Wheat, maize and sunflower cropping systems selectively influence bacteria community structure and diversity in their and succeeding crop’s rhizosphere

doi:10.1016/S2095-3119(15)61147-9

摘要/Abstract

Abstract: Wheat and maize are increasingly used as alternative crops to sunflower monocultures that dominate the Hetao Irrigation District in China. Shifts from sunflower monocultures to alternate cropping systems may have significant effects on belowground microbial communities which control nutrient cycling and influence plant productivity. In this research, rhizosphere bacterial communities were compared among sunflower, wheat and maize cropping systems by 454 pyrosequencing. These cropping systems included 2 years wheat (cultivar Yongliang 4) and maize (cultivar Sidan 19) monoculture, more than 20 years sunflower (cultivar 5009) monoculture, and wheat-sunflower and maize-sunflower rotation. In addition, we investigated rhizosphere bacterial communities of healthy and diseased plants at maturity to determine the relationship between plant health and rotation effect. The results revealed taxonomic information about the overall bacterial community. And significant differences in bacterial community structure were detected among these cropping systems. Eight of the most abundant groups including Proteobacteria, Bacteroidetes, Acidobacteria, Gemmatimonadetes, Chloroflexi, Actinobacteria, Planctomycetes and Firmicutes accounted for more than 85% of the sequences in each treatment. The wheat-wheat rhizosphere had the highest proportion of Acidobacteria, Bacteroidetes and the lowest proportion of unclassified bacteria. Wheat-sunflower cropping system showed more abundant Acidobacteria than maize-sunflower and sunflower monoculture, exhibiting some influences of wheat on the succeeding crop. Maize-maize rhizosphere had the highest proportion of γ- Proteobacteria, Pseudomonadales and the lowest proportion of Acidobacteria. Sunflower rotation with wheat and maize could increase the relative abundance of the Acidobacteria while decrease the relative abundance of the unclassified phyla, as was similar with the health plants. This suggests some positive impacts of rotation with wheat and maize on the bacterial communities within a single field. These results demonstrate that different crop rotation systems can have significant effects on rhizosphere microbiomes that potentially alter plant productivities in agricultural systems.

Key words: bacterial community structure and diversity , rhizosphere , cropping system , 454 pyrosequencing

WEN Xin-ya, Eric Dubinsky, WU Yao, Yu Rong, CHEN Fu. [J]. Journal of Integrative Agriculture, 2016, 15(8): 1892-1902.

WEN Xin-ya, Eric Dubinsky, WU Yao, Yu Rong, CHEN Fu. Wheat, maize and sunflower cropping systems selectively influence bacteria community structure and diversity in their and succeeding crop’s rhizosphere[J]. Journal of Integrative Agriculture, 2016, 15(8): 1892-1902.

参考文献

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.

Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K. 2006. The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiology Ecology, 56, 250–261.

Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K. 2002. Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Applied and Environmental Microbiology, 68, 3328–3338.

Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat E V L, Schulze-Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology, 64, 807–838.

Cook R J, Thomashow L S, Weller D M, Fujimoto D, Mazzola M, Bangera G, Kim D S. 1995. Molecular mechanisms of defense by rhizobacteria against root disease. Proceedings of the National Academy of Sciences of the United States of America, 92, 4197–4201.

Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K. 2006. Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiology Ecology, 56, 236–249.

Donn S, Kirkegaard J A, Perera G, Richardson A E, Watt M. 2015. Evolution of bacterial communities in the wheat crop rhizosphere. Environmental Microbiology, 17, 610–621.

Doornbos R F, van Loon L C, Bakker P A H M. 2012. Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agronomy for Sustainable Development, 32, 227–243.

Felske A, Wolterink A, Van Lis R, Akkermans A D L. 1998. Phylogeny of the main bacterial 16S rRNA sequences in Drentse A grassland soils (The Netherlands). Applied and Environmental Microbiology, 64, 871–879.

Gao W Y, Yu J. 1986. The characteristics and pattern of phreatic evaporation consumption during soil frozen period in Hetao Irrigation District in Inner Mongolia. Inner Mongolia Water Resources, (Z1), 22–27. (in Chinese)

Garbeva P, van Elsas J D, van Veen J A. 2008. Rhizosphere microbial community and its response to plant species and soil history. Plant and Soil, 302, 19–32.

Gu Y F, Zhang X P, Tu S H, Lindström K. 2009. Soil microbial biomass, crop yields, and bacterial community structure as affected by long-term fertilizer treatments under wheat-rice cropping. European Journal of Soil Biology, 45, 239–246.

Haichar F E, Marol C, Berge O, Rangel-Castro J I, Prosser J I, Balesdent J, Heulin T, Achouak W. 2008. Plant host habitat and root exudates shape soil bacterial community structure. ISME Journal, 2, 1221–1230.

Hamel C, Hanson K, Selles F, Cruz A F, Lemke R, McConkey B, Zentner R. 2006. Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie. Soil Biology and Biochemistry, 38, 2104–2116.

Hertenberger G, Zampach P, Bachmann G. 2002. Plant species affect the concentration of free sugars and free amino acids in different types of soil. Journal of Plant Nutrition and Soil Science, 165, 557–565.

Janssen P H. 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Applied and Environmental Microbiology, 72, 1719–1728.

Jansson J K, Neufeld J D, Moran M A, Gilbert J A. 2012. Omics for understanding microbial functional dynamics. Environmental Microbiology, 14, 1–3.

Janvier C, Villeneuve F, Alabouvette C, Edel-Hermann V, Mateille T, Steinberg C. 2007. Soil health through soil disease suppression: Which strategy from descriptors to indicators? Soil Biology and Biochemistry, 39, 1–23.

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

Kielak A, Pijl A S, van Veen J A, Kowalchuk G A. 2008. Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiology Ecology, 63, 372–382

Knight R, Jansson J, Field D, Fierer N, Desai N, Fuhrman J A, Hugenholtz P, van der Lelie D, Meyer F, Stevens R, Bailey M J, Gordon J I, Kowalchuk G A, Gilbert J A. 2012. Unlocking the potential of metagenomics through replicated experimental design. Nature Biotechnology, 30, 513–520.

Kowalchuk G A, Buma D S, de Boer W, Klinkhamer P G L, van Veen J A. 2002. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek Journal of Microbiology, 81, 509–520.

Kumar P S, Brooker M R, Dowd S E, Camerlengo T. 2011. Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS ONE, 6, e20956.

Lauber C L, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology, 75, 5111–5120.

Lemanceau P, Corberand T, Gardan L, Latour X, Laguerre G, Boeufgras J, Alabouvette C. 1995. Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Applied and Environmental Microbiology, 61, 1004–1012.

Li L, Shi H, Jia J, Wang Ch, Liu H. 2010. Simulation of water and salt transport of uncultivated land in Hetao Irrigation District in Inner Mongolia. Transactions of the CSAE, 26, 31–35. (in Chinese)

Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider J H M, Piceno Y M, DeSantis T Z, Andersen G L, Bakker P A H M, Raaijmakers J M. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332, 1097–1100.

Miethling R, Wieland G, Backhaus H, Tebbe C C. 2000. Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microbial Ecology, 40, 43–56.

Navarrete A A, Kuramae E E, de Hollander M, Pijl A S, van Veen J A, Tsai S M. 2013. Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. FEMS Microbiology Ecology, 83, 607–621

Neal A L, Ahmad S, Gordon-Weeks R, Ton J. 2012. Benzoxazinoids in root exudates of maize attract pseudomonas putida to the rhizosphere. PLoS ONE, 7, 1–10.

Nelson A G, Quideau S, Frick B, Niziol D, Clapperton J, Spaner D. 2011. Spring wheat genotypes differentially alter soil microbial communities and wheat breadmaking quality in organic and conventional systems. Canadian Journal of Plant Science, 91, 485–495.

De Oliveira V M, Manfio G P, Coutinho H L D, 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.

Philippot L, Raaijmakers J M, Lemanceau P, van der Putten W H. 2013. Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11, 789–799.

Picard C, Bosco M. 2008. Genotypic and phenotypic diversity in populations of plant-probiotic Pseudomonas spp. colonizing roots. Naturwissenschaften, 95, 1–16.

Quince C, Lanzén A, Curtis T P, Davenport R J, Hall N, Head I M, Read L F, Sloan W T. 2009. Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Methods, 6, 639–641

R Development Core Team. 2006. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Raaijmakers J M, Paulitz T C, Steinberg C, Alabouvette C, Moenne-Loccoz Y. 2009. The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil, 321, 341–361.

Rousk J, Baath E, Brookes P C, Lauber C L, Lozupone C, Caporaso J G, Knight R, Fierer N. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal, 4, 1340–1351

Sanguin H, Sarniguet A, Gazengel K, Moenne-Loccoz Y, Grundmann G L. 2009. Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytologist, 184, 694–707.

Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.

Shiomi Y, Nishiyama M, Onizuka T, Marumoto T. 1999. Comparison of bacterial community structures in the rhizoplane of tomato plants grown in soils suppressive and conducive towards bacterial wilt. Applied and Environmental Microbiology, 65, 3996–4001.

Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G. 2001. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Applied and Environmental Microbiology, 67, 4742–4751.

Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K. 2001. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Applied and Environmental Microbiology, 67, 2284–2291.

Teixeira L C R S, Peixoto R S, Cury J C, Sul W J, Pellizari V H, Tiedje J, Rosado A S. 2010. Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME Journal, 4, 989–1001.

Tong W J, Chen X L, Wen X Y, Chen F, Zhang H L, Chu Q Q, Dikgwatlhe S B. 2015. Applying a salinity response function and zoning saline land for three field crops: A case study in the Hetao Irrigation District, Inner Mongolia, China. Journal of Integrative Agriculture, 14, 178–189.

Viebahn M, Veenman C, Wernars K, van Loon L C, Smit E, Bakker P A H M. 2005. Assessment of differences in ascomycete communities in the rhizosphere of field-grown wheat and potato. FEMS Microbiology Ecology, 53, 245–253.

Wang L P, Liu X, Bai Q Y, Wen Y, Liu Y J. 2011. Research on soil freezing-thawing features using liquid water information. Journal of Inner Mongolia Agricultural University (Natural Science Edition), 2, 15–39. (in Chinese)

Weller D M, Raaijmakers J M, Gardener B B M, Thomashow L S. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40, 309–348.

Yang C H, Crowley D E. 2000. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Applied and Environmental Microbiology, 66, 345–351.

Yang C H, Crowley D E, Menge J A. 2001. 16S rDNA fingerprinting of rhizosphere bacterial communities associated with healthy and Phytophthora infected avocado roots. FEMS Microbiology Ecology, 35, 129–136.

Yu Y, Wang H, Liu J, Wang Q, Shen T L, Guo W H, Wang R Q. 2012. Shifts in microbial community function and structure along the successional gradient of coastal wetlands in Yellow River Estuary. European Journal of Soil Biology, 49, 12–21.

Zamioudis C, Pieterse C M J. 2012. Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions, 25, 139–150.

Zelles L, Bai Q, Rackwitz R, Chadwick D, Beese F. 1995. Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biology and Fertility of Soils, 19, 115–123.

Zelles L, Bai Q Y, Beck T, Beese F. 1992. Signature fatty acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biology and Biochemistry, 24, 317–323.