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Plant and Soil

, Volume 431, Issue 1–2, pp 53–69 | Cite as

Eighty years of maize breeding alters plant nitrogen acquisition but not rhizosphere bacterial community composition

  • Bryan D. EmmettEmail author
  • Daniel H. Buckley
  • Margaret E. Smith
  • Laurie E. Drinkwater
Regular Article

Abstract

Aims

There is considerable interest in breeding for crop genotypes that harness rhizosphere microbial communities and processes in support of plant productivity. However, the extent to which past breeding efforts have altered plant rhizosphere traits and plant-microbe collaborations is unknown.

Methods

We evaluated twelve best-selling and widely adapted maize hybrids released between 1936 and 2011 for changes in rhizosphere bacterial community composition (BCC) and plant access to endogenous soil nitrogen. Plants were grown in replicated monocultures fertilized with 0, 85 or 170 kg N ha−1 and measured for yield, nitrogen uptake and source. Rhizosphere BCC and function was assessed through potential extracellular enzyme assays and 16S rRNA gene amplicon sequencing.

Results

Grain yield and nitrogen uptake from soil pools increased with year of hybrid release at all fertilization levels. Rhizosphere BCC and enzyme activity also varied among hybrids. However, releases from the 1960s and 70s were most distinct, while early and late releases shared similar BCC and enzyme activity.

Conclusions

These results indicate that breeding has increased maize ability to acquire nitrogen from soil reserves, but has not resulted in a directional shift in rhizosphere bacterial community assembly. The variation observed among hybrids reveals the potential for future breeding efforts to influence rhizosphere traits.

Keywords

Bacterial community Maize Microbiome Nitrogen use efficiency Plant breeding Rhizosphere 

Abbreviations

BCC

Bacterial community composition

C

carbon

LFC

log2-fold change

MLPE

maximum likelihood population effects model

N

nitrogen

NUE

nitrogen use efficiency

V6

maize physiological stages: six-leaf

R1

flowering

R3

grain filling

PM

physiological maturity

Notes

Acknowledgements

We thank Dr. Mark Cooper for advising on the selection of hybrids and Dupont-Pioneer for providing the germplasm used in this study. This work was supported by the USDA National Institute of Food and Agriculture, Hatch project no. NYC-145446 and the Agriculture and Food Research Initiative Competitive Grant no. 2015-67019-23588.

Compliance with ethical standards

Conflicts of interest

M.E.S.’s research program receives partial cost reimbursement from Dupont-Pioneer for evaluation of Dupont-Pioneer corn hybrids in public commercial corn silage tests.

Supplementary material

11104_2018_3744_MOESM1_ESM.docx (4.6 mb)
ESM 1 (DOCX 4.58 Mb)

References

  1. Aira M, Gómez-Brandón M, Lazcano C et al (2010) Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 42:2276–2281.  https://doi.org/10.1016/j.soilbio.2010.08.029 CrossRefGoogle Scholar
  2. An G-H, Kobayashi S, Enoki H et al (2010) How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil 327:441–453.  https://doi.org/10.1007/s11104-009-0073-3 CrossRefGoogle Scholar
  3. Averill C, Finzi A (2011) Plant regulation of microbial enzyme production in situ. Soil Biol Biochem 43:2457–2460.  https://doi.org/10.1016/j.soilbio.2011.09.002 CrossRefGoogle Scholar
  4. Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32:921–950.  https://doi.org/10.1081/CSS-100104098 CrossRefGoogle Scholar
  5. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67.  https://doi.org/10.18637/jss.v067.i01
  6. Bertholdsson N-O (2004) Variation in allelopathic activity over 100 years of barley selection and breeding. Weed Res 44:78–86.  https://doi.org/10.1111/j.1365-3180.2003.00375.x CrossRefGoogle Scholar
  7. Berthrong ST, Buckley DH, Drinkwater LE (2013) Agricultural management and labile carbon additions affect soil microbial community structure and interact with carbon and nitrogen cycling. Microb Ecol 66:158–170.  https://doi.org/10.1007/s00248-013-0225-0 CrossRefPubMedGoogle Scholar
  8. Bouffaud M-L, KyselkovÁ M, Gouesnard B et al (2012) Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 21:195–206.  https://doi.org/10.1111/j.1365-294X.2011.05359.x CrossRefPubMedGoogle Scholar
  9. Campos H, Cooper M, Edmeades GO et al (2006) Changes in drought tolerance in maize associated with fifty years of breeding for yield in the US corn belt. Maydica 51:369Google Scholar
  10. Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522.  https://doi.org/10.1073/pnas.1000080107 CrossRefPubMedGoogle Scholar
  11. Cassman KG, Dobermann A, Walters DT (2002) Agroecosystems, nitrogen-use efficiency, and nitrogen management. AMBIO J Hum Environ 31:132–140.  https://doi.org/10.1579/0044-7447-31.2.132 CrossRefGoogle Scholar
  12. Chanway CP, Holl FB (1993) First year field performance of spruce seedlings inoculated with plant growth promoting rhizobacteria. Can J Microbiol 39:1084–1088.  https://doi.org/10.1139/m93-164 CrossRefGoogle Scholar
  13. Ciampitti IA, Vyn TJ (2012) Physiological perspectives of changes over time in maize yield dependency on nitrogen uptake and associated nitrogen efficiencies: a review. Field Crop Res 133:48–67.  https://doi.org/10.1016/j.fcr.2012.03.008 CrossRefGoogle Scholar
  14. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187.  https://doi.org/10.1016/0038-0717(85)90113-0 CrossRefGoogle Scholar
  15. Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for regression relationships between distance matrices: estimating gene flow with distance. J Agric Biol Environ Stat 7:361–372.  https://doi.org/10.1198/108571102320 CrossRefGoogle Scholar
  16. Dawson JC, Huggins DR, Jones SS (2008) Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crop Res 107:89–101.  https://doi.org/10.1016/j.fcr.2008.01.001 CrossRefGoogle Scholar
  17. Dawson W, Hör J, Egert M et al (2017) A small number of low-abundance bacteria dominate plant species-specific responses during rhizosphere colonization. Front Microbiol 8:975.  https://doi.org/10.3389/fmicb.2017.00975 CrossRefPubMedPubMedCentralGoogle Scholar
  18. DeAngelis KM, Brodie EL, DeSantis TZ et al (2009) Selective progressive response of soil microbial community to wild oat roots. Isme J 3:168–178.  https://doi.org/10.1038/ismej.2008.103 CrossRefPubMedGoogle Scholar
  19. DeBruin JL, Schussler JR, Mo H, Cooper M (2017) Grain yield and nitrogen accumulation in maize hybrids released during 1934 to 2013 in the US Midwest. Crop Sci 57:1431–1446.  https://doi.org/10.2135/cropsci2016.08.0704 CrossRefGoogle Scholar
  20. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216.  https://doi.org/10.3389/fmicb.2013.00216 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Drinkwater LE, Snapp SS (2007a) Understanding and managing the rhizosphere in agroecosystems. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere. Academic Press, Burlington, pp 127–153CrossRefGoogle Scholar
  22. Drinkwater LE, Snapp SS (2007b) Nutrients in agroecosystems: rethinking the management paradigm. Adv Agron 92(92):163CrossRefGoogle Scholar
  23. Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Adv Agron 86:83–145CrossRefGoogle Scholar
  24. Duvick DN, Smith JSC, Cooper M (2004) Long-term selection in a commercial hybrid maize breeding program. Plant Breed Rev 24:2Google Scholar
  25. Edwards J, Johnson C, Santos-Medellín C et al (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920.  https://doi.org/10.1073/pnas.1414592112 CrossRefPubMedGoogle Scholar
  26. Emmett, B (2017) Intra- and interspecific variation in rhizosphere bacterial community composition and metabolism among maize and summer annuals in agricultural fields. Doctoral dissertation, Cornell University, Ithaca, NYGoogle Scholar
  27. Emmett BD, Youngblut ND, Buckley DH, Drinkwater LE (2017) Plant phylogeny and life history shape rhizosphere bacterial microbiome of summer annuals in an agricultural field. Front Microbiol 8:2414.  https://doi.org/10.3389/fmicb.2017.02414 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gardner JB, Drinkwater LE (2009) The fate of nitrogen in grain cropping systems: a meta-analysis of N-15 field experiments. Ecol Appl 19:2167–2184.  https://doi.org/10.1890/08-1122.1 CrossRefPubMedGoogle Scholar
  29. German DP, Weintraub MN, Grandy AS et al (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397.  https://doi.org/10.1016/j.soilbio.2011.03.017 CrossRefGoogle Scholar
  30. Germida JJ, Siciliano SD (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils 33:410–415.  https://doi.org/10.1007/s003740100343 CrossRefGoogle Scholar
  31. Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378.  https://doi.org/10.1016/S0038-0717(97)00124-7 CrossRefGoogle Scholar
  32. Haegele JW, Cook KA, Nichols DM, Below FE (2013) Changes in nitrogen use traits associated with genetic improvement for grain yield of maize hybrids released in different decades. Crop Sci 53:1256.  https://doi.org/10.2135/cropsci2012.07.0429 CrossRefGoogle Scholar
  33. Herman DJ, Johnson KK, Jaeger CH et al (2006) Root influence on nitrogen mineralization and nitrification in Avena barbata rhizosphere soil. Soil Sci Soc Am J 70:1504–1511.  https://doi.org/10.2136/sssaj2005.0113 CrossRefGoogle Scholar
  34. Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303.  https://doi.org/10.1111/j.1469-8137.2005.01512.x CrossRefPubMedGoogle Scholar
  35. Jackson LE (1995) Root architecture in cultivated and wild lettuce (Lactuca spp.). Plant Cell Environ 18:885–894.  https://doi.org/10.1111/j.1365-3040.1995.tb00597.x CrossRefGoogle Scholar
  36. Jones DL, Farrar J, Giller KE (2003) Associative nitrogen fixation and root exudation - what is theoretically possible in the rhizosphere? Symbiosis 35:19–38Google Scholar
  37. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev. Ecol Evol Syst 39:215–236.  https://doi.org/10.1146/annurev.ecolsys.39.110707.173423 CrossRefGoogle Scholar
  38. Kiers ET, Hutton MG, Denison RF (2007) Human selection and the relaxation of legume defences against ineffective rhizobia. Proc R Soc B Biol Sci 274:3119–3126.  https://doi.org/10.1098/rspb.2007.1187 CrossRefGoogle Scholar
  39. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120.  https://doi.org/10.1128/AEM.01043-13 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: Tests in linear mixed effects modelsGoogle Scholar
  41. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669.  https://doi.org/10.1111/nph.12235 CrossRefPubMedGoogle Scholar
  42. Leff JW, Lynch RC, Kane NC, Fierer N (2017) Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus. New Phytol 214:412–423.  https://doi.org/10.1111/nph.14323 CrossRefPubMedGoogle Scholar
  43. Lehmann A, Barto EK, Powell JR, Rillig MC (2012) Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil 355:231–250.  https://doi.org/10.1007/s11104-011-1095-1 CrossRefGoogle Scholar
  44. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33.  https://doi.org/10.18637/jss.v069.i01 CrossRefGoogle Scholar
  45. Li X, Rui J, Xiong J et al (2014) Functional potential of soil microbial communities in the maize rhizosphere. PLoS One 9:e112609.  https://doi.org/10.1371/journal.pone.0112609 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Liu W, Wang Q, Hou J et al (2016) Whole genome analysis of halotolerant and alkalotolerant plant growth-promoting rhizobacterium Klebsiella sp. D5A. Sci Rep 6:26710.  https://doi.org/10.1038/srep26710 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Liu X-JA, van Groenigen KJ, Dijkstra P, Hungate BA (2017) Increased plant uptake of native soil nitrogen following fertilizer addition - not a priming effect? Appl Soil Ecol 114:105–110.  https://doi.org/10.1016/j.apsoil.2017.03.011 CrossRefGoogle Scholar
  48. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550.  https://doi.org/10.1186/s13059-014-0550-8 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357.  https://doi.org/10.1093/aob/mcs293 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10.  https://doi.org/10.1007/bf00011685 CrossRefGoogle Scholar
  51. Mahoney AK, Yin C, Hulbert SH (2017) Community structure, species variation, and potential functions of rhizosphere-associated bacteria of different winter wheat (Triticum aestivum) cultivars. Front Plant Sci 8.  https://doi.org/10.3389/fpls.2017.00132
  52. Mazzola M, Gu Y-H (2002) Wheat genotype-specific induction of soil microbial communities suppressive to disease incited by Rhizoctonia solani anastomosis group (AG)-5 and AG-8. Phytopathology 92:1300–1307.  https://doi.org/10.1094/PHYTO.2002.92.12.1300 CrossRefPubMedGoogle Scholar
  53. Mazzola M, Funnell DL, Raaijmakers JM (2004) Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microb Ecol 48:338–348.  https://doi.org/10.1007/s00248-003-1067-y CrossRefPubMedGoogle Scholar
  54. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217CrossRefPubMedPubMedCentralGoogle Scholar
  55. Montañez A, Abreu C, Gill P et al (2009) Biological nitrogen fixation in maize (Zea mays L.) by 15 N isotope-dilution and identification of associated culturable diazotrophs. Biol Fertil Soils 45:253–263.  https://doi.org/10.1007/s00374-008-0322-2 CrossRefGoogle Scholar
  56. Nuccio EE, Anderson-Furgeson J, Estera KY et al (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97:1307–1318.  https://doi.org/10.1890/15-0882.1 CrossRefPubMedGoogle Scholar
  57. Oksanen J, Blanchet FG, Kindt R, et al (2012) vegan: community ecology packageGoogle Scholar
  58. Paterson E, Sim A, Standing D et al (2006) Root exudation from Hordeum vulgare in response to localized nitrate supply. J Exp Bot 57:2413–2420.  https://doi.org/10.1093/jxb/erj214 CrossRefPubMedGoogle Scholar
  59. Peiffer JA, Spor A, Koren O et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci 110:6548–6553.  https://doi.org/10.1073/pnas.1302837110 CrossRefPubMedGoogle Scholar
  60. Pepe-Ranney C, Campbell AN, Koechli C et al (2016) Unearthing the ecology of soil microorganisms using a high resolution DNA-SIP approach to explore cellulose and xylose metabolism in soil. Front Microbiol 7:703.  https://doi.org/10.3389/fmicb.2016.00703 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pérez-Jaramillo JE, Mendes R, Raaijmakers JM (2015) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol:1–10.  https://doi.org/10.1007/s11103-015-0337-7
  62. Pérez-Jaramillo JE, Carrión VJ, Bosse M et al (2017) Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J 11:2244.  https://doi.org/10.1038/ismej.2017.85 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799.  https://doi.org/10.1038/nrmicro3109 CrossRefPubMedGoogle Scholar
  64. Plénet D, Lemaire G (1999) Relationships between dynamics of nitrogen uptake and dry matter accumulation in maize crops. Determination of critical N concentration. Plant Soil 216:65–82.  https://doi.org/10.1023/A:1004783431055 CrossRefGoogle Scholar
  65. Postma JA, Dathe A, Lynch JP (2014) The optimal lateral root branching density for maize dpends on nitrogen and phosphorus availability. Plant Physiol 166:590.  https://doi.org/10.1104/pp.113.233916 CrossRefPubMedPubMedCentralGoogle Scholar
  66. R Development Core Team (2012) R: A language and environment for statistical computing. http://www.R-project.org
  67. Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363.  https://doi.org/10.2134/agronj1999.00021962009100030001x CrossRefGoogle Scholar
  68. Salinero KK, Keller K, Feil WS et al (2009) Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics 10:351–351.  https://doi.org/10.1186/1471-2164-10-351 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Sanchez JE, Paul EA, Willson TC et al (2002) Corn root effects on the nitrogen-supplying capacity of a conditioned soil. Agron J 94:391–396.  https://doi.org/10.2134/agronj2002.3910 CrossRefGoogle Scholar
  70. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.  https://doi.org/10.1890/03-8002 CrossRefGoogle Scholar
  71. Schmidt JE, Bowles TM, Gaudin ACM (2016) Using ancient traits to convert soil health into crop yield: impact of selection on maize root and rhizosphere function. Front Plant Sci 7:373.  https://doi.org/10.3389/fpls.2016.00373 PubMedCrossRefPubMedCentralGoogle Scholar
  72. Sinclair TR, Rufty TW (2012) Nitrogen and water resources commonly limit crop yield increases, not necessarily plant genetics. Glob Food Sec 1:94–98.  https://doi.org/10.1016/j.gfs.2012.07.001 CrossRefGoogle Scholar
  73. Smith JSC, Duvick DN, Smith OS et al (2004) Changes in pedigree backgrounds of Pioneer brand maize hybrids widely grown from 1930 to 1999. Crop Sci 44:1935–1946.  https://doi.org/10.2135/cropsci2004.1935 CrossRefGoogle Scholar
  74. Szoboszlay M, Lambers J, Chappell J et al (2015) Comparison of root system architecture and rhizosphere microbial communities of balsas teosinte and domesticated corn cultivars. Soil Biol Biochem 80:34–44.  https://doi.org/10.1016/j.soilbio.2014.09.001 CrossRefGoogle Scholar
  75. Turner TR, Ramakrishnan K, Walshaw J et al (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258.  https://doi.org/10.1038/ismej.2013.119 CrossRefPubMedPubMedCentralGoogle Scholar
  76. USDA (2016) USDA - National Agricultural Statistics Service. In: Natl. Stat. Corn. https://www.nass.usda.gov/. Accessed 22 Jul 2017
  77. USDA-ERS (2015) USDA Economic Research Service - fertilizer use and price. In: Fertil. Use Price. http://www.ers.usda.gov/. Accessed 4 May 2015
  78. Vitousek PM, Aber JD, Howarth RW et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. https://doi.org/10.1890/1051-0761(1997)007[0737:haotgn]2.0.co;2Google Scholar
  79. Vitousek PM, Naylor R, Crews T et al (2009) Nutrient imbalances in agricultural development. Science 324:1519–1520CrossRefPubMedGoogle Scholar
  80. Whitman T, Pepe-Ranney C, Enders A et al (2016) Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter. ISME J 10:2918–2930.  https://doi.org/10.1038/ismej.2016.68 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New YorkCrossRefGoogle Scholar
  82. Wissuwa M, Mazzola M, Picard C (2009) Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321:409–430.  https://doi.org/10.1007/s11104-008-9693-2 CrossRefGoogle Scholar
  83. Woli KP, Boyer MJ, Elmore RW et al (2016) Corn era hybrid response to nitrogen fertilization. Agron J 108:473.  https://doi.org/10.2134/agronj2015.0314 CrossRefGoogle Scholar
  84. York LM, Galindo-Castañeda T, Schussler JR, Lynch JP (2015) Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. J Exp Bot 66:2347–2358.  https://doi.org/10.1093/jxb/erv074 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zhu B, Gutknecht JLM, Herman DJ et al (2014) Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol Biochem 76:183–192.  https://doi.org/10.1016/j.soilbio.2014.04.033 CrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Horticulture Section, School of Integrative Plant ScienceCornell UniversityIthacaUSA
  2. 2.Soil and Crop Sciences Section, School of Integrative Plant ScienceCornell UniversityIthacaUSA
  3. 3.Plant Breeding and Genetics Section, School of Integrative Plant ScienceCornell UniversityIthacaUSA

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