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Journal of Integrative Agriculture  2016, Vol. 15 Issue (9): 2049-2058    DOI: 10.1016/S2095-3119(16)61354-0
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Identification of candidate soil microbes responsible for small-scale heterogeneity in strawberry plant vigour
WEI Feng1, 2*, FAN Rong1, 2*, Thomas Passey2, HU Xiao-ping1, Xiangming Xu2
1 State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling 712100, P.R.China
2 NIAB East Malling Research, East Malling, Kent, ME19 6BJ, UK
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Abstract      Studies were conducted to identify candidate soil microbes responsible for observed differences in strawberry vigour at a small spatial scale, which was not associated with visual disease symptoms. Samples were obtained from the soils close to the rhizosphere of ‘big’ and ‘small’ plants from small plots which exhibited large local heterogeneity in plant vigour. A metabarcoding approach was used to profile bacterial and fungal compositions, using two primer pairs for 16S ribosomal RNA genes (16S rDNA) and one for the fungal internal transcribed spacer (ITS) region. Of the two 16S rDNA primer sets, the 341F/805R resulted in sequences of better quality. A total 28 operational taxonomic units (OTUs) had differential relative abundance between samples from ‘big’ and ‘small’ plants. However, plausible biological explanation was only possible for three fungal OTUs. Two were possible phytopathogens: Verticillium spp. and Alternaria alternata although the latter has never been considered as a main pathogen of strawberry in the UK. For samples from ‘small’ plants, the abundance of these OTUs was much greater than from ‘big’ plants. The opposite was true for a mycorrhizal OTU. These results suggest that soil microbes related to crop production can be identified using metabarcoding technique. Further research is needed to assess whether A. alternata and Verticillium spp. could affect strawberry growth in the field.
Keywords:  soil microbes        plant health       soilborne pathogens        mycorrhizal fungi        metabarcoding  
Received: 18 December 2015   Accepted:
Fund: 

This research is funded by Innovate UK (100867) with matching funding from several commercial companies. Wei Feng and Fan Rong gratefully acknowledge the financial assistance of the China Scholarship Council (201306300133 and 201506300012).

Corresponding Authors:  HU Xiao-ping, Tel/Fax: +86-29-87091095, E-mail: xphu@nwsuaf.edu.cn; Xiangming Xu, Tel: +44-1732-523753, Fax: +44-1732-849067, E-mail: xiangming.xu@emr.ac.uk    
About author:  WEI Feng, E-mail: weifeng0108@163.com;

Cite this article: 

WEI Feng, FAN Rong, Thomas Passey, HU Xiao-ping, Xiangming Xu. 2016. Identification of candidate soil microbes responsible for small-scale heterogeneity in strawberry plant vigour. Journal of Integrative Agriculture, 15(9): 2049-2058.

Abarenkov K, Henrik Nilsson R, Larsson K H, Alexander I J, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor A F S, Tedersoo L, Ursing B M, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U. 2010. The UNITE database for molecular identification of fungi - Recent updates and future perspectives. New Phytologist, 186, 281–285.

Benjamin L R, Aikman D P. 1995. Predicting growth in stands of mixed species from that in individual species. Annals of Botany, 76, 31–41.

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.

Botha A, Denman S, Lamprecht S C, Mazzola M, Crous P W. 2003. Characterisation and pathogenicity of Rhizoctonia isolates associated with black root rot of strawberries in the Western Cape Province, South Africa. Australasian Plant Pathology, 32, 195–201.

Dangi S R, Gerik J S, Tirado-Corbalá R, Ajwa H. 2015. Soil microbial community structure and target organisms under different fumigation treatments. Applied and Environmental Soil Science, 2015. doi: 10.1155/2015/673264

Dixon P. 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14, 927–930.

Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998.

Fang X L, Phillips D, Li H, Sivasithamparam K, Barbetti M J. 2011. Severity of crown and root diseases of strawberry and associated fungal and oomycete pathogens in Western Australia. Australasian Plant Pathology, 40, 109–119.

Fan L, Dalpe Y, Fang C Q, Dube C, Khanizadeh S. 2011. Influence of arbuscular mycorrhizae on biomass and root morphology of selected strawberry cultivars under salt stress. Botany-Botanique, 89, 397–403.

Gans J, Wolinsky M, Dunbar J. 2005. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science, 309, 1387–1390.

Gardes M, Bruns T D. 1993. ITS primers with enhanced specificity for basidiomycetes - Application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

Gordon T R, Kirkpatrick S C, Hansen J, Shaw D V. 2006. Response of strawberry genotypes to inoculation with isolates of Verticillium dahliae differing in host origin. Plant Pathology, 55, 766–769.

Gurung S, Short D P G, Hu X, Sandoya G V, Hayes R J, Koike S T, Subbarao K V. 2015. Host range of Verticillium isaacii and Verticillium klebahnii from artichoke, spinach, and lettuce. Plant Disease, 99, 933–938.

Guzmán-Dávalos L, Mueller G M, Cifuentes J, Miller A N, Santerre A. 2003. Traditional infrageneric classification of Gymnopilus is not supported by ribosomal DNA sequence data. Mycologia, 95, 1204–1214.

Herlemann D P R, Labrenz M, Jurgens K, Bertilsson S, Waniek J J, Andersson A F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal, 5, 1571–1579.

IUSS Working Group of World Reference Base for Soil Resources. 2015. World Reference Base for Soil Resources 2014. International Soil Classification System for Naming Soils and Creating Legends for Soil Maps. Update 2015. World Soil Resources Reports No. 106. FAO, Rome.

Kent A D, Triplett E W. 2002. Microbial communities and their interactions in soil and rhizosphere ecosystems. Annual Reviews in Microbiology, 56, 211–236.

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner F O. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41, e1.

Ko Y, Chen C Y, Yao K S, Liu C W, Maruthasalam S, Lin C H. 2008. First report of fruit rot of strawberry caused by an Alternaria sp. in Taiwan. Plant Disease, 92, 1248–1248.

Koike S T, Kirkpatrick S C, Gordon T R. 2009. Fusarium wilt of strawberry caused by Fusarium oxysporum in California. Plant Disease, 93, 1077–1077.

Korthals G W, Thoden T C, van den Berg W, Visser J H M. 2014. Long-term effects of eight soil health treatments to control plant-parasitic nematodes and Verticillium dahliae in agro-ecosystems. Applied Soil Ecology, 76, 112–123.

Liu Z, Lozupone C, Hamady M, Bushman F D, Knight R. 2007. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Research, 35, e120.

Li Y, Yanagi A, Miyawaki Y, Okada T, Matsubara Y I. 2010. Disease tolerance and changes in antioxidative abilities in mycorrhizal strawberry plants. Journal of the Japanese Society for Horticultural Science, 79, 174–178.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Manici L M, Caputo F, Baruzzi G. 2005. Additional experiences to elucidate the microbial component of soil suppressiveness towards strawberry black root rot complex. Annals of Applied Biology, 146, 421–431.

Martin F N. 2003. Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annual Review of Phytopathology, 41, 325–350.

Mazzola M, Hewavitharana S S, Strauss S L. 2015. Brassica seed meal soil amendments transform the rhizosphere microbiome and improve apple production through resistance to pathogen reinfestation. Phytopathology, 105, 460–469.

McMurdie P J, Holmes S. 2014. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Computational Biology, 10, e1003531.

Mummey D L, Rillig M C. 2008. Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiology Ecology, 64, 260–270.

Muyzer G, de Waal E C, Uitterlinden A G. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology, 59, 695–700.

Nemec S. 1976. Response of three root rot fungi to strawberry phenolics and the relation of phenolics to disease resistance. Mycopathologia, 59, 37–40.

Omirou M, Rousidou C, Bekris F, Papadopoulou K K, Menkissoglou-Spiroudi U, Ehaliotis C, Karpouzas D G. 2011. The impact of biofumigation and chemical fumigation methods on the structure and function of the soil microbial community. Microbial Ecology, 61, 201–213.

Paulson J N, Stine O C, Bravo H C, Pop M. 2013. Differential abundance analysis for microbial marker-gene surveys. Nature Methods, 10, 1200–1202.

Pegg G F, Brady B L. 2002. Verticillium Wilts. CABI Publishing, New York.

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner F O. 2013. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590–D596.

Rillig M C. 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters, 7, 740–754.

Rillig M C, Mummey D L. 2006. Mycorrhizas and soil structure. New Phytologist, 171, 41–53.

Robinson-Boyer L R, Brain P, Xu X M, Jeffries P. 2015. Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: Effects on population dynamics of fungal species in roots and consequential plant tolerance to water deficiency. Mycorrhiza, 25, 215–227.

Shi Z Y, Liu D H, Wang F Y. 2013. Spatial variation of arbuscular mycorrhizal fungi in two vegetation types in Gurbantonggut Desert. Contemporary Problems of Ecology, 6, 455–464.

Tahmatsidou V, O’Sullivan J, Cassells A C, Voyiatzis D, Paroussi G. 2006. Comparison of AMF and PGPR inoculants for the suppression of Verticillium wilt of strawberry (Fragaria×ananassa cv. Selva). Applied Soil Ecology 32, 316–324.

Wada H, Cavanni P, Bugiani R, Kodama M, Otani H. 1996. Occurrence of the strawberry pathotype of Alternaria alternata in Italy. Plant Disease, 80, 372–374.

Wang Q, Ma Y, Yang H, Chang Z. 2014. Effect of biofumigation and chemical fumigation on soil microbial community structure and control of pepper Phytophthora blight. World Journal of Microbiology and Biotechnology, 30, 507–518.

Wei F, Passey T, Xu X. 2016a. Amplicon-based metabarcoding reveals temporal response of soil microbial community to fumigation-derived products. Applied Soil Ecology, 103, 83–92.

Wei F, Passey T, Xu X. 2016b. Effects of individual and combined use of bio-fumigation-derived products on the viability of Verticillium dahliae microsclerotia in soil. Crop Protection, 79, 170–176.

Werner J J, Zhou D, Caporaso J G, Knight R, Angenent L T. 2012. Comparison of Illumina paired-end and single-direction sequencing for microbial 16S rRNA gene amplicon surveys. The ISME Journal, 6, 1273–1276.

Xu X, Passey T, Wei F, Saville R, Harrison R J. 2015. Amplicon-based metagenomics identified candidate organisms in soils that caused yield decline in strawberry. Horticulture Research, 2, doi: 10.1038/hortres.2015.1022

Yang Y H, Yao J, Hu S, Qi Y. 2000. Effects of agricultural chemicals on DNA sequence diversity of soil microbial community: A study with RAPD marker. Microbial Ecology in Health and Disease, 39, 72–79.

Yohalem D, Passey T. 2011. Amendment of soils with fresh and post-extraction lavender (Lavandula angustifolia) and lavandin (Lavandula×intermedia) reduce inoculum of Verticillium dahliae and inhibit wilt in strawberry. Applied Soil Ecology, 49, 187–196.

Yuen G Y, Schroth M N, Weinhold A R, Hancock J G. 1991. Effects of soil fumigation with methyl bromide and chloropicrin on root health and yield of strawberry. Plant Disease, 75, 416–420.
[1] S L Strauss, D A Kluepfel. Anaerobic soil disinfestation: A chemical-independent approach to pre-plant control of plant pathogens[J]. >Journal of Integrative Agriculture, 2015, 14(11): 2309-2318.
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