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Response of soil, leaf endosphere and phyllosphere bacterial communities to elevated CO2 and soil temperature in a rice paddy

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Abstract

Aims

The objective of this study was to elucidate the composition of bacterial communities from the soil, and endosphere and phyllosphere of upper and lower leaves and clarify the responses to elevated CO2 and/or soil temperature.

Methods

Using 454 pyrosequencing, the 16S rRNA gene was analyzed from various bacterial communities in a rice paddy that was exposed to different atmospheric CO2 concentrations (ambient, +200 μmol.mol−1) and soil temperatures (ambient, +2 °C).

Results

The treatments of elevated temperature and elevated CO2 plus temperature exerted significant influence on the structure of bacterial communities from the lower leaf endosphere. A significant influence of elevated CO2 plus temperature on the community structure was also observed in the upper leaf phyllosphere. The richness and diversity of bacterial communities from the lower leaf phyllosphere, upper leaf endosphere, and upper leaf phyllosphere were significantly affected by elevated CO2 plus temperature. However, we did not observe any significant influence of all climate change treatments (elevated CO2, elevated temperature, and their combination) on the richness, diversity, and structure of soil bacterial communities. We also did not observe any significant effect of the single factor, elevated CO2, on the structure of the leaf endosphere and phyllosphere bacterial communities. Enterobacteriaceae and Xanthomonadaceae were the most shifted phylotypes in response to elevated temperature and elevated CO2 plus temperature.

Conclusions

Soil bacterial communities were more resistant to the tested climate change factors compare with foliar bacterial communities. Temperature was a more important factor in shaping the structure of foliar bacterial communities compared with CO2. The response of leaf-associated bacterial communities could be influenced by the leaf location (upper leaf or lower leaf) within the rice plants and by the habitats (leaf endosphere or phyllosphere).

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References

  • Abril AB, Torres PA, Bucher EH (2005) The importance of phyllosphere microbial populations in nitrogen cycling in the Chaco semi-arid woodland. J Trop Ecol 21:103–107

    Article  Google Scholar 

  • Adhikari TB, Joseph CM, Yang G, Phillips DA, Nelson LM (2001) Evaluation of bacteria isolated from rice for plant growth promotion and biological control of seedling disease of rice. Can J Microbiol 47:916–924

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA, Leakey ADB, Ort DR, Long SP (2008) FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2] impacts on crop yield and food supply. New Phytol 179:5–9

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372

    Article  PubMed  Google Scholar 

  • Araújo WL, Marcon J, Maccheroni W, van Elsas JD, van Vuurde JWL, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914

    Article  PubMed Central  PubMed  Google Scholar 

  • Austin EE, Castro HF, Sides KE, Schadt CW, Classen AT (2009) Assessment of 10 years of CO2 fumigation on soil microbial communities and function in a sweetgum plantation. Soil Biol Biochem 41:514–520

    Article  CAS  Google Scholar 

  • Bálint M, Tiffin P, Hallströem B, O’Hara RB, Olson MS, Fankhauser JD, Piepenbring M, Schmitt I (2013) Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS One 8:e53987

    Article  PubMed Central  PubMed  Google Scholar 

  • Balint-Kurti P, Simmons SJ, Blum JE, Ballaré CL, Stapleton AE (2010) Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol Plant-Microbe Interact 23:473–484

    Article  CAS  PubMed  Google Scholar 

  • Belote RT, Weltzin JF, Norby RJ (2004) Response of an understory plant community to elevated [CO2] depends on differential responses of dominant invasive species and is mediated by soil water availability. New Phytol 161:827–835

    Article  Google Scholar 

  • Bengtsson J, Eriksson KM, Hartmann M, Wang Z, Shenoy BD, Grelet GA, Abarenkov K, Petri A, Rosenblad MA, Nilsson RH (2011) Metaxa: a software tool for automated detection and discrimination among ribosomal small subunit (12S/16S/18S) sequences of archaea, bacteria, eukaryotes, mitochondria, and chloroplasts in metagenomes and environmental sequencing datasets. Antonie Van Leeuwenhoek 100:471–475

    Article  PubMed  Google Scholar 

  • Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chinnadurai C, Balachandar D, Sundaram SP (2009) Characterization of 1-aminocyclopropane-1-carboxylate deaminase producing methylobacteria from phyllosphere of rice and their role in ethylene regulation. World J Microbiol Biotechnol 25:1403–1411

    Article  CAS  Google Scholar 

  • Coince A, Cordier T, Lengellé J, Defossez E, Vacher C, Robin C, Buée M, Marcais B (2014) Leaf and root-associated fungal assemblages do not follow similar elevational diversity patterns. PLoS One 9:e100668

    Article  PubMed Central  PubMed  Google Scholar 

  • Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214

    CAS  PubMed  Google Scholar 

  • Cordier T, Robin C, Capdevielle X, Desprez-Loustau M-L, Vacher C (2012a) Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus syluatica). Fungal Ecol 5:509–520

    Article  Google Scholar 

  • Cordier T, Robin C, Capdevielle X, Fabreguettes O, Desprez-Loustau M-L, Vacher C (2012b) The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. New Phytol 196:510–519

    Article  PubMed  Google Scholar 

  • Costa DM, Samarasinghe SST, Dias HRD, Dissanayake DMN (2008) Control of rice sheath blight by phyllosphere epiphytic microbial antagonists. Phytoparasitica 36:52–65

    Article  Google Scholar 

  • De Maayer P, Chan WY, Blom J, Venter SN, Duffy B, Smits THM, Coutinho TA (2012) The large universal Pantoea plasmid LPP-1 plays a major role in biological and ecological diversification. BMC Genomics 13:625

    Article  PubMed Central  PubMed  Google Scholar 

  • Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106:16428–16433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detec-tion. Bioinformatics 27:2194–2200

  • Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato Y-I, Morisaki H, Mitsui H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46:617–629

    Article  Google Scholar 

  • Ellis RJ, Thompson IP, Bailey MJ (1999) Temporal fluctuations in the pseudomonad population associated with sugar beet leaves. FEMS Microbiol Ecol 28:345–356

    Article  CAS  Google Scholar 

  • Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–570

    Article  PubMed  Google Scholar 

  • Feng YJ, Shen DL, Dong XZ, Song W (2003) In vitro symplasmata formation in the rice diazotrophic endophyte Pantoea agglomerans YS19. Plant Soil 255:435–444

    Article  CAS  Google Scholar 

  • Ferrando L, Mañay JF, Scavino AF (2012) Molecular and culture-dependent analyses revealed similarities in the endophytic bacterial community composition of leaves from three rice (Oryza sativa) varieties. FEMS Microbiol Ecol 80:696–708

    Article  CAS  PubMed  Google Scholar 

  • Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105:17994–17999

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804

    Article  PubMed  Google Scholar 

  • Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl Environ Microbiol 77:7647–7655

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freiberg E (1998) Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a Costa Rican premontane rain forest. Oecologia 117:9–18

    Article  Google Scholar 

  • Garbeva P, van Overbeek L, van Vuurde J, van Elsas J (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383

    Article  CAS  PubMed  Google Scholar 

  • Gyaneshwar P, James EK, Mathan N, Reddy PM, Reinhold-Hurek B, Ladha JK (2001) Endophytic colonization of rice by a diazotrophic strain of Serratia marcescens. J Bacteriol 183:2634–2645

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hardoim PR, Hardoim CCP, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hartmann M, Howes CG, Abarenkov K, Mohn WW, Nilsson RH (2010) V-Xtractor: An open-source, high-throughput software tool to identify and extract hypervariable regions of small subunit (16S/18S) ribosomal RNA gene sequences. J Microbiol Methods 83:250–253

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa T, Sakai H, Tokida T, Nakamura H, Zhu C, Usui Y, Yoshimoto M, Fukuoka M, Wakatsuki H, Katayanagi N, Matsunami T, Kaneta Y, Sato T, Takakai F, Sameshima R, Okada M, Mae T, Makino A (2013) Rice cultivar responses to elevated CO2 at two free-air CO2 enrichment (FACE) sites in Japan. Funct Plant Biol 40:148–159

    Article  CAS  Google Scholar 

  • He ZL, Xu MY, Deng Y, Kang S, Kang S, Kellogg L, Wu LY, Van Nostrand JD, Hobbie SE, Reich PB, Zhou JZ (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13:564–575

    Article  PubMed  Google Scholar 

  • Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255

    Article  PubMed Central  PubMed  Google Scholar 

  • Idso KE, Idso SB (1994) Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years’ research. Agric For Meteorol 69:153–203

    Article  Google Scholar 

  • Ikeda S, Tokida T, Nakamura H, Sakai H, Usui Y, Okubo T, Tago K, Hayashi K, Sekiyama Y, Ono H, Tomita S, Hayatsu M, Hasegawa T, Minamisawa K (2015) Characterization of leaf blade- and leaf sheath-associated bacterial communities and assessment of their responses to environmental changes in CO2, temperature, and nitrogen levels under field conditions. Microbes Environ. doi:10.1264/jsme2.ME14117

    Google Scholar 

  • Janarthine SRS, Eganathan P (2012) Plant growth promoting of endophytic Sporosarcina aquimarina SjAM16103 isolated from the pneumatophores of Avicennia marina L. Int J Microbiol 2012:1–10

    Article  Google Scholar 

  • Janus L, Angeloni N, McCormack J, Rier S, Tuchman N, Kelly J (2005) Elevated atmospheric CO2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots. Microb Ecol 50:102–109

    Article  PubMed  Google Scholar 

  • Kim HJ, Lee JH, Kang BR, Rong X, Gardener BBM, Ji HJ, Park C-S, Kim YC (2012) Draft genome sequence of Pantoea ananatis B1-9, a nonpathogenic plant growth-promoting bacterium. J Bacteriol 194:729

  • Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leadley PW, Niklaus PA, Stocker R, Körner C (1999) A field study of the effects of elevated CO2 on plant biomass and community structure in a calcareous grassland. Oecologia 118:39–49

    Article  CAS  PubMed  Google Scholar 

  • Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lipson DA, Blair M, Barron-Gafford G, Grieve K, Murthy R (2006) Relationships between microbial community structure and soil processes under elevated atmospheric carbon dioxide. Microb Ecol 51:302–314

    Article  PubMed  Google Scholar 

  • Lopez-Velasco G, Welbaum GE, Boyer RR, Mane SP, Ponder MA (2011) Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16S rRNA amplicons. J Appl Microbiol 110:1203–1214

    Article  CAS  PubMed  Google Scholar 

  • Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115

    Article  PubMed  Google Scholar 

  • Madhaiyan M, Peng N, Ji LH (2013) Complete genome sequence of Enterobacter sp. strain R4-368, an endophytic N-fixing Gammaproteobacterium isolated from surface-sterilized roots of Jatropha curcas L. Genome Announc 1:e00544-13

    Article  PubMed Central  PubMed  Google Scholar 

  • Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117

    Article  PubMed  Google Scholar 

  • Mano H, Tanaka F, Nakamura C, Kaga H, Morisaki H (2007) Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 22:175–185

    Article  Google Scholar 

  • Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 21:86–100

    Article  Google Scholar 

  • Mishra A, Chauhan PS, Chaudhry V, Tripathi M, Nautiyal CS (2011) Rhizosphere competent Pantoea agglomerans enhances maize (Zea mays) and chickpea (Cicer arietinum L.) growth, without altering the rhizosphere functional diversity. Antonie Van Leeuwenhoek 100:405–413

    Article  PubMed  Google Scholar 

  • Miyamoto T, Kawahara M, Minamisawa K (2004) Novel endophytic nitrogen-fixing clostridia from the grass Miscanthus sinensis as revealed by terminal restriction fragment length polymorphism analysis. Appl Environ Microbiol 70:6580–6586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Montealegre CM, Van Kessel C, Blumenthal JM, Hur H-G, Hartwig UA, Sadowsky MJ (2000) Elevated atmospheric CO2 alters microbial population structure in a pasture ecosystem. Glob Chang Biol 6:475–482

    Article  Google Scholar 

  • Morris CE (2002) Phyllosphere. In: Encyclopedia of life sciences. John Wiley & Sons Ltd, Chichester. http://www.els.net. Accessed March 2002

  • Morris CE, Kinkel LL (2002) Fifty years of phyllosphere microbiology: significant contributions to research in related fields. In: Lindow SE, HechtPoinar EI, Elliott VJ (eds) Phyllosphere microbiology. APS Press, St Paul, pp 365–375

    Google Scholar 

  • Nakamura H, Tokida T, Yoshimoto M, Sakai H, Fukuoka M, Hasegawa T (2012) Performance of the enlarged Rice-FACE system using pure CO2 installed in Tsukuba, Japan. J Agric Meteorol 68:15–23

    Article  Google Scholar 

  • Okada H, Sakai H, Tokida T, Usui Y, Nakamura H, Hasegawa T (2014) Elevated temperature has stronger effects on the soil food web of a flooded paddy than does CO2. Soil Biol Biochem 70:166–175

    Article  CAS  Google Scholar 

  • Okubo T, Tokida T, Ikeda S, Bao Z, Tago K, Hayatsu M, Nakamura H, Sakai H, Usui Y, Hayashi K, Hasegawa T, Minamisawa K (2014) Effects of elevated carbon dioxide, elevated temperature, and rice growth stage on the community structure of rice root-associated bacteria. Microbes Environ 29:184–190

    Article  PubMed Central  PubMed  Google Scholar 

  • Osono T (2014) Diversity and ecology of endophytic and epiphytic fungi of tree leaves in Japan: a review. In: Gange AC, Verma VC (eds) Advances in endophytic research. Springer, India, pp 3–26

    Chapter  Google Scholar 

  • Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact ? Front Plant Sci 2:100

    Article  PubMed Central  PubMed  Google Scholar 

  • Peñuelas J, Rico L, Ogaya R, Jump AS, Terradas J (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biol 14:565–575

    Article  PubMed  Google Scholar 

  • Peñuelas J, Terradas J (2014) The foliar microbiome. Trends Plant Sci 19:278–280

    Article  PubMed  Google Scholar 

  • Quecine MC, Araújo WL, Rossetto PB, Ferreira A, Tsui S, Lacava PT, Mondin M, Azevedo JL, Pizzirani-Kleiner AA (2012) Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1. Appl Environ Microbiol 78:7511–7518

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rasche F, Marco-Noales E, Velvis H, van Overbeek LS, López MM, van Elsas JD, Sessitsch A (2006) Structural characteristics and plant-beneficial effects of bacteria colonizing the shoots of field grown conventional and genetically modified T4-lysozyme producing potatoes. Plant Soil 289:123–140

    Article  CAS  Google Scholar 

  • Rastogi G, Coaker GL, Leveau JHJ (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10

    Article  CAS  PubMed  Google Scholar 

  • Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6:1812–1822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893

    Article  PubMed Central  PubMed  Google Scholar 

  • Redford AJ, Fierer N (2009) Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb Ecol 58:189–198

    Article  PubMed  Google Scholar 

  • Reisberg E, Hildebrandt U, Riederer M, Hentschel U (2012) Phyllosphere bacterial communities of trichome-bearing and trichomeless Arabidopsis thaliana leaves. Antonie Van Leeuwenhoek 101:551–560

    Article  PubMed  Google Scholar 

  • Ren GD, Zhang HY, Lin XG, Zhu JG, Jia ZJ (2014a) Response of phyllosphere bacterial communities to elevated CO2 during rice growing season. Appl Microbiol Biotechnol 98:9459–9471

    Article  CAS  PubMed  Google Scholar 

  • Ren GD, Zhu JG, Jia ZJ (2014b) Contrasting response patterns of rice phyllosphere bacterial taxa to elevated CO2. Pedosphere 24:544–552

    Article  Google Scholar 

  • Rico L, Ogaya R, Terradas J, Penuelas J (2014) Community structures of N2-fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought. Plant Biol 16:586–593

    Article  CAS  PubMed  Google Scholar 

  • Ruinen J (1961) The phyllosphere. I. An ecologically neglected milieu. Plant Soil 15:81–109

    Article  Google Scholar 

  • Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525

    Article  CAS  PubMed  Google Scholar 

  • Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta A, Mishra P, Gupta H (2008) Characterization of a cold-tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J Microbiol Biotechnol 24:955–960

    Article  CAS  Google Scholar 

  • Sessitsch A, Hardoim P, Döering J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36

    Article  CAS  PubMed  Google Scholar 

  • Shahzad S, Khalid A, Arshad M, Khalid M, Mehboob I (2008) Integrated use of plant growth promoting bacteria and P-enriched compost for improving growth, yield and nodulation of chickpea. Pak J Bot 40:1735–1741

    Google Scholar 

  • Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365

    Article  Google Scholar 

  • Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840

    Article  CAS  PubMed  Google Scholar 

  • Wang BZ, Zhang CX, Liu JL, Zeng XW, Li FR, Wu YC, Lin XG, Xiong ZQ, Xu J, Jia ZJ (2012) Microbial community changes along a land-use gradient of desert soil origin. Pedosphere 22:593–603

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755

    Article  CAS  PubMed  Google Scholar 

  • Witzel K, Gwinn-Giglio M, Nadendla S, Shefchek K, Ruppel S (2012) Genome sequence of Enterobacter radicincitans DSM16656T, a plant growth-promoting endophyte. J Bacteriol 194:5469

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong XQ, Liao HD, Ma JS, Liu XM, Zhang LY, Shi XW, Yang XL, Lu XN, Zhu YH (2014) Isolation of a rice endophytic bacterium, Pantoea sp. Sd-1, with ligninolytic activity and characterization of its rice straw degradation ability. Lett Appl Microbiol 58:123–129

    Article  CAS  PubMed  Google Scholar 

  • Zhang XX, Gao JS, Cao YH, Ma XT, He JZ (2013) Long-term rice and green manure rotation alters the endophytic bacterial communities of the rice root. Microb Ecol 66:917–926

    Article  PubMed  Google Scholar 

  • Zhu B, Chen M, Lin L, Yang L, Li Y, An Q (2012) Genome sequence of Enterobacter sp. strain SP1, an endophytic nitrogen-fixing bacterium isolated from sugarcane. J Bacteriol 194:6963–6964

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by National Basic Research Program of China (973 Program, 2014CB954500) and the National Science Foundation of China (40971153 and 41090281). The FACE/warming experiment was financially supported by the Ministry of Agriculture, Forestry and Fisheries, Japan, through a research project entitled “Development of technologies for mitigation and adaptation to climate change in Agricure, Forestry and Fisheries”. This work was also supported by the Distinguished Young Scholar Programme of Jiangsu Province (BK2012048). We would like to thank Drs. Justin Kuczynski, Martin Hartmann, Johan Bengtsson, K. Martin Eriksson, Zheng Wang, Qiong Wang, and Huayong Zhang for their assistance in bioinformatics analysis. We also thank the anonymous reviewers for their constructive suggestions that helped us to greatly improved the manuscript.

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    Authors and Affiliations

    1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, Jiangsu Province, People’s Republic of China

      Gaidi Ren, Chunwu Zhu, M. Saiful Alam, Jianguo Zhu & Zhongjun Jia

    2. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, Jiangsu Province, People’s Republic of China

      Gaidi Ren

    3. Agro-Meteorology Division, National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki, 305-8604, Japan

      Chunwu Zhu, Hidemitsu Sakai, Yasuhiro Usui & Toshihiro Hasegawa

    4. Department of Soil Science, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

      M. Saiful Alam

    5. Carbon and Nutrient Cycles Division, National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki, 305-8604, Japan

      Takeshi Tokida

    6. Taiyo Keiki Co. Ltd., 1-12-3, Nakajujo, Kita-ku, Tokyo, 114-0032, Japan

      Hirofumi Nakamura

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    1. Gaidi Ren
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    Correspondence to Toshihiro Hasegawa or Zhongjun Jia.

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    Gaidi Ren and Chunwu Zhu contributed equally to this work.

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    Ren, G., Zhu, C., Alam, M.S. et al. Response of soil, leaf endosphere and phyllosphere bacterial communities to elevated CO2 and soil temperature in a rice paddy. Plant Soil 392, 27–44 (2015). https://doi.org/10.1007/s11104-015-2503-8

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    • DOI: https://doi.org/10.1007/s11104-015-2503-8

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