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Journal of Integrative Agriculture  2020, Vol. 19 Issue (9): 2265-2273    DOI: 10.1016/S2095-3119(20)63186-0
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Effects of different rotation patterns on the occurrence of clubroot disease and diversity of rhizosphere microbes
YANG Xiao-xiang1, 2, HUANG Xiao-qin1, 2, WU Wen-xian1, XIANG Yun-jia1, DU Lei1, ZHANG Lei1, 2, LIU Yong1, 2 
1 Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, P.R.China
2 Key Laboratory of Integrated Pest Management on Crops in Southwest, Ministry of Agriculture and Rural Affairs, Chengdu 610066, P.R.China
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Clubroot disease, caused by Plasmodiophora brassicae, is one of the most destructive soil-borne diseases in cruciferous crops worldwide.  New strategies are urgently needed to control this disease, as no effective disease-resistant varieties or chemical control agents exist.  Previously, we found that the incidence rate and disease index of clubroot in oilseed rape decreased by 50 and 40%, respectively, when oilseed rape was planted after soybean.  In order to understand how different rotation patterns affect the occurrence of clubroot in oilseed rape, high-throughput sequencing was used to analyze the rhizosphere microbial community of oilseed rape planted after leguminous (soybean, clover), gramineous (rice, maize) and cruciferous (oilseed rape, Chinese cabbage) crops.  Results showed that planting soybeans before oilseed rape significantly increased the population density of microbes that could inhibit P. brassicae (e.g., Sphingomonas, Bacillus, Streptomyces and Trichoderma).  Conversely, consecutive cultivation of cruciferous crops significantly accumulated plant pathogens, including P. brassicae, Olpidium and Colletotrichum (P<0.05).  These results will help to develop the most effective rotation pattern for reducing clubroot damage.
Keywords:  oilseed rape        clubroot        Gramineae        Leguminosae        Cruciferae        rhizosphere soil  
Received: 15 October 2019   Accepted:
Fund: This work was supported by the National Key Research and Development Program of China (2017YFD0200600), the Financial Innovation Capacity Enhancement Project in Sichuan Province, China (2019QNJJ-011), and the National Modern Agricultural Industry Technology System of Sichuan Rape Innovation Team, China (2019–2023).
Corresponding Authors:  Correspondence ZHANG Lei, Tel/Fax: +86-28-84504089, E-mail:; LIU Yong, Tel/Fax: +86-28-84504089, E-mail:   
About author:  YANG Xiao-xiang, E-mail:;

Cite this article: 

YANG Xiao-xiang, HUANG Xiao-qin, WU Wen-xian, XIANG Yun-jia, DU Lei, ZHANG Lei, LIU Yong. 2020. Effects of different rotation patterns on the occurrence of clubroot disease and diversity of rhizosphere microbes. Journal of Integrative Agriculture, 19(9): 2265-2273.

Bais H P, Weir T L, Perry L G, Gilroy S, Vivanco J M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233–266.
Bona E, Lingua G, Manassero P, Cantamessa S, Marsano F, Todeschini V, Copetta A, Agostino G D, Massa N, Avidano L, Gamalero E, Berta G. 2015. AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels. Mycorrhiza, 25, 181–193.
Chai A L, Xie X W, Shi Y X, Li B J. 2010. Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Canadian Journal of Plant Pathology, 32, 43–57.
Cheah L H, Veerakone S, Kent G. 2000. Biological control of clubroot on cauliflower with Trichoderma and Streptomyces spp. New Zealand Plant Protection, 53, 18–21.
Chen T, Bi K, He Z C, Gao Z X, Zhao Y, Fu Y P, Cheng J S, Xie J T, Jiang D H. 2016. Arabidopsis mutant bik1 exhibits strong resistance to Plasmodiophora brassicae. Frontiers in Physiology, 7, 402.
Cui E P, Fan X Y, Li Z Y, Liu Y, Neal A L, Hu C, Gao F. 2019. Variations in soil and plant-microbiome composition with different quality irrigation waters and biochar supplementation. Applied Soil Ecology, 142, 99–109.
Dixon G R. 2009. The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation, 28, 194–202.
Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998.
Enya J, Shinohara H, Yoshida S, Tsukiboshi T, Negishi H, Suyama K. 2007. Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microbial Ecology, 53, 524–536.
Friberg H, Lagerlöf J, Rämert B. 2006. Usefulness of nonhost plants in managing Plasmodiophora brassicae. Plant Pathology, 55, 690–695.
He P J, Cui W Y, Munir S, He P F, Li X Y, Wu Y X, Yang X W, Tang P, He Y Q. 2019. Plasmodiophora brassicae root hair interaction and control by Bacillus subtilis XF-1 in Chinese cabbage. Biological Control, 128, 56–63.
Hwang S F, Strelkov S E, Feng J, Gossen B D, Howard R J. 2012. Plasmodiophora brassicae: A review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Molecular Plant Pathology, 13, 105–113.
Innerebner G, Knief C, Vorholt J A. 2011. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Applied and Environmental Microbiology, 77, 3202–3210.
Jian L, Li M, Gao X X, Fang F. 2018. Corn straw mulching affects Parthenium hysterophorus and rhizosphere organisms. Crop Protection, 113, 90–96.
Jin R D, Han T H, Kim Y W, Kim K Y. 2006. Suppression of clubroot formation in Chinese cabbage by the chitin compost and broth. Journal of Applied Biological Chemistry, 49, 171–175.
Kageyama K, Asano T. 2009. Life cycle of Plasmodiophora brassicae. Journal of Plant Growth Regulation, 28, 203–211.
Kowata-Dresch L S, May-De Mio L L. 2012. Clubroot management of highly infested soils. Crop Protection, 35, 47–52.
Li J P, Li Y, Shi Y X, Xie X W, Chai A L. 2013. Development of a real-time PCR assay for Plasmodiophora brassicae and its detection in soil samples. Journal of Integrative Agriculture, 12, 1799–1806.
Li W H, Liu Q Z. 2019. Changes in fungal community and diversity in strawberry rhizosphere soil after 12 years in the greenhouse. Journal of Integrative Agriculture, 18, 677–687.
Lu L H, Yin S X, Liu X, Zhang W M, Gu T H, Shen Q R, Qiu H Z. 2013. Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biology & Biochemistry, 65, 186–194.
Luo J Y, Zhang S, Zhu X Z, Lu L M, Wang C Y, Li C H, Cui J J, Zhou Z Q. 2017. Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields. Journal of Integrative Agriculture, 16, 1624–1633.
Magoc T, Salzberg S L. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27, 2957–2963.
Murakami H, Tsushima S, Kuroyanagi Y, Shishido Y. 2002. Reduction of resting spore density of Plasmodiophora brassicae and clubroot disease severity by liming. Soil Science and Plant Nutrition, 48, 685–691.
Nehl D B, Allen S J, Brown J F. 1996. Deleterious rhizosphere bacteria: An integrating perspective. Applied Soil Ecology, 5, 1–20.
Shakeel Q, Lyu A, Zhang J, Wu M D, Chen S W, Chen W D, Li G Q, Yang L. 2016. Optimization of the cultural medium and conditions for production of antifungal substances by Streptomyces platensis 3–10 and evaluation of its efficacy in suppression of clubroot disease (Plasmodiophora brassicae) of oilseed rape. Biological Control, 101, 59–68.
Wachowska U, Irzykowski W, J?dryczka M, G?owacka K. 2013. Biological control of winter wheat pathogens with the use of antagonistic Sphingomonas bacteria under greenhouse conditions. Biocontrol Science and Technology, 23, 1110–1122.
Wagner M R, Lundberg D S, Coleman-Derr D, Tringe S G, Dangl J L, Mitchell-Olds T. 2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecology Letters, 17, 717–726.
Zhang Y, Ruyter-Spira C, Bouwmeester H J. 2015. Engineering the plant rhizosphere. Current Opinion in Biotechnology, 32, 136–142.
Zhao Y, Gao Z X, Tian B N, Bi K, Chen T, Liu H Q, Xie J T, Cheng J S, Fu Y P, Jiang D H. 2017. Endosphere microbiome comparison between symptomatic and asymptomatic roots of Brassica napus infected with Plasmodiophora brassicae. PLoS ONE, 12, e0185907.
Zhou N, Liu P, Wang Z Y, Xu G D. 2011. The effects of rapeseed root exudates on the forms of aluminum in aluminum stressed rhizosphere soil. Crop Protection, 30, 631–636.
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