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Title: Genetic variation in Zea mays influences microbial nitrification and denitrification in conventional agroecosystems

Journal Article · · Plant and Soil

Nitrogenous fertilizers provide a short-lived benefit to crops in agroecosystems, but stimulate nitrification and denitrification, processes that result in nitrate pollution, N2O production, and reduced soil fertility. Recent advances in plant microbiome science suggest that genetic variation in plants can modulate the composition and activity of rhizosphere N-cycling microorganisms. Here we attempted to determine whether genetic variation exists in Zea mays for the ability to influence the rhizosphere nitrifier and denitrifier microbiome under “real-world” conventional agricultural conditions. To capture an extensive amount of genetic diversity within maize we grew and sampled the rhizosphere microbiome of a diversity panel of germplasm that included ex-PVP inbreds (Z. mays ssp. mays), ex-PVP hybrids (Z. mays ssp. mays), and teosinte (Z. mays ssp. mexicana and Z. mays ssp. parviglumis). From these samples, we characterized the microbiome, a suite of microbial genes involved in nitrification and denitrification and carried out N-cycling potential assays. Here we are showing that populations/genotypes of a single species can vary in their ecological interaction with denitrifers and nitrifers. Some hybrid and teosinte genotypes supported microbial communities with lower potential nitrification and potential denitrification activity in the rhizosphere, while inbred genotypes stimulated/did not inhibit these N-cycling activities. These potential differences translated to functional differences in N2O fluxes, with teosinte plots producing less GHG than maize plots. Taken together, these results suggest that Zea genetic variation can lead to changes in N-cycling processes that result in N leaching and N2O production, and thereby are selectable targets for crop improvement. Understanding the underlying genetic variation contributing to belowground microbiome N-cycling into our conventional agricultural system could be useful for sustainability.

Research Organization:
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation Integrative Graduate Education and Research Traineeship (NSF IGERT)
Grant/Contract Number:
SC0018420
OSTI ID:
2352261
Journal Information:
Plant and Soil, Journal Name: Plant and Soil Vol. 506; ISSN 0032-079X
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (99)

Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome journal February 2019
Addressing agricultural nitrogen losses in a changing climate journal August 2018
Denitrification in a clay soil under pasture and annual crop: Estimation of potential losses using intact soil cores journal August 1993
Microbe-dependent heterosis in maize journal July 2021
Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition journal June 2017
How Plant Root Exudates Shape the Nitrogen Cycle journal August 2017
Managing nitrogen for sustainable development journal November 2015
Rhizosphere priming: a nutrient perspective journal January 2013
Road MAPs to engineer host microbiomes journal June 2018
Plant evolution driven by interactions with symbiotic and pathogenic microbes journal February 2021
Anthocyanin formation in maize roots journal September 1979
Quantitative estimation of root exudation of maize plants journal June 1985
Microbial community profiling of ammonia and nitrite oxidizing bacterial enrichments from brackishwater ecosystems for mitigating nitrogen species journal March 2020
Dynamic Controls on Field‐Scale Soil Nitrous Oxide Hot Spots and Hot Moments Across a Microtopographic Gradient journal November 2019
Mechanism of biological denitrification inhibition: procyanidins induce an allosteric transition of the membrane-bound nitrate reductase through membrane alteration journal February 2016
Exploiting crop genotype-specific root-soil interactions to enhance agronomic efficiency journal March 2023
Global Research Alliance N 2 O chamber methodology guidelines: Considerations for automated flux measurement journal September 2020
Abiotic correlates of microbial community structure and nitrogen cycling functions vary within wetlands journal June 2016
Genome-wide dissection of changes in maize root system architecture during modern breeding journal November 2022
Search and clustering orders of magnitude faster than BLAST journal August 2010
Plant–microbiome interactions: from community assembly to plant health journal August 2020
Global agriculture and nitrous oxide emissions journal May 2012
Rhizosphere Spatiotemporal Organization–A Key to Rhizosphere Functions journal July 2020
Application of plant extended phenotypes to manage the agricultural microbiome belowground journal May 2023
N 2 O Emissions From Two Agroecosystems: High Spatial Variability and Long Pulses Observed Using Static Chambers and the Flux‐Gradient Technique journal July 2019
PROGRESSIVE N LIMITATION IN FORESTS: REVIEW AND IMPLICATIONS FOR LONG-TERM RESPONSES TO ELEVATED CO 2 journal January 2006
The Microbial Engines That Drive Earth's Biogeochemical Cycles journal May 2008
Bioenergy Underground: Challenges and opportunities for phenotyping roots and the microbiome for sustainable bioenergy crop production journal January 2022
Genotypic variation in maize (Zea mays) influences rates of soil organic matter mineralization and gross nitrification journal July 2021
Human Alteration of the Global Nitrogen Cycle: Sources and Consequences journal August 1997
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley journal March 2015
A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI) journal October 2012
FunGene: the functional gene pipeline and repository journal January 2013
Maize Productivity as Influenced by Form and Availability of Nitrogen journal May 1993
Plant Growth Stage Drives the Temporal and Spatial Dynamics of the Bacterial Microbiome in the Rhizosphere of Vigna subterranea journal February 2022
Overview of recent researches on nitrifying microorganisms in soil journal October 2021
A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application journal September 2019
Linking microbial communities to ecosystem functions: what we can learn from genotype–phenotype mapping in organisms journal March 2020
N-Cycling Microbiome Recruitment Differences Between Modern and Wild Zea mays journal January 2022
Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli journal February 2019
Identification of the rhizosphere microbes that actively consume plant-derived carbon journal March 2022
Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems journal July 2013
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages journal June 2016
Biological denitrification inhibition (BDI) in the field: A strategy to improve plant nutrition and growth journal September 2019
Identification of barley genetic regions influencing plant–microbe interactions and carbon cycling in soil journal August 2021
Evolutionary Metabolomics Identifies Substantial Metabolic Divergence between Maize and Its Wild Ancestor, Teosinte journal June 2019
Barley genotype influences stabilization of rhizodeposition-derived C and soil organic matter mineralization journal April 2016
Genetic variation among elite inbred lines suggests potential to breed for BNI-capacity in maize journal August 2023
Maize germplasm chronosequence shows crop breeding history impacts recruitment of the rhizosphere microbiome journal March 2021
Survey of Anthocyanin Composition and Concentration in Diverse Maize Germplasms journal May 2017
A specialized metabolic network selectively modulates Arabidopsis root microbiota journal May 2019
Plant traits related to nitrogen uptake influence plant-microbe competition journal August 2015
FLASH: fast length adjustment of short reads to improve genome assemblies journal September 2011
Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field journal October 2019
Changes in soil pore structure generated by the root systems of maize, sorghum and switchgrass affect in situ N2O emissions and bacterial denitrification journal August 2023
Identification of the Pr1 Gene Product Completes the Anthocyanin Biosynthesis Pathway of Maize journal May 2011
Nutrient Uptake, Partitioning, and Remobilization in Modern, Transgenic Insect‐Protected Maize Hybrids journal January 2013
QIIME allows analysis of high-throughput community sequencing data journal April 2010
A “more ammonium solution” to mitigate nitrogen pollution and boost crop yields journal May 2021
Large-scale replicated field study of maize rhizosphere identifies heritable microbes journal June 2018
The Nitrogen Adaptation Strategy of the Wild Teosinte Ancestor of Modern Maize, subsp. journal January 2011
Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation: Rhizosphere feedbacks in CO2-enriched forests journal December 2010
Effect of Sampling Frequency on Estimates of Cumulative Nitrous Oxide Emissions journal January 2008
Predation increases multiple components of microbial diversity in activated sludge communities journal December 2021
FUNCTION OF ROOT BORDER CELLS IN PLANT HEALTH: Pioneersin the Rhizosphere journal September 1998
The structure and function of the global citrus rhizosphere microbiome journal November 2018
A plant perspective on nitrogen cycling in the rhizosphere journal March 2019
Impacts of directed evolution and soil management legacy on the maize rhizobiome journal June 2020
Is plant evolutionary history impacting recruitment of diazotrophs and nifH expression in the rhizosphere? journal February 2016
The Impact of Genetic Changes during Crop Domestication journal July 2018
Nitrate leaching and nitrous oxide emissions from maize after grass-clover on a coarse sandy soil: Mitigation potentials of 3,4-dimethylpyrazole phosphate (DMPP) journal April 2020
Diversity and heritability of the maize rhizosphere microbiome under field conditions journal April 2013
Dynamic biochar effects on soil nitrous oxide emissions and underlying microbial processes during the maize growing season journal July 2018
Rhizosphere microbiome assemblage is affected by plant development journal November 2013
WGCNA: an R package for weighted correlation network analysis journal December 2008
Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis journal October 2017
Genome-wide Analysis of Transcriptional Variability in a Large Maize-Teosinte Population journal March 2018
The microbial nitrogen-cycling network journal February 2018
Biological nitrification inhibition in maize—isolation and identification of hydrophobic inhibitors from root exudates journal June 2021
Microfluidic Quantitative PCR for Simultaneous Quantification of Multiple Viruses in Environmental Water Samples journal September 2014
Extremophilic nitrite-oxidizing Chloroflexi from Yellowstone hot springs journal October 2019
Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome journal May 2021
Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil journal October 2019
Rewilding complex ecosystems journal April 2019
The causes of the selection of biological nitrification inhibition (BNI) in relation to ecosystem functioning and a research agenda to explore them journal March 2022
Enlisting wild grass genes to combat nitrification in wheat farming: A nature-based solution journal August 2021
Isolation and characterization of the hydrophilic BNI compound, 6-methoxy-2(3H)-benzoxazolone (MBOA), from maize roots journal April 2023
Maize plant contributions to root zone available carbon and microbial transformations of nitrogen journal September 1997
Revisiting plant biological nitrification inhibition efficiency using multiple archaeal and bacterial ammonia-oxidising cultures journal January 2021
Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites journal July 2014
Going back to the roots: the microbial ecology of the rhizosphere journal September 2013
Rewilding crops for climate resilience: economic analysis and de novo domestication strategies journal June 2021
Heterosis of leaf and rhizosphere microbiomes in field‐grown maize journal July 2020
Long Term Influence of Fertility and Rotation on Soil Nitrification Potential and Nitrifier Communities journal March 2022
Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils journal June 2003
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB journal July 2006
The plant microbiome: The dark and dirty secrets of plant growth journal November 2020
Antireduction: an ancient strategy fit for future journal August 2016
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997