Impacts of directed evolution and soil management legacy on the maize rhizobiome
Abstract
Domestication and agricultural intensification dramatically altered maize and its cultivation environment. Changes in maize genetics (G) and environmental (E) conditions increased productivity under high-synthetic-input conditions. However, novel selective pressures on the rhizobiome may have incurred undesirable tradeoffs in organic agroecosystems, where plants obtain nutrients via microbially mediated processes including mineralization of organic matter. Using twelve maize genotypes representing an evolutionary transect (teosintes, landraces, inbred parents of modern elite germplasm, and modern hybrids) and two agricultural soils with contrasting long-term management, here we integrated analyses of rhizobiome community structure, potential microbe-microbe interactions, and N-cycling functional genes to better understand the impacts of maize evolution and soil management legacy on rhizobiome recruitment. We show complex shifts in rhizobiome communities during directed evolution of maize (defined as the transition from teosinte to modern hybrids), with a larger effect of domestication (teosinte to landraces) than modern breeding (inbreds to hybrids) on rhizobiome structure and greater impacts of modern breeding on potential microbe-microbe interactions. Rhizobiome structure was significantly correlated with plant nutrient composition. Furthermore, plant biomass and nutrient content were affected by G x E interactions in which teosinte and landrace genotypes had better relative performance in the organic legacy soil than inbred and modernmore »
- Authors:
-
- Univ. of California, Davis, CA (United States). Dept. of Plant Sciences
- Univ. of California, Davis, CA (United States). Dept. of Land, Air, and Water Resources
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Univ. of Illinois at Urbana-Champaign, IL (United States). Dept. of Natural Resources and Environmental Sciences
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); USDA
- OSTI Identifier:
- 1635192
- Grant/Contract Number:
- AC02-05CH11231; CA-D-PLS-2332-H
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 145; Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; agroecosystem; breeding; domestication; genotype-by-environment interaction; maize; rhizosphere
Citation Formats
Schmidt, Jennifer E., Mazza Rodrigues, Jorge L., Brisson, Vanessa L., Kent, Angela, and Gaudin, Amélie C. M. Impacts of directed evolution and soil management legacy on the maize rhizobiome. United States: N. p., 2020.
Web. doi:10.1016/j.soilbio.2020.107794.
Schmidt, Jennifer E., Mazza Rodrigues, Jorge L., Brisson, Vanessa L., Kent, Angela, & Gaudin, Amélie C. M. Impacts of directed evolution and soil management legacy on the maize rhizobiome. United States. https://doi.org/10.1016/j.soilbio.2020.107794
Schmidt, Jennifer E., Mazza Rodrigues, Jorge L., Brisson, Vanessa L., Kent, Angela, and Gaudin, Amélie C. M. Fri .
"Impacts of directed evolution and soil management legacy on the maize rhizobiome". United States. https://doi.org/10.1016/j.soilbio.2020.107794. https://www.osti.gov/servlets/purl/1635192.
@article{osti_1635192,
title = {Impacts of directed evolution and soil management legacy on the maize rhizobiome},
author = {Schmidt, Jennifer E. and Mazza Rodrigues, Jorge L. and Brisson, Vanessa L. and Kent, Angela and Gaudin, Amélie C. M.},
abstractNote = {Domestication and agricultural intensification dramatically altered maize and its cultivation environment. Changes in maize genetics (G) and environmental (E) conditions increased productivity under high-synthetic-input conditions. However, novel selective pressures on the rhizobiome may have incurred undesirable tradeoffs in organic agroecosystems, where plants obtain nutrients via microbially mediated processes including mineralization of organic matter. Using twelve maize genotypes representing an evolutionary transect (teosintes, landraces, inbred parents of modern elite germplasm, and modern hybrids) and two agricultural soils with contrasting long-term management, here we integrated analyses of rhizobiome community structure, potential microbe-microbe interactions, and N-cycling functional genes to better understand the impacts of maize evolution and soil management legacy on rhizobiome recruitment. We show complex shifts in rhizobiome communities during directed evolution of maize (defined as the transition from teosinte to modern hybrids), with a larger effect of domestication (teosinte to landraces) than modern breeding (inbreds to hybrids) on rhizobiome structure and greater impacts of modern breeding on potential microbe-microbe interactions. Rhizobiome structure was significantly correlated with plant nutrient composition. Furthermore, plant biomass and nutrient content were affected by G x E interactions in which teosinte and landrace genotypes had better relative performance in the organic legacy soil than inbred and modern genotypes. The abundance of six N-cycling genes of relevance for plant nutrition and N loss pathways did not significantly differ between teosinte and modern rhizospheres in either soil management legacy. These results provide insight into the potential for improving maize adaptation to organic systems and contribute to interdisciplinary efforts toward developing resource-efficient, biologically based agroecosystems.},
doi = {10.1016/j.soilbio.2020.107794},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 145,
place = {United States},
year = {Fri Apr 10 00:00:00 EDT 2020},
month = {Fri Apr 10 00:00:00 EDT 2020}
}
Web of Science
Works referenced in this record:
Making a microbiome: the many determinants of host-associated microbial community composition
journal, February 2017
- Adair, Karen L.; Douglas, Angela E.
- Current Opinion in Microbiology, Vol. 35
Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities
journal, December 2010
- Aira, Manuel; Gómez-Brandón, María; Lazcano, Cristina
- Soil Biology and Biochemistry, Vol. 42, Issue 12
Fungal diversity notes 111–252—taxonomic and phylogenetic contributions to fungal taxa
journal, November 2015
- Ariyawansa, Hiran A.; Hyde, Kevin D.; Jayasiri, Subashini C.
- Fungal Diversity, Vol. 75, Issue 1
Host and Microbiome Genome-Wide Association Studies: Current State and Challenges
journal, January 2019
- Awany, Denis; Allali, Imane; Dalvie, Shareefa
- Frontiers in Genetics, Vol. 9
Regulation and function of root exudates
journal, June 2009
- Badri, Dayakar V.; Vivanco, Jorge M.
- Plant, Cell & Environment, Vol. 32, Issue 6
Deciphering microbial interactions and detecting keystone species with co-occurrence networks
journal, May 2014
- Berry, David; Widder, Stefanie
- Frontiers in Microbiology, Vol. 5
Is diversification history of maize influencing selection of soil bacteria by roots?
journal, November 2011
- Bouffaud, Marie‐Lara; KyselkovÁ, Martina; Gouesnard, Brigitte
- Molecular Ecology, Vol. 21, Issue 1
A New Method to Correct for Habitat Filtering in Microbial Correlation Networks
journal, March 2019
- Brisson, Vanessa; Schmidt, Jennifer; Northen, Trent R.
- Frontiers in Microbiology, Vol. 10
Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil
journal, October 2019
- Brisson, Vanessa L.; Schmidt, Jennifer E.; Northen, Trent R.
- Scientific Reports, Vol. 9, Issue 1
Phenotypic Diversity of Root Anatomical and Architectural Traits in Zea Species
journal, May 2013
- Burton, Amy L.; Brown, Kathleen M.; Lynch, Jonathan P.
- Crop Science, Vol. 53, Issue 3
DADA2: High-resolution sample inference from Illumina amplicon data
journal, May 2016
- Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J.
- Nature Methods, Vol. 13, Issue 7
Historical nitrogen fertilizer use in agricultural ecosystems of the contiguous United States during 1850–2015: application rate, timing, and fertilizer types
journal, January 2018
- Cao, Peiyu; Lu, Chaoqun; Yu, Zhen
- Earth System Science Data, Vol. 10, Issue 2
Effect of twenty four wheat genotypes on soil biochemical and microbial properties
journal, February 2016
- Corneo, Paola E.; Suenaga, Haruna; Kertesz, Michael A.
- Plant and Soil, Vol. 404, Issue 1-2
The ecology of the microbiome: Networks, competition, and stability
journal, November 2015
- Coyte, K. Z.; Schluter, J.; Foster, K. R.
- Science, Vol. 350, Issue 6261
The origin and evolution of maize in the Southwestern United States
journal, January 2015
- da Fonseca, Rute R.; Smith, Bruce D.; Wales, Nathan
- Nature Plants, Vol. 1, Issue 1
Associations between species and groups of sites: indices and statistical inference
journal, December 2009
- Cáceres, Miquel De; Legendre, Pierre
- Ecology, Vol. 90, Issue 12
Engineering the Rhizosphere
journal, March 2016
- Dessaux, Yves; Grandclément, Catherine; Faure, Denis
- Trends in Plant Science, Vol. 21, Issue 3
Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015
- Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
Eighty years of maize breeding alters plant nitrogen acquisition but not rhizosphere bacterial community composition
journal, July 2018
- Emmett, Bryan D.; Buckley, Daniel H.; Smith, Margaret E.
- Plant and Soil, Vol. 431, Issue 1-2
Investigation of the bottleneck leading to the domestication of maize
journal, April 1998
- Eyre-Walker, A.; Gaut, R. L.; Hilton, H.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 8
Microbial interactions: from networks to models
journal, July 2012
- Faust, Karoline; Raes, Jeroen
- Nature Reviews Microbiology, Vol. 10, Issue 8
Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize
journal, August 2019
- Galindo‐Castañeda, Tania; Brown, Kathleen M.; Kuldau, Gretchen A.
- Plant, Cell & Environment, Vol. 42, Issue 11
Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia
journal, July 2018
- Garrido-Oter, Ruben; Nakano, Ryohei Thomas; Dombrowski, Nina
- Cell Host & Microbe, Vol. 24, Issue 1
The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize
journal, January 2014
- Gaudin, Amelie CM; McClymont, Sarah A.; Soliman, Sameh SM
- BMC Genetics, Vol. 15, Issue 1
Using wild relatives to improve maize
journal, August 2019
- Hake, Sarah; Richardson, Annis
- Science, Vol. 365, Issue 6454
Corrigendum to “Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR” [J. Microbiol. Methods 59 (2004) 327–335]
journal, May 2005
- Henry, Sonia; Baudoin, Ezékiel; López-Gutiérrez, Juan C.
- Journal of Microbiological Methods, Vol. 61, Issue 2
Quantitative Detection of the nosZ Gene, Encoding Nitrous Oxide Reductase, and Comparison of the Abundances of 16S rRNA, narG, nirK, and nosZ Genes in Soils
journal, August 2006
- Henry, S.; Bru, D.; Stres, B.
- Applied and Environmental Microbiology, Vol. 72, Issue 8
Digestion of plant tissue for analysis by ICP emission spectroscopy
journal, September 1985
- Huang, Chao‐Yong Luh; Schulte, E. E.
- Communications in Soil Science and Plant Analysis, Vol. 16, Issue 9
Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.)
journal, December 2017
- Iannucci, Anna; Fragasso, Mariagiovanna; Beleggia, Romina
- Frontiers in Plant Science, Vol. 8
Microfluidic Quantitative PCR for Simultaneous Quantification of Multiple Viruses in Environmental Water Samples
journal, September 2014
- Ishii, Satoshi; Kitamura, Gaku; Segawa, Takahiro
- Applied and Environmental Microbiology, Vol. 80, Issue 24
Abundance of narG, nirS, nirK, and nosZ Genes of Denitrifying Bacteria during Primary Successions of a Glacier Foreland
journal, September 2006
- Kandeler, E.; Deiglmayr, K.; Tscherko, D.
- Applied and Environmental Microbiology, Vol. 72, Issue 9
Mediating mutualisms: farm management practices and evolutionary changes in symbiont co-operation: Mediating mutualisms
journal, October 2002
- Kiers, E. Toby; West, Stuart A.; Denison, R. Ford
- Journal of Applied Ecology, Vol. 39, Issue 5
Towards a unified paradigm for sequence-based identification of fungi
journal, September 2013
- Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy
- Molecular Ecology, Vol. 22, Issue 21
Disentangling Interactions in the Microbiome: A Network Perspective
journal, March 2017
- Layeghifard, Mehdi; Hwang, David M.; Guttman, David S.
- Trends in Microbiology, Vol. 25, Issue 3
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Soil Microbiome Is More Heterogeneous in Organic Than in Conventional Farming System
journal, January 2017
- Lupatini, Manoeli; Korthals, Gerard W.; de Hollander, Mattias
- Frontiers in Microbiology, Vol. 7
Soil Fertility and Biodiversity in Organic Farming
journal, May 2002
- Mader, P.
- Science, Vol. 296, Issue 5573
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Plant health: feedback effect of root exudates-rhizobiome interactions
journal, December 2018
- Olanrewaju, Oluwaseyi Samuel; Ayangbenro, Ayansina Segun; Glick, Bernard R.
- Applied Microbiology and Biotechnology, Vol. 103, Issue 3
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies
journal, October 2015
- Parada, Alma E.; Needham, David M.; Fuhrman, Jed A.
- Environmental Microbiology, Vol. 18, Issue 5
Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013
- Peiffer, J. A.; Spor, A.; Koren, O.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
Impact of plant domestication on rhizosphere microbiome assembly and functions
journal, June 2015
- Pérez-Jaramillo, Juan E.; Mendes, Rodrigo; Raaijmakers, Jos M.
- Plant Molecular Biology, Vol. 90, Issue 6
Comparison of nifH Gene Pools in Soils and Soil Microenvironments with Contrasting Properties
journal, May 2001
- Poly, F.; Ranjard, L.; Nazaret, S.
- Applied and Environmental Microbiology, Vol. 67, Issue 5
Rhizosphere engineering and management for sustainable agriculture
journal, May 2009
- Ryan, Peter R.; Dessaux, Yves; Thomashow, Linda S.
- Plant and Soil, Vol. 321, Issue 1-2
Using Ancient Traits to Convert Soil Health into Crop Yield: Impact of Selection on Maize Root and Rhizosphere Function
journal, March 2016
- Schmidt, Jennifer E.; Bowles, Timothy M.; Gaudin, Amélie C. M.
- Frontiers in Plant Science, Vol. 7
Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling
journal, November 2019
- Schmidt, Jennifer E.; Kent, Angela D.; Brisson, Vanessa L.
- Microbiome, Vol. 7, Issue 1
A tribute to Claude Shannon (1916-2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon-Wiener’ Index
journal, April 2003
- Spellerberg, Ian F.; Fedor, Peter J.
- Global Ecology and Biogeography, Vol. 12, Issue 3
Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars
journal, January 2015
- Szoboszlay, Márton; Lambers, Julie; Chappell, Janet
- Soil Biology and Biochemistry, Vol. 80
Role of root microbiota in plant productivity
journal, April 2015
- Tkacz, A.; Poole, P.
- Journal of Experimental Botany, Vol. 66, Issue 8
Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms
journal, May 2008
- Tourna, Maria; Freitag, Thomas E.; Nicol, Graeme W.
- Environmental Microbiology, Vol. 10, Issue 5, p. 1357-1364
Conservation of species interaction networks
journal, October 2010
- Tylianakis, Jason M.; Laliberté, Etienne; Nielsen, Anders
- Biological Conservation, Vol. 143, Issue 10
Beyond species loss: the extinction of ecological interactions in a changing world
journal, November 2014
- Valiente‐Banuet, Alfonso; Aizen, Marcelo A.; Alcántara, Julio M.
- Functional Ecology, Vol. 29, Issue 3
The importance of the microbiome of the plant holobiont
journal, February 2015
- Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie
- New Phytologist, Vol. 206, Issue 4
Population structure and genetic diversity of New World maize races assessed by DNA microsatellites
journal, September 2008
- Vigouroux, Y.; Glaubitz, J. C.; Matsuoka, Y.
- American Journal of Botany, Vol. 95, Issue 10
Large-scale replicated field study of maize rhizosphere identifies heritable microbes
journal, June 2018
- Walters, William A.; Jin, Zhao; Youngblut, Nicholas
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River
journal, October 2016
- Wang, Wenhui; Wang, Hui; Feng, Youzhi
- Scientific Reports, Vol. 6, Issue 1
Normalization and microbial differential abundance strategies depend upon data characteristics
journal, March 2017
- Weiss, Sophie; Xu, Zhenjiang Zech; Peddada, Shyamal
- Microbiome, Vol. 5, Issue 1
Novel approaches in plant breeding for rhizosphere-related traits
journal, July 2008
- Wissuwa, Matthias; Mazzola, Mark; Picard, Christine
- Plant and Soil, Vol. 321, Issue 1-2
The century experiment: the first twenty years of UC Davis' Mediterranean agroecological experiment
journal, January 2018
- Wolf, Kristina M.; Torbert, Emma E.; Bryant, Dennis
- Ecology, Vol. 99, Issue 2
The genetic architecture of teosinte catalyzed and constrained maize domestication
journal, March 2019
- Yang, Chin Jian; Samayoa, Luis Fernando; Bradbury, Peter J.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 12
Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress
journal, March 2015
- York, L. M.; Galindo-Castaneda, T.; Schussler, J. R.
- Journal of Experimental Botany, Vol. 66, Issue 8