Changes in fungal community and diversity in strawberry rhizosphere soil after 12 years in the greenhouse

doi:10.1016/S2095-3119(18)62003-9

摘要/Abstract

Abstract:

Soil fungi play a very important role in the soil ecological environment. In agricultural production, long-term monoculture and continuous cropping lead to changes in fungal community diversity. However, the effects of long-term monoculture and continuous cropping on strawberry plant health and fungal community diversity have not been elucidated. In this study, using high-throughput sequencing (HTS), we compared the fungal community and diversity of strawberry rhizosphere soil after various durations of continuous cropping (0, 2, 4, 6, 8, 10 and 12 years). The results showed that soil fungal diversity increased with consecutive cropping years. Specifically, the soil-borne disease pathogens Fusarium and Guehomyces were significantly increased after strawberry continuous cropping, and the abundance of nematicidal (Arthrobotrys) fungi decreased from the fourth year of continuous cropping. The results of correlation analysis suggest that these three genera might be key fungi that contribute to the changes in soil properties that occur during continuous cropping. In addition, physicochemical property analysis showed that the soil nutrient content began to decline after the fourth year of continuous cropping. Spearman’s correlation analysis showed that soil pH, available potassium (AK) and ammonium nitrogen (NH4+-N) were the most important edaphic factors leading to contrasting beneficial and pathogenic associations across consecutive strawberry cropping systems.

Key words: fungal community , soil-borne disease , replanted , strawberry rhizosphere soil , agricultural soil ecology

. [J]. Journal of Integrative Agriculture, 2019, 18(3): 677-687.

LI Wei-hua, LIU Qi-zhi. Changes in fungal community and diversity in strawberry rhizosphere soil after 12 years in the greenhouse[J]. Journal of Integrative Agriculture, 2019, 18(3): 677-687.

参考文献

Alloway B J. 1995. Heavy metals in soils. Environmental Pollution, 90, 1318–1324.
Amato K R, Yeoman C J, Kent A, Righini N, Carbonero F, Estrada A, Gaskins H R, Stumpf R M, Yildirim S, Torralba M, Gillis M, Wilson B A, Nelson K E, White B A, Leigh S R. 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME Journal, 7, 1344–1353.
Bai L, Cui J, Jie W, Cai B. 2015. Analysis of the community compositions of rhizosphere fungi in soybeans continuous cropping fields. Microbiological Research, 180, 49–56.
Baroncelli R, Zapparata A, Sarrocco S, Sukno S A, Lane C R, Thon M R, Vannacci G, Holub E, Sreenivasaprasad S. 2015. Molecular diversity of anthracnose pathogen populations associated with UK strawberry production suggests multiple introductions of three different Colletotrichum species. PLoS ONE, 10, 1371–1392.
Berendsen R L, Pieterse C M J, Bakker P A H M. 2012. The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478–486.
Braun P G, Sutton J C. 1988. Infection cycles and population dynamics of Botrytis cinerea in strawberry leaves. Canadian Journal of Plant Pathology, 10, 133–141.
Bron P A, van Baarlen P, Kleerebezem M. 2012. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nature Reviews Microbiology, 10, 66–90.
Campell R N, Schweers V H, Hall D H. 1982. Corky root of tomato in California caused by Pyrenochaeta lycopersici and control by soil fumigation. Plant Disease, 66, 657–661.
Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal, 6, 1621–1624.
Chu H, Grogan P. 2010. Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape. Plant and Soil, 329, 411–420.
Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B. 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environmental Microbiology, 10, 1–9.
Frey S D, Knorr M, Parrent J L, Simpson R T. 2004. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecology and Management, 196, 159–171.
Fuentes M, Govaerts B, De Leon F, Hidalgo C, Dendooven L, Sayre K D, Etchevers J. 2009. Fourteen years of applying zero and conventional tillage, crop rotation and residue management systems and its effect on physical and chemical soil quality. European Journal of Agronomy, 30, 228–237.
Gálvez L, Urbaniak M, Wa?kiewicz A, St?pień A, Palmero D. 2017. Fusarium proliferatum - Causal agent of garlic bulb rot in Spain: Genetic variability and mycotoxin production. Food Microbiology, 67, 41–48.
Geisseler D, Horwath W R, Joergensen R G, Ludwig B. 2010. Pathways of nitrogen utilization by soil microorganisms - A review. Soil Biology and Biochemistry, 42, 2058–2067.
Gullino M L, Minuto A, Gilardi G, Garibaldi A, Ajwa H, Duafala T. 2002. Efficacy of preplant soil fumigation with chloropicrin for tomato production in Italy. Crop Protection, 21, 741–749.
Guo C, Li L, Huang J, Liu J, Yang Z, Wei F, Liu J. 2015. Effects of cotton straw incorporation on soil microbial biomass carbon, nitrogen and phosphorus in long-term continuous cropping cotton field. Journal of Agricultural Resources and Environment, 32, 296–304.
Han W, Kemmitt S J, Brookes P C. 2007. Soil microbial biomass and activity in Chinese tea gardens of varying stand age and productivity. Soil Biology and Biochemistry, 39, 1468–1478.
Harris D C. 1990. Control of verticillium wilt and other soil-borne diseases of strawberry in Britain by chemical soil disinfestation. Journal of Horticultural Science, 65, 401–408.
He J Z, Xu Z H, Hughes J. 2005. Analyses of soil fungal communities in adjacent natural forest and hoop pine plantation ecosystems of subtropical Australia using molecular approaches based on 18S rRNA genes. FEMS Microbiology Letters, 247, 91–100.
Henry P M, Kirkpatrick S C, Islas C M, Pastrana A M, Yoshisato J, Koike S T, Daugovish O, Gordon T. 2016. The population of Fusarium oxysporum f. sp. fragariae, cause of Fusarium wilt of strawberry, in California. Plant Disease, 101, 550–556.
Hoitink H, Boehm M J. 1999. Biocontrol within the context of soil microbial communities: A substrate-dependent phenomenon. Annual Review of Phytopathology, 37, 427–446.
Huang L, Song L, Xia X, Mao W, Shi K, Zhou Y, Yu J. 2013. Plant-soil feedbacks and soil sickness: From mechanisms to application in agriculture. Journal of Chemical Ecology, 39, 232–242.
Karimian N, Johnston S G, Burton E D. 2017. Effect of cyclic redox oscillations on water quality in freshwater acid sulfate soil wetlands. Science of the Total Environment, 581, 314–327.
Li S, Li H, Yang C, Wang Y, Xue H, Niu Y. 2016. Rates of soil acidification in tea plantations and possible causes. Agriculture Ecosystems and Environment, 233, 60–66.
Li X, Lewis E E, Liu Q, Li H, Bai C, Wang Y. 2016. Effects of long-term continuous cropping on soil nematode community and soil condition associated with replant problem in strawberry habitat. Scientific Reports, 6, 30466–30478.
Ling N, Deng K, Song Y, Wu Y, Zhao J, Raza W, Huang Q, Shen Q. 2014. Variation of rhizosphere bacterial community in watermelon continuous mono-cropping soil by long-term application of a novel bioorganic fertilizer. Microbiological Research, 169, 570–578.
Liu W, Wang Q, Wang B, Wang X, Franks A E, Teng Y, Li Z, Luo Y. 2015. Changes in the abundance and structure of bacterial communities under long-term fertilization treatments in a peanut monocropping system. Plant and Soil, 395, 415–427.
McTee M R, Lekberg Y, Bullington L, Rummel A, Mummey D L, Ramsey P W, Hinman N W. 2017. Restoring ecological properties of acidic soils contaminated with elemental sulfur. The Science of the Total Environment, 587–588, 449–456.
Maas J L. 1984. Compendium of strawberry diseases. Mycologia, 77, 179.
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal, 17, 200.
Mendes R, Garbeva P, Raaijmakers J M. 2013. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37, 634–663.
Mendes R, Kruijt M, De B I, Dekkers E, Van D V M, Schneider J H, Piceno Y M, Desantis T Z, Andersen G L, Bakker P A. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332, 1097.
Meyer W B, Turner B L I. 1992. Human population growth and global land-use/cover change. Annual Review of Ecology & Systematics, 23, 39–61.
Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson B P, Kukwa M, Lucking R, Hestmark G, Garcia Otalora M, Rauhut A, Buedel B, Scheidegger C, Timdal E, Stenroos S, Brodo I, Perlmutter G B, Ertz D, et al. 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia, 98, 1088–1103.
Nallanchakravarthula S, Mahmood S, Alström S, Finlay R D. 2014. Influence of soil type, cultivar and Verticillium dahliae on the structure of the root and rhizosphere soil fungal microbiome of strawberry. PLoS ONE, 9, e111455.
Nannipieri P, Ascher J, Ceccherini M T, Landi L, Pietramellara G, Renella G. 2003. Microbial diversity and soil functions. European Journal of Soil Science, 54, 655–670.
Nelson D W, Sommers L E, Sparks D L, Page A L, Helmke P A, Loeppert R H, Soltanpour P N, Tabatabai M A, Johnston C T, Sumner M E. 1996. Total carbon, organic carbon, and organic matter. Methods of Soil Analysis, 9, 961–1010.
Okayama K, Nakano T, Matsutani S, Sugimura T. 2009. A simple and reliable method for evaluating the effectiveness of fungicides for control of powdery mildew (Sphaerotheca macularis) on Strawberry. Japanese Journal of Phytopathology, 61, 536–540.
Olaru L, Olaru N, Popa V I. 2004. On enzymatic degradation of cellulose acetate. Iranian Polymer Journal, 13, 235–240.
De Oliveira V M, Manfio G P, Coutinho H, Keijzer-Wolters A C, van Elsas J D. 2006. A ribosomal RNA gene intergenic spacer based PCR and DGGE fingerprinting method for the analysis of specific rhizobial communities in soil. Journal of Microbiological Methods, 64, 366–379.
Page A L, Miller R H, Keeney D R. 1982. Chemical and Microbiological Properties. American Society of Agronomy: Soil Science Society of America, Madison.
Puls J, Altaner C, Saake B. 2004. Degradation and modification of cellulose acetates by biological systems. Macromolecular Symposia, 208, 239–253.
Puls J, Wilson S A, Hölter D. 2011. Degradation of cellulose acetate-based materials: A review. Journal of Polymers and the Environment, 19, 152–165.
Pešakovi? M, Karaklaji?-Staji? ?, Milenkovi? S, Mitrovi? O. 2013. Biofertilizer affecting yield related characteristics of strawberry (Fragaria×ananassa Duch.) and soil microorganisms. Scientia Horticulturae, 150, 238–243.
Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q, 2012. Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biology and Fertility of Soils, 48, 807–816.
Redman R S, Freeman S, Clifton D R, Morrel J, Brown G, Rodriguez R J. 1999. Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna. Plant Physiology, 119, 795–804.
Romanowicz K J, Freedman Z B, Upchurch R A, Argiroff W A, Zak D R. 2016. Active microorganisms in forest soils differ from the total community yet are shaped by the same environmental factors: the influence of pH and soil moisture. FEMS Microbiology Ecology, 92, fiw149.
Smith F B. 2010. Soil science society of America. Journal of Geology, 5, 176.
Smith S E, Jakobsen I, Gronlund M, Smith F A. 2011. Roles of Arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology, 156, 1050–1057.
Song T, Xu Z, Chen Y, Ding Q, Sun Y, Miao Y, Zhang K, Niu X. 2017. Potent nematicidal activity and new hybrid metabolite production by disruption of a cytochrome P450 gene Involved in the biosynthesis of morphological regulatory arthrosporols in nematode-trapping fungus Arthrobotrys oligospora. Journal of Agricultural and Food Chemistry, 65, 4111–4120.
Su H G. 2012. The improvement measures of soil acidification in tea garden in Anxi. Guangdong Tea, Z1, 31–32. (in Chinese)
Sláviková E, Kosíková B, Mikulásová M. 2002. Biotransformation of waste lignin products by the soil-inhabiting yeast Trichosporon pullulans. Canadian Journal of Microbiology, 48, 200.
Tang C, Weligama C, Sale P. 2013. Subsurface Soil Acidification in Farming Systems: Its Possible Causes and Management Options. Molecular Environmental Soil Science. Springer Netherlands, Berlin. pp. 389–412.
Van Bruggen A, Semenov A M. 2000. In search of biological indicators for soil health and disease suppression. Applied Soil Ecology, 15, 13–24.
Wang M, Wu C, Cheng Z, Meng H, Zhang M, Zhang H. 2014. Soil chemical property changes in eggplant/garlic relay intercropping systems under continuous cropping. PLoS ONE, 9, 0111040.
Wang Y, Luo C, Li J, Yin H, Zhang G. 2014. Influence of plants on the distribution and composition of PBDEs in soils of an e-waste dismantling area: Evidence of the effect of the rhizosphere and selective bioaccumulation. Environmental Pollution, 186, 104–109.
Wolters V. 2000. Invertebrate control of soil organic matter stability. Biology and Fertility of Soils, 31, 1–19.
Xie X, Pu L, Wang Q, Zhu M, Xu Y, Zhang M. 2017. Response of soil physicochemical properties and enzyme activities to long-term reclamation of coastal saline soil, Eastern China. The Science of the Total Environment, 607–608, 1419–1427.
Xiong W, Zhao Q, Zhao J, Xun W, Li R, Zhang R, Wu H, Shen Q. 2015. Different continuous cropping spans significantly affect microbial community membership and structure in a Vanilla-grown soil as revealed by deep pyrosequencing. Microbial Ecology, 70, 209–218.
Yang J, Ruegger P M, McKenry M V, Becker J O, Borneman J. 2012. Correlations between root-associated microorganisms and peach replant disease symptoms in a California soil. PLoS ONE, 7, 0046420.
Yin C, Jones K L, Peterson D E, Garrett K A, Hulbert S H, Paulitz T C. 2010. Members of soil bacterial communities sensitive to tillage and crop rotation. Soil Biology and Biochemistry, 42, 2111–2118.
Zelles L, Bai Q Y, Beck T, Beese F. 1992. Signature fatty acids in phospholioids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biology and Biochemistry, 24, 317–323.
Zelles L, Rackwitz R, Bai Q Y, Beck T, Beese F. 1995. Discrimination of microbial diversity by fatty-acid profiles of phospholipids and lipopolysaccharides in differently cultivated soils. Plant and Soil, 170, 115–122.
Zhou X, Wu F. 2012. Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiology Ecology, 80, 469–478.
Zhou Y, Zhao Z Q, Guo Q Y, Lei B. 2017. First report of wilt of sugar beet caused by Gibellulopsis nigrescens in the Xinjiang region of China. Plant Disease, 101, 1318–1319.