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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
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
References
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
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
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
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
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
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
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
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
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 51:369
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
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
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
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
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
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
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
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
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
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
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
Drinkwater LE, Snapp SS (2007a) Understanding and managing the rhizosphere in agroecosystems. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere. Academic Press, Burlington, pp 127–153
Drinkwater LE, Snapp SS (2007b) Nutrients in agroecosystems: rethinking the management paradigm. Adv Agron 92(92):163
Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Adv Agron 86:83–145
Duvick DN, Smith JSC, Cooper M (2004) Long-term selection in a commercial hybrid maize breeding program. Plant Breed Rev 24:2
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
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, NY
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
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
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
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
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
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
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
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
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
Jones DL, Farrar J, Giller KE (2003) Associative nitrogen fixation and root exudation - what is theoretically possible in the rhizosphere? Symbiosis 35:19–38
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
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
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
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: Tests in linear mixed effects models
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
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
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
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
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
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
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
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
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
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10. https://doi.org/10.1007/bf00011685
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
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
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
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217
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
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
Oksanen J, Blanchet FG, Kindt R, et al (2012) vegan: community ecology package
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
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
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
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
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
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
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
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
R Development Core Team (2012) R: A language and environment for statistical computing. http://www.R-project.org
Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363. https://doi.org/10.2134/agronj1999.00021962009100030001x
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
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
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. https://doi.org/10.1890/03-8002
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
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
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
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
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
USDA (2016) USDA - National Agricultural Statistics Service. In: Natl. Stat. Corn. https://www.nass.usda.gov/. Accessed 22 Jul 2017
USDA-ERS (2015) USDA Economic Research Service - fertilizer use and price. In: Fertil. Use Price. http://www.ers.usda.gov/. Accessed 4 May 2015
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;2
Vitousek PM, Naylor R, Crews T et al (2009) Nutrient imbalances in agricultural development. Science 324:1519–1520
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
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Responsible Editor: Stéphane Compant.
Electronic supplementary material
ESM 1
(DOCX 4.58 Mb)
Rights and permissions
About this article
Cite this article
Emmett, B.D., Buckley, D.H., Smith, M.E. et al. Eighty years of maize breeding alters plant nitrogen acquisition but not rhizosphere bacterial community composition. Plant Soil 431, 53–69 (2018). https://doi.org/10.1007/s11104-018-3744-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3744-0