Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar
Abstract
Domestication and breeding have affected interactions between plants and their microbiomes in ways that are only beginning to be understood but may have important implications for recruitment of rhizosphere microorganisms, particularly under stress conditions. We investigated the responses of a modern maize (Zea mays subsp. mays) cultivar and its wild relative, teosinte (Z. mays subsp. parviglumis), to different phosphate availabilities. We appraised responses of the plant-microbial holobiont to phosphate stresses by profiling root exudate metabolomes, and microbial communities in the root endosphere and rhizosphere. We also performed plate assays to quantify phosphate-solubilizing microorganisms from the rhizosphere. Although root exudate metabolite profiles were distinct between the teosinte and modern maize under high phosphate, both plants shifted exudate compositions in response to phosphate stress toward a common metabolite profile. Root and rhizosphere microbial communities also responded significantly to both plant type and the phosphate availability. A subset of bacterial and fungal taxa were differentially abundant under the different phosphate conditions, with each of the three conditions favoring different taxa. Both teosinte and maize rhizospheres harbored phosphate-solubilizing microorganisms under all growth conditions. These results suggest that the root exudation response to phosphate stress was conserved through the domestication of maize from teosinte, shiftingmore »
- Authors:
-
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- University of California, Davis, CA (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC); USDA; National Institute of Food and Agriculture (NIFA); Foundation for Food and Agriculture Research
- OSTI Identifier:
- 1860650
- Alternate Identifier(s):
- OSTI ID: 1923759
- Report Number(s):
- LLNL-JRNL-817896
Journal ID: ISSN 2471-2906; 1028119
- Grant/Contract Number:
- AC52-07NA27344; AC02-05CH11231; CA-D-PLS-2332-H
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Phytobiomes Journal
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2471-2906
- Publisher:
- American Phytopathological Society (APS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; maize; metabolomics; microbiome; phosphate-solubilizing microorganisms; phosphate stress; rhizosphere and phyllosphere; root exudates; teosinte; Zea mays
Citation Formats
Brisson, Vanessa L., Richardy, Jesper, Kosina, Suzanne M., Northen, Trent R., Vogel, John P., and Gaudin, Amélie M. Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar. United States: N. p., 2022.
Web. doi:10.1094/pbiomes-06-21-0041-r.
Brisson, Vanessa L., Richardy, Jesper, Kosina, Suzanne M., Northen, Trent R., Vogel, John P., & Gaudin, Amélie M. Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar. United States. https://doi.org/10.1094/pbiomes-06-21-0041-r
Brisson, Vanessa L., Richardy, Jesper, Kosina, Suzanne M., Northen, Trent R., Vogel, John P., and Gaudin, Amélie M. Mon .
"Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar". United States. https://doi.org/10.1094/pbiomes-06-21-0041-r. https://www.osti.gov/servlets/purl/1860650.
@article{osti_1860650,
title = {Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar},
author = {Brisson, Vanessa L. and Richardy, Jesper and Kosina, Suzanne M. and Northen, Trent R. and Vogel, John P. and Gaudin, Amélie M.},
abstractNote = {Domestication and breeding have affected interactions between plants and their microbiomes in ways that are only beginning to be understood but may have important implications for recruitment of rhizosphere microorganisms, particularly under stress conditions. We investigated the responses of a modern maize (Zea mays subsp. mays) cultivar and its wild relative, teosinte (Z. mays subsp. parviglumis), to different phosphate availabilities. We appraised responses of the plant-microbial holobiont to phosphate stresses by profiling root exudate metabolomes, and microbial communities in the root endosphere and rhizosphere. We also performed plate assays to quantify phosphate-solubilizing microorganisms from the rhizosphere. Although root exudate metabolite profiles were distinct between the teosinte and modern maize under high phosphate, both plants shifted exudate compositions in response to phosphate stress toward a common metabolite profile. Root and rhizosphere microbial communities also responded significantly to both plant type and the phosphate availability. A subset of bacterial and fungal taxa were differentially abundant under the different phosphate conditions, with each of the three conditions favoring different taxa. Both teosinte and maize rhizospheres harbored phosphate-solubilizing microorganisms under all growth conditions. These results suggest that the root exudation response to phosphate stress was conserved through the domestication of maize from teosinte, shifting exudation levels of specific metabolites. Although microbial communities also shifted, plate-based assays did not detect selective recruitment of phosphate solubilizers in response to phosphate availability.},
doi = {10.1094/pbiomes-06-21-0041-r},
journal = {Phytobiomes Journal},
number = 1,
volume = 6,
place = {United States},
year = {Mon Jan 24 00:00:00 EST 2022},
month = {Mon Jan 24 00:00:00 EST 2022}
}
Works referenced in this record:
Impacts of directed evolution and soil management legacy on the maize rhizobiome
journal, June 2020
- Schmidt, Jennifer E.; Mazza Rodrigues, Jorge L.; Brisson, Vanessa L.
- Soil Biology and Biochemistry, Vol. 145
Phosphate solubilizing bacteria and their role in plant growth promotion
journal, October 1999
- Rodrı́guez, Hilda; Fraga, Reynaldo
- Biotechnology Advances, Vol. 17, Issue 4-5
Associations between species and groups of sites: indices and statistical inference
journal, December 2009
- Cáceres, Miquel De; Legendre, Pierre
- Ecology, Vol. 90, Issue 12
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases
journal, July 2015
- Yao, Yushu; Sun, Terence; Wang, Tony
- Metabolites, Vol. 5, Issue 3
The evolution of apical dominance in maize
journal, April 1997
- Doebley, John; Stec, Adrian; Hubbard, Lauren
- Nature, Vol. 386, Issue 6624
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review
journal, January 2015
- Pii, Youry; Mimmo, Tanja; Tomasi, Nicola
- Biology and Fertility of Soils, Vol. 51, Issue 4
Symbiotic phosphate transport in arbuscular mycorrhizas
journal, January 2005
- Karandashov, Vladimir; Bucher, Marcel
- Trends in Plant Science, Vol. 10, Issue 1
Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes
journal, April 2019
- Zeffa, Douglas Mariani; Perini, Luiz Júnior; Silva, Mayara Barbosa
- PLOS ONE, Vol. 14, Issue 4
Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, December 2010
- Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
- Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1
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
An efficient microbiological growth medium for screening phosphate solubilizing microorganisms
journal, January 1999
- Nautiyal, C. Shekhar
- FEMS Microbiology Letters, Vol. 170, Issue 1
Has agricultural intensification impacted maize root traits and rhizosphere interactions related to organic N acquisition?
journal, June 2020
- Schmidt, Jennifer E.; Poret-Peterson, Amisha; Lowry, Carolyn J.
- AoB PLANTS, Vol. 12, Issue 4
Current knowledge and perspectives of Paenibacillus: a review
journal, December 2016
- Grady, Elliot Nicholas; MacDonald, Jacqueline; Liu, Linda
- Microbial Cell Factories, Vol. 15, Issue 1
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
Xanthomonas oryzae pathovars: model pathogens of a model crop
journal, September 2006
- NiÑO-Liu, David O.; Ronald, Pamela C.; Bogdanove, Adam J.
- Molecular Plant Pathology, Vol. 7, Issue 5
Dealing with the unknown: Metabolomics and Metabolite Atlases
journal, September 2010
- Bowen, Benjamin P.; Northen, Trent R.
- Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9
Corn growth and nitrogen nutrition after additions of biochars with varying properties to a temperate soil
journal, October 2011
- Rajkovich, Shelby; Enders, Akio; Hanley, Kelly
- Biology and Fertility of Soils, Vol. 48, Issue 3
Diverse traits for pathogen fitness in Gibberella zeae: This paper was a contribution to the symposium entitled Phytopathological Challenges, held during The Canadian Phytopathological Society Annual Meeting at Waterton Lakes National Park, Alta., June 2002.
journal, March 2003
- Desjardins, A. E.; Plattner, R. D.
- Canadian Journal of Plant Pathology, Vol. 25, Issue 1
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 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
Functional biology of plant phosphate uptake at root and mycorrhiza interfaces: Tansley review
journal, December 2006
- Bucher, Marcel
- New Phytologist, Vol. 173, Issue 1
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton
journal, June 2015
- Apprill, A.; McNally, S.; Parsons, R.
- Aquatic Microbial Ecology, Vol. 75, Issue 2
Phosphorus Stress-Induced Changes in Plant Root Exudation Could Potentially Facilitate Uranium Mobilization from Stable Mineral Forms
journal, May 2018
- Edayilam, Nimisha; Montgomery, Dawn; Ferguson, Brennan
- Environmental Science & Technology, Vol. 52, Issue 14
The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions
journal, September 2017
- Jacoby, Richard; Peukert, Manuela; Succurro, Antonella
- Frontiers in Plant Science, Vol. 8
Phosphate solubilization by Rhizobium strains
journal, March 2009
- Sridevi, M.; Mallaiah, K. V.
- Indian Journal of Microbiology, Vol. 49, Issue 1
A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system
journal, June 2012
- Barillot, Cindy D. C.; Sarde, Claude-Olivier; Bert, Valerie
- Annals of Microbiology, Vol. 63, Issue 2
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Long-Term Rock Phosphate Fertilization Impacts the Microbial Communities of Maize Rhizosphere
journal, July 2017
- Silva, Ubiana C.; Medeiros, Julliane D.; Leite, Laura R.
- Frontiers in Microbiology, Vol. 8
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
Mechanism of Absorption of Phosphate from Soil by Endogone Mycorrhizas
journal, September 1971
- Sanders, F. E.; Tinker, P. B.
- Nature, Vol. 233, Issue 5317
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
Alternaria spp.: from general saprophyte to specific parasite
journal, July 2003
- Thomma, Bart P. H. J.
- Molecular Plant Pathology, Vol. 4, Issue 4
Physiological and genetic analysis for maize root characters and yield in response to low phosphorus stress
journal, January 2018
- Liu, Zhigang; Liu, Xiangsheng; Craft, Eric J.
- Breeding Science, Vol. 68, Issue 2
Combined effects of biochar addition and nitrogen fertilizer reduction on the rhizosphere metabolomics of maize (Zea mays L.) seedlings
journal, September 2018
- Cheng, Nan; Peng, Yujie; Kong, Yanglu
- Plant and Soil, Vol. 433, Issue 1-2
Root-Associated Microbiome of Maize Genotypes with Contrasting Phosphorus Use Efficiency
journal, January 2018
- Gomes, Eliane A.; Lana, Ubiraci G. P.; Quensen, John F.
- Phytobiomes Journal, Vol. 2, Issue 3
Bioleaching of rare earth elements from monazite sand: Bioleaching of Rare Earth Elements from Monazite
journal, September 2015
- Brisson, Vanessa L.; Zhuang, Wei-Qin; Alvarez-Cohen, Lisa
- Biotechnology and Bioengineering, Vol. 113, Issue 2
A specialized metabolic network selectively modulates Arabidopsis root microbiota
journal, May 2019
- Huang, Ancheng C.; Jiang, Ting; Liu, Yong-Xin
- Science, Vol. 364, Issue 6440
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
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962
- Murashige, Toshio; Skoog, Folke
- Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497
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
Solubilization of Phosphates and Micronutrients by the Plant-Growth-Promoting and Biocontrol Fungus Trichoderma harzianum Rifai 1295-22
journal, July 1999
- Altomare, C.; Norvell, W. A.; Björkman, T.
- Applied and Environmental Microbiology, Vol. 65, Issue 7
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts
journal, April 1993
- Gardes, M.; Bruns, T. D.
- Molecular Ecology, Vol. 2, Issue 2
Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates
journal, July 2015
- Oteino, Nicholas; Lally, Richard D.; Kiwanuka, Samuel
- Frontiers in Microbiology, Vol. 6
Global maize production, utilization, and consumption: Maize production, utilization, and consumption
journal, March 2014
- Ranum, Peter; Peña-Rosas, Juan Pablo; Garcia-Casal, Maria Nieves
- Annals of the New York Academy of Sciences, Vol. 1312, Issue 1
Fusarium Pathogenomics
journal, September 2013
- Ma, Li-Jun; Geiser, David M.; Proctor, Robert H.
- Annual Review of Microbiology, Vol. 67, Issue 1
Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning: Phosphate and Petunia mycorrhiza development and functioning
journal, November 2010
- Breuillin, Florence; Schramm, Jonathan; Hajirezaei, Mohammad
- The Plant Journal, Vol. 64, Issue 6
Agriculture and the Disruption of Plant–Microbial Symbiosis
journal, May 2020
- Porter, Stephanie S.; Sachs, Joel L.
- Trends in Ecology & Evolution, Vol. 35, Issue 5
The combination of Arachis pintoi green manure and natural phosphate improves maize growth, soil microbial community structure and enzymatic activities
journal, November 2018
- de Medeiros, Erika Valente; Silva, Aline Oliveira; Duda, Gustavo Pereira
- Plant and Soil, Vol. 435, Issue 1-2
Massilia phosphatilytica sp. nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil
journal, August 2017
- Zheng, Bang-Xiao; Bi, Qing-Fang; Hao, Xiu-Li
- International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 8
Microbiome Datasets Are Compositional: And This Is Not Optional
journal, November 2017
- Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera
- Frontiers in Microbiology, Vol. 8
Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics
book, January 1990
- White, T. J.; Bruns, T.; Lee, S.
- PCR Protocols
Plant–microbiome interactions: from community assembly to plant health
journal, August 2020
- Trivedi, Pankaj; Leach, Jan E.; Tringe, Susannah G.
- Nature Reviews Microbiology, Vol. 18, Issue 11
Solubilization of insoluble phosphates by some soil fungi isolated from nursery seedbeds
journal, September 1970
- Agnihotri, V. P.
- Canadian Journal of Microbiology, Vol. 16, Issue 9
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species
journal, October 2015
- Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali
- New Phytologist, Vol. 209, Issue 2
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
The importance and ecology of yeasts in soil
journal, January 2011
- Botha, Alfred
- Soil Biology and Biochemistry, Vol. 43, Issue 1
Root microbiota drive direct integration of phosphate stress and immunity
journal, March 2017
- Castrillo, Gabriel; Teixeira, Paulo José Pereira Lima; Paredes, Sur Herrera
- Nature, Vol. 543, Issue 7646
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
Mortierella Species as the Plant Growth-Promoting Fungi Present in the Agricultural Soils
journal, December 2020
- Ozimek, Ewa; Hanaka, Agnieszka
- Agriculture, Vol. 11, Issue 1
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