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Title: Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks

Abstract

Plants may actively cultivate microorganisms in their roots and rhizosphere that enhance their nutrition. To develop cropping strategies that substitute mineral fertilizers for beneficial root symbioses, we must first understand how microbial communities associated with plant roots differ among plant taxa and how they respond to fertilization. Arbuscular mycorrhizal (AM) fungi and rhizobacteria are of particular interest because they enhance nutrient availability to plants and perform a suite of nutrient cycling functions. The purpose of this experiment is to examine the root and soil microbiome in a longterm switchgrass (Panicum virgatum) biofuel feedstock experiment and determine how AM fungi and rhizobacteria respond to plant diversity and soil fertility. We hypothesize that intra- and interspecific plant diversity, nitrogen fertilization (+N), and their interaction will influence the biomass and community composition of AM fungi and rhizobacteria. We further hypothesize that +N will reduce the abundance of nitrogenase-encoding nifH genes on the rhizoplane. Roots and soils were sampled from three switchgrass cultivars (Cave-in-Rock, Kanlow, Southlow) grown in monoculture, intraspecific mixture, and interspecific planting mixtures with either Andropogon gerardii or diverse native tallgrass prairie species. Molecular sequencing was performed on root and soil samples, fatty acid extractions were assessed to determine microbial biomass, andmore » quantitative polymerase chain reaction (qPCR) was performed on nifH genes from the rhizoplane. Sequence data determined core AM fungal and bacterial microbiomes and indicator taxa for plant diversity and +N treatments. We found that plant diversity and +N influenced AM fungal biomass and community structure. Across all plant diversity treatments, +N reduced the biomass of AM fungi and nifH gene abundance by more than 40%. The AM fungal genus Scutellospora was an indicator for +N, with relative abundance significantly greater under +N and in monoculture treatments. Community composition of rhizobacteria was influenced by plant diversity but not by +N. Verrucomicrobia and Proteobacteria were the dominant bacterial phyla in both roots and soils. Our findings provide evidence that soil fertility and plant diversity structure the root and soil microbiome. Optimization of soil communities for switchgrass production must take into account differences among cultivars and their unique responses to shifts in soil fertility.« less

Authors:
 [1];  [2];  [3];  [4];  [5]
  1. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences; Univ. of Miami, FL (United States). Dept. of Biology
  2. Oklahoma State Univ., Stillwater, OK (United States). Dept. of Natural Resource Ecology, Management
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Environmental Science Division
  4. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences
  5. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences and School of Earth, Sustainability
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States); Northern Arizona Univ., Flagstaff, AZ (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDA: National Institute of Food and Agriculture (NIFA)
OSTI Identifier:
1628295
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Plant sciences; soil microbiome; switchgrass; rhizobacteria; arbuscular mycorrhizal fungi; resource availability; plant–microbial interaction

Citation Formats

Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, and Johnson, Nancy Collins. Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks. United States: N. p., 2019. Web. https://doi.org/10.3389/fpls.2019.01018.
Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, & Johnson, Nancy Collins. Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks. United States. https://doi.org/10.3389/fpls.2019.01018
Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, and Johnson, Nancy Collins. Wed . "Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks". United States. https://doi.org/10.3389/fpls.2019.01018. https://www.osti.gov/servlets/purl/1628295.
@article{osti_1628295,
title = {Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks},
author = {Revillini, Daniel and Wilson, Gail W. T. and Miller, R. Michael and Lancione, Ryan and Johnson, Nancy Collins},
abstractNote = {Plants may actively cultivate microorganisms in their roots and rhizosphere that enhance their nutrition. To develop cropping strategies that substitute mineral fertilizers for beneficial root symbioses, we must first understand how microbial communities associated with plant roots differ among plant taxa and how they respond to fertilization. Arbuscular mycorrhizal (AM) fungi and rhizobacteria are of particular interest because they enhance nutrient availability to plants and perform a suite of nutrient cycling functions. The purpose of this experiment is to examine the root and soil microbiome in a longterm switchgrass (Panicum virgatum) biofuel feedstock experiment and determine how AM fungi and rhizobacteria respond to plant diversity and soil fertility. We hypothesize that intra- and interspecific plant diversity, nitrogen fertilization (+N), and their interaction will influence the biomass and community composition of AM fungi and rhizobacteria. We further hypothesize that +N will reduce the abundance of nitrogenase-encoding nifH genes on the rhizoplane. Roots and soils were sampled from three switchgrass cultivars (Cave-in-Rock, Kanlow, Southlow) grown in monoculture, intraspecific mixture, and interspecific planting mixtures with either Andropogon gerardii or diverse native tallgrass prairie species. Molecular sequencing was performed on root and soil samples, fatty acid extractions were assessed to determine microbial biomass, and quantitative polymerase chain reaction (qPCR) was performed on nifH genes from the rhizoplane. Sequence data determined core AM fungal and bacterial microbiomes and indicator taxa for plant diversity and +N treatments. We found that plant diversity and +N influenced AM fungal biomass and community structure. Across all plant diversity treatments, +N reduced the biomass of AM fungi and nifH gene abundance by more than 40%. The AM fungal genus Scutellospora was an indicator for +N, with relative abundance significantly greater under +N and in monoculture treatments. Community composition of rhizobacteria was influenced by plant diversity but not by +N. Verrucomicrobia and Proteobacteria were the dominant bacterial phyla in both roots and soils. Our findings provide evidence that soil fertility and plant diversity structure the root and soil microbiome. Optimization of soil communities for switchgrass production must take into account differences among cultivars and their unique responses to shifts in soil fertility.},
doi = {10.3389/fpls.2019.01018},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {United States},
year = {2019},
month = {8}
}

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Works referenced in this record:

Plant Growth-Promoting Rhizobacteria Allow Reduced Application Rates of Chemical Fertilizers
journal, May 2009


Effects of switchgrass cultivars and intraspecific differences in root structure on soil carbon inputs and accumulation
journal, January 2016


Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation
journal, January 2016


Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture
journal, June 2017

  • Alori, Elizabeth T.; Glick, Bernard R.; Babalola, Olubukola O.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00971

A new method for non-parametric multivariate analysis of variance
journal, February 2001


Nutrient cycling in the mycorrhizosphere
journal, January 2015


Regulation and function of root exudates
journal, June 2009


Diversity of Nitrogen-Fixing Bacteria Associated with Switchgrass in the Native Tallgrass Prairie of Northern Oklahoma
journal, July 2014

  • Bahulikar, Rahul A.; Torres-Jerez, Ivone; Worley, Eric
  • Applied and Environmental Microbiology, Vol. 80, Issue 18
  • DOI: 10.1128/AEM.02091-14

The Soil-Borne Legacy
journal, March 2018


Belowground biodiversity and ecosystem functioning
journal, November 2014

  • Bardgett, Richard D.; van der Putten, Wim H.
  • Nature, Vol. 515, Issue 7528
  • DOI: 10.1038/nature13855

Examining the global distribution of dominant archaeal populations in soil
journal, November 2010

  • Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory
  • The ISME Journal, Vol. 5, Issue 5
  • DOI: 10.1038/ismej.2010.171

Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities
journal, June 2012


An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability
journal, June 2016

  • Bender, S. Franz; Wagg, Cameron; van der Heijden, Marcel G. A.
  • Trends in Ecology & Evolution, Vol. 31, Issue 6
  • DOI: 10.1016/j.tree.2016.02.016

Unraveling the plant microbiome: looking back and future perspectives
journal, June 2014


The under-recognized dominance of Verrucomicrobia in soil bacterial communities
journal, July 2011


Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism
journal, January 2009


Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
journal, December 2012

  • Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
  • Nature Methods, Vol. 10, Issue 1
  • DOI: 10.1038/nmeth.2276

Molecular breeding of switchgrass for use as a biofuel crop
journal, December 2007


Evaluation of Switchgrass Rhizosphere Microflora for Enhancing Seedling Yield and Nutrient Uptake
journal, March 1907


Research priorities for harnessing plant microbiomes in sustainable agriculture
journal, March 2017


PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Associations between species and groups of sites: indices and statistical inference
journal, December 2009

  • Cáceres, Miquel De; Legendre, Pierre
  • Ecology, Vol. 90, Issue 12
  • DOI: 10.1890/08-1823.1

Improving indicator species analysis by combining groups of sites
journal, September 2010


Fungal/bacterial ratios in grasslands with contrasting nitrogen management
journal, August 2006


Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing
journal, February 2011


Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands
journal, November 2007

  • Egerton-Warburton, Louise M.; Johnson, Nancy Collins; Allen, Edith B.
  • Ecological Monographs, Vol. 77, Issue 4
  • DOI: 10.1890/06-1772.1

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013


Global patterns in belowground communities
journal, November 2009


The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil
journal, April 1996

  • Frostega�rd, A.; Ba�a�th, E.
  • Biology and Fertility of Soils, Vol. 22, Issue 1
  • DOI: 10.1007/s003740050076

Use and misuse of PLFA measurements in soils
journal, August 2011


A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase
journal, July 2012


Current understanding of the human microbiome
journal, April 2018

  • Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
  • Nature Medicine, Vol. 24, Issue 4
  • DOI: 10.1038/nm.4517

The Earth Microbiome project: successes and aspirations
journal, August 2014


Identifying the Active Microbiome Associated with Roots and Rhizosphere Soil of Oilseed Rape
journal, September 2017

  • Gkarmiri, Konstantia; Mahmood, Shahid; Ekblad, Alf
  • Applied and Environmental Microbiology, Vol. 83, Issue 22
  • DOI: 10.1128/AEM.01938-17

Nitrogen transfer in the arbuscular mycorrhizal symbiosis
journal, June 2005

  • Govindarajulu, Manjula; Pfeffer, Philip E.; Jin, Hairu
  • Nature, Vol. 435, Issue 7043
  • DOI: 10.1038/nature03610

Multiple Climate Change Factors Interact to Alter Soil Microbial Community Structure in an Old-Field Ecosystem
journal, January 2011

  • Gray, Sharon B.; Classen, Aimée T.; Kardol, Paul
  • Soil Science Society of America Journal, Vol. 75, Issue 6
  • DOI: 10.2136/sssaj2011.0135

Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture
journal, June 2017

  • Hannula, S. Emilia; Morriën, Elly; de Hollander, Mattias
  • The ISME Journal, Vol. 11, Issue 10
  • DOI: 10.1038/ismej.2017.90

Microbe management: application of mycorrhyzal fungi in sustainable agriculture
journal, December 2005


Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems
journal, June 2014


A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi
journal, March 2010


The economic value of grassland species for carbon storage
journal, April 2017

  • Hungate, Bruce A.; Barbier, Edward B.; Ando, Amy W.
  • Science Advances, Vol. 3, Issue 4
  • DOI: 10.1126/sciadv.1601880

N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses
journal, January 2018


Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture
journal, April 2004


Can Fertilization of Soil Select Less Mutualistic Mycorrhizae?
journal, November 1993

  • Johnson, Nancy Collins
  • Ecological Applications, Vol. 3, Issue 4
  • DOI: 10.2307/1942106

Nitrogen Enrichment Alters Mycorrhizal Allocation at five Mesic to Semiarid Grasslands
journal, July 2003


Resource limitation is a driver of local adaptation in mycorrhizal symbioses
journal, January 2010

  • Johnson, N. C.; Wilson, G. W. T.; Bowker, M. A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
  • DOI: 10.1073/pnas.0906710107

Mycorrhizal phenotypes and the Law of the Minimum
journal, November 2014

  • Johnson, Nancy Collins; Wilson, Gail W. T.; Wilson, Jacqueline A.
  • New Phytologist, Vol. 205, Issue 4
  • DOI: 10.1111/nph.13172

Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition
journal, June 2003


Mycorrhizae: Possible Explanation for Yield Decline with Continuous Corn and Soybean
journal, January 1992


Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms
journal, December 2008


Host sanctions and the legume–rhizobium mutualism
journal, September 2003

  • Kiers, E. Toby; Rousseau, Robert A.; West, Stuart A.
  • Nature, Vol. 425, Issue 6953
  • DOI: 10.1038/nature01931

Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis
journal, August 2011


The interactive effects of plant microbial symbionts: a review and meta-analysis
journal, September 2010


Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi: PCR primers for arbuscular mycorrhizal fungi
journal, August 2008


Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems
journal, August 2014


UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


Plant-Growth-Promoting Rhizobacteria
journal, October 2009


Swarm: robust and fast clustering method for amplicon-based studies
journal, January 2014

  • Mahé, Frédéric; Rognes, Torbjørn; Quince, Christopher
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.593

Native Perennial Grassland Species for Bioenergy: Establishment and Biomass Productivity
journal, January 2011

  • Mangan, Margaret E.; Sheaffer, Craig; Wyse, Donald L.
  • Agronomy Journal, Vol. 103, Issue 2
  • DOI: 10.2134/agronj2010.0360

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015


An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011

  • McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
  • The ISME Journal, Vol. 6, Issue 3
  • DOI: 10.1038/ismej.2011.139

Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant
journal, December 1984


Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes
journal, October 2015

  • Moore, Jessica A. M.; Jiang, Jiang; Patterson, Courtney M.
  • Journal of Ecology, Vol. 103, Issue 6, p. 1442-1453
  • DOI: 10.1111/1365-2745.12484

Genotypic diversity effects on biomass production in native perennial bioenergy cropping systems
journal, January 2016

  • Morris, Geoffrey P.; Hu, Zhenbin; Grabowski, Paul P.
  • GCB Bioenergy, Vol. 8, Issue 5
  • DOI: 10.1111/gcbb.12309

The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling
journal, November 2008


Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization
journal, October 2016

  • Oates, Lawrence G.; Duncan, David S.; Sanford, Gregg R.
  • Agriculture, Ecosystems & Environment, Vol. 233
  • DOI: 10.1016/j.agee.2016.09.008

The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil
journal, May 1995


The Biology and Agronomy of Switchgrass for Biofuels
journal, September 2005


Differential abundance analysis for microbial marker-gene surveys
journal, September 2013

  • Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
  • Nature Methods, Vol. 10, Issue 12
  • DOI: 10.1038/nmeth.2658

The ecological coherence of high bacterial taxonomic ranks
journal, June 2010

  • Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J.
  • Nature Reviews Microbiology, Vol. 8, Issue 7
  • DOI: 10.1038/nrmicro2367

FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

  • Price, M. N.; Dehal, P. S.; Arkin, A. P.
  • Molecular Biology and Evolution, Vol. 26, Issue 7
  • DOI: 10.1093/molbev/msp077

Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide
journal, November 2014

  • Prober, Suzanne M.; Leff, Jonathan W.; Bates, Scott T.
  • Ecology Letters, Vol. 18, Issue 1
  • DOI: 10.1111/ele.12381

Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply
journal, May 2016

  • Püschel, David; Janoušková, Martina; Hujslová, Martina
  • Ecology and Evolution, Vol. 6, Issue 13
  • DOI: 10.1002/ece3.2207

Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012


Functional Ecology of Free-Living Nitrogen Fixation: A Contemporary Perspective
journal, December 2011


The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems
journal, April 2016

  • Revillini, Daniel; Gehring, Catherine A.; Johnson, Nancy Collins
  • Functional Ecology, Vol. 30, Issue 7
  • DOI: 10.1111/1365-2435.12668

Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture
journal, May 2005


Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis
journal, March 2017

  • Rubin, Rachel L.; van Groenigen, Kees Jan; Hungate, Bruce A.
  • Plant and Soil, Vol. 416, Issue 1-2
  • DOI: 10.1007/s11104-017-3199-8

Use of specific phospholipid fatty acids for identifying and quantifying the external hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea
journal, November 2004


The Plant Microbiome at Work
journal, March 2015


Fungal diversity regulates plant-soil feedbacks in temperate grassland
journal, November 2018

  • Semchenko, Marina; Leff, Jonathan W.; Lozano, Yudi M.
  • Science Advances, Vol. 4, Issue 11
  • DOI: 10.1126/sciadv.aau4578

Comparison of biochemical and microscopic methods for quantification of arbuscular mycorrhizal fungi in soil and roots
journal, November 2015


Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio
journal, March 2017


Plant compartment and genetic variation drive microbiome composition in switchgrass roots
journal, January 2019

  • Singer, Esther; Bonnette, Jason; Kenaley, Shawn C.
  • Environmental Microbiology Reports, Vol. 11, Issue 2
  • DOI: 10.1111/1758-2229.12727

Plant community composition influences fine root production and biomass allocation in perennial bioenergy cropping systems of the upper Midwest, USA
journal, October 2017


Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications
journal, September 2010


Carbon-Negative Biofuels from Low-Input High-Diversity Grassland Biomass
journal, December 2006


Core microbiomes for sustainable agroecosystems
journal, April 2018


The Phyllosphere: Microbial Jungle at the Plant–Climate Interface
journal, November 2016


A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment
journal, July 2015

  • van der Heijden, Marcel GA; Bruin, Susanne de; Luckerhoff, Ludo
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.120

Plant-soil feedbacks: the past, the present and future challenges
journal, February 2013

  • van der Putten, Wim H.; Bardgett, Richard D.; Bever, James D.
  • Journal of Ecology, Vol. 101, Issue 2
  • DOI: 10.1111/1365-2745.12054

The importance of the microbiome of the plant holobiont
journal, February 2015

  • Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13312

Mycorrhizal fungi associated with high soil N:P ratios are more likely to be lost upon conversion from grasslands to arable agriculture
journal, July 2015


The influence of biotic interactions on soil biodiversity
journal, July 2006


Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems
journal, October 2013

  • Wei, Cunzheng; Yu, Qiang; Bai, Edith
  • Global Change Biology, Vol. 19, Issue 12
  • DOI: 10.1111/gcb.12348

Aboveground productivity and root–shoot allocation differ between native and introduced grass species
journal, August 2006


Switchgrass selection as a “model” bioenergy crop: A history of the process
journal, June 2010


Sustainable intensification of high-diversity biomass production for optimal biofuel benefits
journal, November 2018


Nitrogenase gene diversity and microbial community structure: a cross-system comparison
journal, July 2003


Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist
journal, September 2014

  • Zheng, Chaoyuan; Ji, Baoming; Zhang, Junling
  • New Phytologist, Vol. 205, Issue 1
  • DOI: 10.1111/nph.13025

Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland
journal, December 2015


Compositional and Functional Shifts in Microbial Communities Due to Soil Warming
journal, January 1997