Bt crops on non-target insect pests . Biodiv Sci, 26(6): 636-644.
[5] Yu Zhang, Zhenggao Xiao, Linhui Jiang, Lei Qian, Xiaoyun Chen, Fajun Chen, Feng Hu, Manqiang Liu. (2018) Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests . Biodiv Sci, 26(12): 1296-1307.
[6] Jiliang Liu, Fengrui Li. (2018) Effects of oasis expansion regimes on ecosystem function and dominant functional groups of soil biota in arid regions . Biodiv Sci, 26(10): 1116-1126.
[7] Ying Sun, Lei Wang, Xue Yang, Axiang Wang, Miao He. (2017) Research on the Double Fertilization of Adonis amurensis . Chin Bull Bot, 52(4): 480-486.
[8] Yang-Qing LUO, Mei-Sheng YU, Jing-Jing YU, Shi-Lu ZHENG, Jia-Jia LIU, Ming-Jian YU. (2017) Effects of plant traits and the relative abundance of common woody species on seedling herbivory in the Thousand Island Lake region . Chin J Plan Ecolo, 41(10): 1033-1040.
[9] Qing-Pei YANG, Ming OUYANG, Guang-Yao YANG, Qing-Ni SONG, Chun-Lan GUO, Xiang-Min FANG, Xin CHEN, Lan HUANG, Fu-Sheng CHEN. (2016) Research on ecological stoichiometry in bamboos: From biological basis to applications in silviculture of bamboo forests . Chin J Plan Ecolo, 40(3): 264-278.
[10] Bin-Bin KONG, Xin-Hua WEI, Jia-Li DU, Ying-Nian LI, Zhi-Hong ZHU. (2016) Effects of clipping and fertilization on the temporal dynamics of species diversity and functional diversity and their relationships in an alpine meadow . Chin J Plan Ecolo, 40(3): 187-199.
[11] JIN Wan-Yu,LI Ming,HE Yang-Hui,DU Zheng-Gang,SHAO Jun-Jiong,ZHANG Guo-Dong,ZHOU Ling-Yan,ZHOU Xu-Hui. (2015) Effects of different levels of nitrogen fertilization on soil respiration during growing season in winter wheat (Triticum aestivum) . Chin J Plan Ecolo, 39(3): 249-257.
[12] WANG Qing-Kui,LI Yan-Peng,ZHANG Fang-Yue,HE Tong-Xin. (2015) Short-term nitrogen fertilization decreased root and microbial respiration in a young Cunninghamia lanceolata plantation . Chin J Plan Ecolo, 39(12): 1166-1175.
[13] Ding Ma, Ruiting Ju, Bo Li. (2015) Preference of Laelia coenosa for native and introduced populations of invasive Spartina alterniflora . Biodiv Sci, 23(1): 101-108.
[14] GAO Ben-Qiang, YUAN Zi-Qiang, WANG Bin-Xian, GAO Hui, and ZHANG Rong. (2014) Effects of fertilization and clipping on species diversity, productivity and their relationship in subalpine meadow . Chin J Plan Ecolo, 38(5): 417-424.
[15] ZHU Qiang-Gen, JIN Ai-Wu, WANG Yi-Kun, QIU Yong-Hua, LI Xue-Tao, and ZHANG Si-Hai. (2013) Biomass allocation of branches and leaves in Phyllostachys heterocycla ‘Pubescens’ under different management modes: allometric scaling analysis . Chin J Plan Ecolo, 37(9): 811-819.
Full text