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Illumina sequencing reveals a rhizosphere bacterial community associated with foxtail millet smut disease suppression

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Abstract

Background and aims

Smut disease is a severe limiting factor in foxtail millet production, caused by the Ustilago crameri fungus. The aim of this study is to characterize specific bacterial populations that might contribute to smut disease suppression.

Methods

Rhizosphere bacterial community compositions of three foxtail millet cultivars differing in smut disease resistance were compared using high throughput Illumina sequencing.

Results

As a disease-resistant cultivar, Jigu20 showed the lowest disease incidence (0.7 %) after Ustilago crameri inoculation, compared with 14.8 % and 62.5 % for Jingu21 and Changnong35, respectively. Under the Ustilago crameri-inoculation condition, higher bacterial diversity was present in the rhizosphere of Jigu20 (I.Ji20) than in other two soil samples (I.Jin21 and I.Chang35). The same trend was observed in enzyme activities of phosphatase, catalase, and polyphenol oxidase. Compared to I.Jin21 and I.Chang35, I.Ji20 harbored higher abundance of Actinobacteria, while lower abundance of Bacteroidetes and Firmicutes. At the genus level, the hierarchical cluster of I.Ji20 was clearly separated from I.Jin21 and I.Chang35. Pearson’s correlation analysis showed that the abundance of Bradyrhizobium and Streptomyces was negatively correlated with smut disease incidence (P < 0.05).

Conclusions

Different smut resistant cultivars occupied different rhizosphere bacterial communities, and smut disease suppression might be correlated with high bacterial diversity.

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References

  • Alkorta I, Aizpurua A, Riga P, Albizu I, Amezaga I, Garbisu C (2003) Soil enzyme activities as biological indicators of soil health. Rev Environ Health 18:65–73

    PubMed  Google Scholar 

  • An M, Zhou X, Wu F, Ma Y, Yang P (2011) Rhizosphere soil microorganism populations and community structures of different watermelon cultivars with differing resistance to Fusarium oxysporum f. sp. niveum. Can J Microbiol 57:355–365

    Article  CAS  PubMed  Google Scholar 

  • Anupama VN, Amrutha PN, Chitra GS, Krishnakumar B (2008) Phosphatase activity in anaerobic bioreactors for wastewater treatment. Water Res 42:2796–2802

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizoshpere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Borneman J, Becker JO (2007) Identifying microorganisms involved in specific pathogen suppression in soil. Annu Rev Phytopathol 45:153–172

    Article  CAS  PubMed  Google Scholar 

  • Chu H, Wang C, Wang H, Chen H, Tang M (2016) Pine wilt disease alters soil properties and root-associated fungal communities in Pinus tabulaeformis forest. Plant Soil 404:237–249

    Article  CAS  Google Scholar 

  • Dick WA, Cheng L, Wang P (2000) Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biol Biochem 32:1915–1919

    Article  CAS  Google Scholar 

  • Etebarian HR (2006) Evaluation of Streptomyces strains for biological control of charcoal stem rot of melon caused by Macrophomina phaseolina. Plant Pathol J 5:83–87

    Article  Google Scholar 

  • Garbeva P, Veen JA, Elsas JD (2004) Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes. FEMS Microbiol Ecol 47:51–64

    Article  CAS  PubMed  Google Scholar 

  • Gunasinghe WKRN, Karunaratne AM (2009) Interactions of Colletotrichum musae and Lsiodiplodia thebromae and their biocontrol by Pantoea agglomerans and Flavobacterium sp. in expression of crown rot of “Embul” banana. Biocontrol 54:587–596

    Article  Google Scholar 

  • Hwang BK, Ahn SJ, Moon SS (1994) Production, purification, and antifungal activity of the antibiotic nucleoside, tubercidin, produced by Streptomyces violaceoniger. Can J Bot 72:480–485

    Article  CAS  Google Scholar 

  • Kumar B (2011) First record of smut disease of foxtail millet caused by Ustilago crameri Korn. J Mycol Plant Pathol 41:459–461

    Google Scholar 

  • Liu R, Dai Y, Sun L (2015) Effect of rhizosphere enzymes on phytoremediation in PAH-contaminated soil using five plant species. PLoS ONE 10, e0120369

    Article  PubMed  PubMed Central  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • McSpadden Gardener BB, Weller DM (2001) Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Appl Environ Microbiol 67:4414–4425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mithöfer A, Bhagwat AA, Feger M, Ebel J (1996) Suppression of fungal β-glucan-induced plant defence in soybean (Glycine max L.) by cyclic 1,3-1,6-β-glucans from the symbiont Bradyrhizobium japonicum. Planta 199:270–275

    Article  Google Scholar 

  • Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusariumgraminearum and induced resistance. Plant Sci 162:491–498

    Article  CAS  Google Scholar 

  • Moline H, Hubbard JE, Karns JS, Buyer JS, Cohen JD (1999) Selective isolation of bacterial antagonists of Botrytis cinerea. Eur J Plant Pathol 105:95–101

    Article  Google Scholar 

  • Niu Q, Li P, Hao S et al (2015) Dynamic distribution of the gut microbiota and the relationship with apparent crude fiber digestibility and growth stages in pigs. Sci Rep 5:9938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omar SA, Abd-Alla MH (1998) Biocontrol of fungal root rot diseases of crop plants by the use of Rhizobia and Bradyrhizobia. Folia Microbiol 43:431–437

    Article  CAS  Google Scholar 

  • Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Biol Fertil Soils 48:807–816

    Article  CAS  Google Scholar 

  • Ros M, Pascual JA, Garcia C, Hernandez MT, Insam H (2006) Hydrolase activities, microbial biomass and bacterial community in a soil after long-term amendment with different composts. Soil Biol Biochem 38:3443–3452

    Article  CAS  Google Scholar 

  • Rosenzweig N, Tiedje JM, Quensen JFIII, Meng Q, Hao JJ (2012) Microbial communities associated with potato common scab-suppressive soil determined by pyrosequencing analyses. Plant Dis 96:718–725

    Article  Google Scholar 

  • Sanguin H, Sarniguet A, Gazengel K, Moënne-Loccoz Y, Grundmann GL (2009) Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol 184:694–707

    Article  CAS  PubMed  Google Scholar 

  • Schmidt J, Messmer M, Wilbois KP (2015) Beneficial microorganisms for soybean (Glycine max (L.) Merr), with a focus on low root-zone temperatures. Plant Soil 397:411–445

    Article  CAS  Google Scholar 

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781

    Article  PubMed  Google Scholar 

  • Shekhar N, Bhattacharya D, Kumar D, Gupta RK (2006) Biocontrol of wood-rotting fungi with Streptomyces violaceusniger XL-2. Can J Microbiol 52:805–808

    Article  CAS  PubMed  Google Scholar 

  • Shen Z, Wang D, Ruan Y, Xue C, Zhang J, Li R, Shen Q (2014) Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana fusarium wilt disease suppression induced by bio-organic fertilizer application. PLoS ONE 9, e98420

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen Z, Ruan Y, Xue C, Zhong S, Li R, Shen Q (2015) Soils naturally suppressive to banana Fusarium wilt disease harbor unique bacterial communities. Plant Soil 393:21–33

    Article  CAS  Google Scholar 

  • Shi ZJ, Lu Y, Xu ZG, Fu SL (2008) Enzyme activities of urban soils under different land use in the Shenzhen city, China. Plant Soil Environ 54:341–346

    CAS  Google Scholar 

  • Shi C, Wang C, Xu X, Huang B, Wu L, Yang D (2015) Comparison of bacterial communities in soil between nematode-infected and nematode-uninfected Pinus massoniana pinewood forest. Appl Soil Ecol 85:11–20

    Article  Google Scholar 

  • Siddiqui IA, Shaukat SS (2002) Mixtures of plant disease suppressive bacteria enhance biological control of multiple tomato pathogens. Biol Fertil Soils 36:260–268

    Article  Google Scholar 

  • Singh N, Somai BM, Pillay D (2004) Smut disease assessment by PCR and microscopy in inoculated tissue cultured sugarcane cultivars. Plant Sci 167:987–994

    Article  CAS  Google Scholar 

  • Sun J, Peng M, Wang Y, Li W, Xia Q (2013) The effects of different disease-resistant cultivars of banana on rhizosphere microbial communities and enzyme activities. FEMS Microbiol Lett 345:121–126

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Zhang Q, Zhou J, Wei Q (2014a) Pyrosequencing technology reveals the impact of different manure doses on the bacterial community in apple rhizosphere soil. Appl Soil Ecol 78:28–36

    Article  Google Scholar 

  • Sun J, Zhang Q, Zhou J, Wei Q (2014b) Illumina amplicon sequencing of 16S rRNA tag reveals bacterial community development in the rhizosphere of apple nurseries at a replant disease site and a new planting site. PLoS ONE 9, e111744

    Article  PubMed  PubMed Central  Google Scholar 

  • Trivedi P, He Z, Nostrand JDV, Albrigo G, Zhou J, Wang N (2012) Huanglongbing alters the structure and functional diversity of microbial communities associated with citrus rhizosphere. ISME J 6:363–383

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2013) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49:435–446

    Article  Google Scholar 

  • Weller D, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348

    Article  CAS  PubMed  Google Scholar 

  • Wu K, Yuan S, Wang L, Shi J, Zhao J, Shen B, Shen Q (2014) Effects of bio-organic fertilizer plus soil amendment on the control of tobacco bacterial wilt and composition of soil bacterial communities. Biol Fertil Soils 50:961–971

    Article  Google Scholar 

  • Wu F, Chen S, Chang C, An M, Zhou X, Xu W (2015) Rhizosphere soil microorganism populations and community structures of different watermelon cultivars with differing resistance to Fusarium oxysporum f. sp. Niveum inoculation. Pak J Bot 47:1535–1546

    CAS  Google Scholar 

  • Xu W, Wu F, Chang C, Liu S, Zhou Y (2013) Effects of wheat as companion cropping on growth, soil enzymes and disease resistance of watermelon. Allelopath J 32:267–278

    Google Scholar 

  • Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrod D, Dhingra A, Schillinger WF, Paulitz TC (2013) Role of bacterial communities in the natural suppression of rhizoctonia solani bar patch disease of wheat (Triticum aestivum L.). Appl Environ Microbiol 79:7428–7438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan WM, Crawford DL (1995) Characterization of streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou BL, Chen ZX, Du L, Ye XL, Liu YF (2012) Resistance of eggplant (Solanum melongena L.) to verticillium wilt correlates to microbial abundance and soil enzyme activities. Am J Exp Agric 2:557–572

    Article  Google Scholar 

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Acknowledgments

This research was supported by the National Natural Science Foundation of China (30470318, 30870454, 31371868, 31500504), National Special Fund for the Construction of Modern Agricultural Technology System (CARS-07-12.5-A10), Research Fund for the Doctoral Program of Higher Education of China (20070108007, 20121401110007) and Shanxi Scholarship Council of China (2009022, 2012013). We are very grateful to Shanghai Personal Biotechnology Co., Ltd for Illumina sequencing.

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Correspondence to Huilan Yi.

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Han, Y., Xu, L., Liu, L. et al. Illumina sequencing reveals a rhizosphere bacterial community associated with foxtail millet smut disease suppression. Plant Soil 410, 411–421 (2017). https://doi.org/10.1007/s11104-016-3042-7

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