Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Effects of biological agents on soil microbiology, enzyme activity and fruit quality of kiwifruit with root rot

Yongli Ku https://orcid.org/0000-0003-3460-8455 A # , Guoyi Xu B # , Shaoxin Su C and Cuiling Cao D *
+ Author Affiliations
- Author Affiliations

A College of Forestry, Northwest A&F University, Yangling 712100, People’s Republic of China.

B Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou 450000, People’s Republic of China.

C College of Foreign Language, Shangqiu University, Shangqiu 476000, People’s Republic of China.

D College of Life Sciences, Northwest A&F University, Yangling 712100, People’s Republic of China.

* Correspondence to: cuilingcao@163.com
# These authors contributed equally to this paper

Handling Editor: Samuel Abiven

Soil Research 60(3) 279-293 https://doi.org/10.1071/SR20311
Submitted: 6 November 2020  Accepted: 30 August 2021   Published: 9 November 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Root rot is common for kiwifruit (Actinidia chinensis var. diliciosa) plants. It is not easily controlled by chemical methods, and biological agents are an alternative.

Aims: This study investigated the effects of biological agents on the activity and diversity of soil microorganisms, soil enzyme activity and physicochemical indices during the growth period of kiwifruit plants.

Methods: There were four treatments: (1) root-rot plants applied with traditional fertiliser (RP); (2) root-rot plants applied with biological agents CY (CY); (3) root-rot plants applied with biological agents CL (CL); and (4) healthy plants with traditional fertiliser (HP). Most samples were taken during the growth period of kiwifruit plants, while activities of defensive-related enzymes and quality of kiwifruits were tested in the fructescence period.

Key results: CY and CL treatments significantly improved microbial activity, changed microbial structure, increased the diversity, richness and uniformity of microbial species, and altered the relative utilisation ratio of six carbon sources. Soil nutrients of kiwifruit plants with root rot improved with CY and CL compared to RP. Health of kiwifruit plants with CY and CL also improved compared to RP. Activities of defensive-related enzymes in CY and CL treatments were significantly higher than in RP treatment (P < 0.05). Fruit quality indices were also higher than RP.

Conclusions: CY and CL changed the microbial communities in soil, and improved soil nutrients and plant health.

Implications: By altering the soil microbial structure, biological agents used to control root rot in kiwifruit plants improved tree health and fruit quality, and provide an alternative to chemical control of root rot.

Keywords: biological agents, defensive-related enzymes, fruit quality, microbial community diversity, root-rot plants, soil available nutrients content, soil enzyme activity.


References

Acosta-Martínez V, Acosta-Mercado D, Sotomayor-Ramírez D, Cruz-Rodríguez L (2008) Microbial communities and enzymatic activities under different management in semiarid soils. Applied Soil Ecology 38, 249–260.
Microbial communities and enzymatic activities under different management in semiarid soils.Crossref | GoogleScholarGoogle Scholar |

Adamczyk B, Kitunen V, Smolander A (2009) Polyphenol oxidase, tannase and proteolytic activity in relation to tannin concentration in the soil organic horizon under silver birch and Norway spruce. Soil Biology and Biochemistry 41, 2085–2093.
Polyphenol oxidase, tannase and proteolytic activity in relation to tannin concentration in the soil organic horizon under silver birch and Norway spruce.Crossref | GoogleScholarGoogle Scholar |

Amira MB, Lopez D, Mohamed AT, Khouaja A, Chaar H, Fumanal B, et al. (2017) Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biological Control 110, 70–78.
Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees.Crossref | GoogleScholarGoogle Scholar |

Bao SD (2000) ‘Soil and agricultural chemistry analysis’. (China Agriculture Press: Beijing)

Barnett S, Zhao S, Ballard R, Franco C (2017) Selection of microbes for control of Rhizoctonia root rot on wheat using a high throughput pathosystem. Biological Control 113, 45–57.
Selection of microbes for control of Rhizoctonia root rot on wheat using a high throughput pathosystem.Crossref | GoogleScholarGoogle Scholar |

Bastida F, Kandeler E, Moreno JL, Ros M, García C, Hernández T (2008) Application of fresh and composted organic wastes modifies structure, size and activity of soil microbial community under semiarid climate. Applied Soil Ecology 40, 318–329.
Application of fresh and composted organic wastes modifies structure, size and activity of soil microbial community under semiarid climate.Crossref | GoogleScholarGoogle Scholar |

Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A, et al. (2012) Critical review: Vegetables and fruit in the prevention of chronic diseases. European Journal of Nutrition 51, 637–663.
Critical review: Vegetables and fruit in the prevention of chronic diseases.Crossref | GoogleScholarGoogle Scholar | 22684631PubMed |

Bragazza L, Fontana M, Guillaume T, et al. (2021) Nutrient stoichiometry of a plant–microbe–soil system in response to cover crop species and soil type. Plant and Soil 461, 517–531.
Nutrient stoichiometry of a plant–microbe–soil system in response to cover crop species and soil type.Crossref | GoogleScholarGoogle Scholar |

Cai F, Pang G, Li R-X, Li R, Gu X-L, Shen Q-R, Chen W (2017) Bioorganic fertilizer maintains a more stable soil microbiome than chemical fertilizer for monocropping. Biology and Fertility of Soils 53, 861–872.
Bioorganic fertilizer maintains a more stable soil microbiome than chemical fertilizer for monocropping.Crossref | GoogleScholarGoogle Scholar |

Cao J, Jiang W, Zhao Y (2007) ‘Experimental guidance on postharvest physiology and biochemistry of fruits and vegetables’. (China Light Industry Press: Beijing)

Castle SC, Morrison CD, Barger NN (2011) Extraction of chlorophyll a from biological soil crusts: a comparison of solvents for spectrophotometric determination. Soil Biology and Biochemistry 43, 853–856.
Extraction of chlorophyll a from biological soil crusts: a comparison of solvents for spectrophotometric determination.Crossref | GoogleScholarGoogle Scholar |

Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6, 71–80.
Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid.Crossref | GoogleScholarGoogle Scholar |

Chen JL, Shi SL, Juan QI (2016) Effect of combined application of phosphate and microbial fertilizer on soil microbial quantity and soil enzyme activity in alpine region. Grassland & Turf 36, 7–13.

Chen X, Jin Y, Ou B, Zhong J, Lin F, Wu H (2017) Analysis of soil microbial functional diversity of different understory planting dictyophora land based on Biolog-ECO technology. Genomics and Applied Biology 1, 370–375.

Choi K-H, Dobbs FC (1999) Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. Journal of Microbiological Methods 36, 203–213.
Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities.Crossref | GoogleScholarGoogle Scholar | 10379806PubMed |

Classen AT, Boyle SI, Haskins KE, Overby ST, Hart SC (2003) Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils. FEMS Microbiology Ecology 44, 319–328.
Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils.Crossref | GoogleScholarGoogle Scholar | 19719613PubMed |

Dobranic JK, Zak JC (1999) A microtiter plate procedure for evaluating fungal functional diversity. Mycologia 91, 756–765.
A microtiter plate procedure for evaluating fungal functional diversity.Crossref | GoogleScholarGoogle Scholar |

Egamberdiyeva D, Renella G, Landi L, Mench M, Nannipieri P (2005) Soil protease activity during decomposition of model root exudates released by a model root surface in Cd contaminated soil. FEBS Journal 272, 153

Erper I, Agustí-Brisach C, Tunali B, Armengol J (2013) Characterization of root rot disease of kiwifruit in the Black Sea region of Turkey. European Journal of Plant Pathology 136, 291–300.
Characterization of root rot disease of kiwifruit in the Black Sea region of Turkey.Crossref | GoogleScholarGoogle Scholar |

Fangfang F, Jingsong W, Erwei D, Jiao X, Yuchuan D, Anlian W, et al. (2015) Effect of sorghum continuous cropping on soil microbial community functional diversity. Journal of Shanxi Agricultural Sciences 43, 847–853.

Fu Q, Gu J, Li Y, Qian X, Sun W, Wang X, et al. (2015) Analyses of microbial biomass and community diversity in kiwifruit orchard soils of different planting ages. Acta Ecologica Sinica 35, 22–28.
Analyses of microbial biomass and community diversity in kiwifruit orchard soils of different planting ages.Crossref | GoogleScholarGoogle Scholar |

Fusuo RWWJZ, Jianbo S (1999) The application of rhizosphere micro-ecosystem theory to continuous cropping problem. Review of China Agricultural Science and Technology 4, 014

Gao F, You CH, Liu CK, Zhang T, Tang SK, Li GU, et al. (2014) Effect of a microbial agent on rhizospheric microecology and economic traits of flue-cured tobaccos. Fujian Journal of Agricultural Sciences 48, 331–345.

Gao J (2006) ‘Plant physiology experiment guide’. (Higher Education Press)

Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Applied and Environmental Microbiology 57, 2351–2359.
Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization.Crossref | GoogleScholarGoogle Scholar | 16348543PubMed |

Ge Z, Du H, Gao Y, Qiu W (2018) Analysis on metabolic functions of stored rice microbial communities by BIOLOG ECO microplates. Frontiers in Microbiology 9, 1375
Analysis on metabolic functions of stored rice microbial communities by BIOLOG ECO microplates.Crossref | GoogleScholarGoogle Scholar | 30018600PubMed |

Guan S (1986). ‘Soil enzymes and their research methods’. (Agricultural Publishing House)

Hamza A, Mohamed A, Hamed S (2016) New trends for biological and non-biological control of tomato root rot, caused by Fusarium solani, under greenhouse conditions. Egyptian Journal of Biological Pest Control 26, 89–96.

Hao YJ, Wei J, Liu CY, Wang Y, Wang WL (2009) Effects of biological soil amendment on defense enzyme activity and phenolic compound of cucumber continuous cropping. Acta Phytopathologica Sinica 39, 444–448.

Hu K, Li H-X, Lu W-S, Liu Y-J, Wang L-B (2010) Effect of microbial organic fertilizer application on soil microbial activity. Chinese Journal of Eco-Agriculture 18, 303–306.
Effect of microbial organic fertilizer application on soil microbial activity.Crossref | GoogleScholarGoogle Scholar |

Huang J, Li Z, Zhang J (2012) Improvement of indophenol blue colorimetric method on activity of urease in soil. Journal of Civil Architectural & Environmental Engineering 34, 102–107.

Krausz JP, Caldwell JD (1987) Cylindrocladium root rot of kiwifruit. Plant Disease 71, 374–375.
Cylindrocladium root rot of kiwifruit.Crossref | GoogleScholarGoogle Scholar |

Kuşcu İSK (2015) Soil enzymes and characteristics. International Journal of Engineering Sciences & Research Technology 4, 34–38.

Ladd JN, Butler JHA (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biology and Biochemistry 4, 19–30.
Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates.Crossref | GoogleScholarGoogle Scholar |

Lago MCF, Castro J, Briones MJI, Gallego PP, Barreal ME (2015) Effect of agricultural management on kiwifruit nutritional plant status, fruit quality and yield. Acta Horticulturae 1096, 79–86.
Effect of agricultural management on kiwifruit nutritional plant status, fruit quality and yield.Crossref | GoogleScholarGoogle Scholar |

Latorre BA, Alvarez C, Ribeiro OK (1991) Phytophthora root rot of kiwifruit in Chile. Plant Disease 75, 949
Phytophthora root rot of kiwifruit in Chile.Crossref | GoogleScholarGoogle Scholar |

Lee KJ, Jung JS, Mo YM, Yoon YJ, Kim SI (2017) Isolation of antagonistic microbes for biological control of ginseng root rot. Planta Medica International Open 4,
Isolation of antagonistic microbes for biological control of ginseng root rot.Crossref | GoogleScholarGoogle Scholar |

Li F, Kong Q, Zhang Q, Wang H, Wang L, Luo T (2020) Spent mushroom substrates affect soil humus composition, microbial biomass and functional diversity in paddy fields. Applied Soil Ecology 149, 103489
Spent mushroom substrates affect soil humus composition, microbial biomass and functional diversity in paddy fields.Crossref | GoogleScholarGoogle Scholar |

Li S, Gu L, Liu K, Liao Z (2009) Effects of combined application of organic fertilizers on the control of soilborne diseases and the regulation of soil microbial diversity. Plant Nutrition & Fertilizer Science 965–969.

Li Z, Zheng L (2016) Soil sucrase: detection conditions based on DNS colorimetric. Chinese Agricultural Science Bulletin 32, 171–176.

Lloyd AB, Sheaffe MJ (1973) Urease activity in soils. Plant and Soil 39, 71–80.
Urease activity in soils.Crossref | GoogleScholarGoogle Scholar |

López-Aizpún M, Arango-Mora C, Santamaría C, Lasheras E, Santamaría JM, Ciganda VS, et al. (2018) Atmospheric ammonia concentration modulates soil enzyme and microbial activity in an oak forest affecting soil microbial biomass. Soil Biology and Biochemistry 116, 378–387.
Atmospheric ammonia concentration modulates soil enzyme and microbial activity in an oak forest affecting soil microbial biomass.Crossref | GoogleScholarGoogle Scholar |

Luo J, Zhao S, Yuan Y, Hu J, Shen Q (2011) Effects of a bio-organic fertilizer on the disease resistance-related enzymes activities of cotton. Journal of Nanjing Agricultural University 3, 89–93.

Luo Y, Tian G, Zhang D, Hao R, Wang C (2015) Effects of biological bacterial manure on soil nutrient and nitrate-N accumulation in greenhouse. Chinese Agricultural Science Bulletin 224–228.

Maciá‐Vicente JG, Rosso LC, Ciancio A, Jansson HB, Lopez‐Llorca LV (2009) Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: effects on plant growth and disease. Annals of Applied Biology 155, 391–401.
Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: effects on plant growth and disease.Crossref | GoogleScholarGoogle Scholar |

Narasimha G, Sridevi A, Reddy AVS, Banu MT, Reddy BR (2012) Effect of cotton ginning mill industrial effluents on soil dehydrogenase, phosphatase, amylase and invertase enzyme activities. International Journal of Agricultural and Food Science 2, 1–6.

Orland C, Emilson EJS, Basiliko N, et al. (2019) Microbiome functioning depends on individual and interactive effects of the environment and community structure. The ISME Journal 13, 1–11.
Microbiome functioning depends on individual and interactive effects of the environment and community structure.Crossref | GoogleScholarGoogle Scholar | 30042502PubMed |

Parkinson D, Gray TRG, Williams ST (1971) ‘Methods for studying the ecology of soil micro-organisms’. (Blackwell Scientific Pub)

Peng QR (2015) An investigation into root rot causes of kiwi fruit and prevention technology. Times Agricultural Machinery 42, 154–155.

Qian X, Gu J, Sun W, et al. (2014) Changes in the soil nutrient levels, enzyme activities, microbial community function, and structure during apple orchard maturation. Applied Soil Ecology 77, 18–25.
Changes in the soil nutrient levels, enzyme activities, microbial community function, and structure during apple orchard maturation.Crossref | GoogleScholarGoogle Scholar |

Richardson DP, Ansell J, Drummond LN (2018) The nutritional and health attributes of kiwifruit: a review. European Journal of Nutrition 57, 2659–2676.
The nutritional and health attributes of kiwifruit: a review.Crossref | GoogleScholarGoogle Scholar | 29470689PubMed |

Rogers BF, Tate Iii RL (2001) Temporal analysis of the soil microbial community along a toposequence in Pineland soils. Soil Biology and Biochemistry 33, 1389–1401.
Temporal analysis of the soil microbial community along a toposequence in Pineland soils.Crossref | GoogleScholarGoogle Scholar |

Shan D, Jingli HE, Xing E, Rong H, Liu Y (2017) Effects of microbial fertilizer on microorganism and soil enzyme activity in coal mine dump of typical steppe. Bulletin of Soil & Water Conservation 37, 81–85.

Shao Y, Xu L, Song S, Qi K, Fu L, Cui Y (2015) Situation and development for kiwifruit grading in the A region of Shanxi Province. Journal of Agricultural Mechanization Research 2, 249–253.

Sharma M, Tarafdar A, Ghosh R, Gopalakrishanan S (2017) Biological control as a tool for eco-friendly management of plant pathogens. Advances in Soil Microbiology: Recent Trends and Future Prospects PP153–188.

Shimizu S, Yano T, Miyoshi T, Tachibana Y (2005) (93) First report of kiwifruit root rot caused by Pythium spp. (Abstracts of the papers presented at the 2005 annual meeting in Shizuoka). Annals of the Phytopathological Society of Japan 71, 210

Staddon W, Duchesne L, Trevors J (1997) Microbial diversity and community structure of postdisturbance forest soils as determined by sole-carbon-source utilization patterns. Microbial Ecology 34, 125–130.
Microbial diversity and community structure of postdisturbance forest soils as determined by sole-carbon-source utilization patterns.Crossref | GoogleScholarGoogle Scholar | 9230100PubMed |

Stefanowicz A (2006) The Biolog plates technique as a tool in ecological studies of microbial communities. Polish Journal of Environmental Studies 15, 669–676.

Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry 1, 301–307.
Use of p-nitrophenyl phosphate for assay of soil phosphatase activity.Crossref | GoogleScholarGoogle Scholar |

Tan ZZ, Lin J, Liu KX, Liao ZW (2007) Effects of complex microbial fertilizer on tomato bacterial wilt and soil microbial diversities. Journal of South China Agricultural University 2, 10–14.

Thomidis T, Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49–51.
Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit.Crossref | GoogleScholarGoogle Scholar |

Wang R-Y, Gao B, Li X-H, Ma J, Chen S-L (2014) First report of Fusarium solani causing Fusarium root rot and stem canker on storage roots of sweet potato in China. Plant Disease 98, 160
First report of Fusarium solani causing Fusarium root rot and stem canker on storage roots of sweet potato in China.Crossref | GoogleScholarGoogle Scholar | 30708580PubMed |

Wang Y, Pan F, Zhan X, Wang G, Zhang G, Yanli HU, et al. (2015) Effects of five kinds of phenolic acid on the function of mitochondria and antioxidant systems in roots of Malus hupehensis Rehd. seedlings. Acta Ecologica Sinica 35, 6566–6573.

Xie YY, Jie GU, Gao H, Zhang SQ, Xia X, Liu L, et al. (2010) Dynamic changes of soil enzyme activities in microorganism inoculants, enzymes and chemical fertilizers in different proportions after straw returning soil. Research of Soil & Water Conservation 17, 233–238.

Yan R, Wei Z, Qiqige W, Chen J, Dai J, Yao J, et al. (2017) Effect of combined microbial fertilizer on soil microorganism and enzyme activity in the Hulunber punching Leymus chinensis Meadow Steppe. Ecology & Environmental Sciences 4, 597–604.

Yang PY, Yao CC, Xiao-Ying LI, Dong H, Qiao JM (2014) Study on the growth and development regularity of ‘Xuxiang’ kiwifruit. Northern Horticulture 18, 47–50.

Yang R, Tang J, Chen X, Hu S (2007) Effects of coexisting plant species on soil microbes and soil enzymes in metal lead contaminated soils. Applied Soil Ecology 37, 240–246.
Effects of coexisting plant species on soil microbes and soil enzymes in metal lead contaminated soils.Crossref | GoogleScholarGoogle Scholar |

Yang Y, Yao J, Hua X (2000) Effect of pesticide pollution against functional microbial diversity in soil. Journal of Microbiology 20, 23–25.

Ying-Ying YU, Liang C, Zhao HH (2017) The pathogen causing bower kiwifruit Fusarium root rot. Mycosystema 36, 1369–1375.

Yonghwan L, Hyeongjin J, Kwanghong C, Sookjoo K, Kibeum P (2001) Occurrence of Phytophthora root rot on kiwifruit in Korea. Plant Pathology Journal 17, 154–158.

Yuan S, Li M, Fang Z, et al. (2016) Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae. Biological Control Theory & Application in Pest Management 92, 164–171.
Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae.Crossref | GoogleScholarGoogle Scholar |

Zhang Q-M, Lin M, Zhou X-T (2006) Application of biofertilizer in ecological remediation of polluted soil. Journal of Agro-Environment Science 283–284,

Zhang WW, Jun XU, Dong FS, Liu XG, Xiang WS, Zheng YQ, et al. (2014) Responses of microbial community functional diversity to bensulfuron-methyl in paddy soil. Journal of Agro-Environment Science 33, 1749–1754.

Zhu D, Zhang L, Wei Z, Liu X, Zhou Z, Dai X, et al. (2014) Effects of bacterial manure on soil physicochemical properties and microbial community diversity in rhizosphere of highland barley. Acta Pedologica Sinica 3, 627–637.

Zhuang QG, Wen XG, Wang LH, Jian-Hua LI, Gan TJ, Ming-Zhang LI (2015) Field trials of 4 pesticides to Hongyang kiwifruit root rot disease. Resource Development & Market 4, 387–389.