Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar

Brisson, Vanessa L.; Richardy, Jesper; Kosina, Suzanne M.; Northen, Trent R.; Vogel, John P.; Gaudin, Amélie M.

doi:10.1094/pbiomes-06-21-0041-r

Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar

Journal Article · Mon Jan 24 04:00:00 EST 2022 · Phytobiomes Journal

DOI:https://doi.org/10.1094/pbiomes-06-21-0041-r· OSTI ID:1860650

^[1]; Richardy, Jesper ^[2]; Kosina, Suzanne M. ^[3]; Northen, Trent R. ^[4]; Vogel, John P. ^[5]; Gaudin, Amélie M. ^[2]

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)

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.

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Research Organization:: 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 Organization:: 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

Grant/Contract Number:: AC52-07NA27344; AC02-05CH11231

OSTI ID:: 1860650

Alternate ID(s):: OSTI ID: 1923759

Report Number(s):: LLNL-JRNL-817896; 1028119

Journal Information:: Phytobiomes Journal, Journal Name: Phytobiomes Journal Journal Issue: 1 Vol. 6; ISSN 2471-2906

Publisher:: American Phytopathological Society (APS)Copyright Statement

Country of Publication:: United States

Language:: English

References (64)

Bioleaching of rare earth elements from monazite sand: Bioleaching of Rare Earth Elements from Monazite Brisson, Vanessa L.; Zhuang, Wei-Qin; Alvarez-Cohen, Lisa Biotechnology and Bioengineering, Vol. 113, Issue 2 https://doi.org/10.1002/bit.25823	journal	September 2015
Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1 https://doi.org/10.1002/jpln.201000085	journal	December 2010
Corn growth and nitrogen nutrition after additions of biochars with varying properties to a temperate soil Rajkovich, Shelby; Enders, Akio; Hanley, Kelly Biology and Fertility of Soils, Vol. 48, Issue 3 https://doi.org/10.1007/s00374-011-0624-7	journal	October 2011
Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review Pii, Youry; Mimmo, Tanja; Tomasi, Nicola Biology and Fertility of Soils, Vol. 51, Issue 4 https://doi.org/10.1007/s00374-015-0996-1	journal	January 2015
Impact of plant domestication on rhizosphere microbiome assembly and functions Pérez-Jaramillo, Juan E.; Mendes, Rodrigo; Raaijmakers, Jos M. Plant Molecular Biology, Vol. 90, Issue 6 https://doi.org/10.1007/s11103-015-0337-7	journal	June 2015
Eighty years of maize breeding alters plant nitrogen acquisition but not rhizosphere bacterial community composition Emmett, Bryan D.; Buckley, Daniel H.; Smith, Margaret E. Plant and Soil, Vol. 431, Issue 1-2 https://doi.org/10.1007/s11104-018-3744-0	journal	July 2018
Combined effects of biochar addition and nitrogen fertilizer reduction on the rhizosphere metabolomics of maize (Zea mays L.) seedlings Cheng, Nan; Peng, Yujie; Kong, Yanglu Plant and Soil, Vol. 433, Issue 1-2 https://doi.org/10.1007/s11104-018-3811-6	journal	September 2018
The combination of Arachis pintoi green manure and natural phosphate improves maize growth, soil microbial community structure and enzymatic activities de Medeiros, Erika Valente; Silva, Aline Oliveira; Duda, Gustavo Pereira Plant and Soil, Vol. 435, Issue 1-2 https://doi.org/10.1007/s11104-018-3887-z	journal	November 2018
Phosphate solubilization by Rhizobium strains Sridevi, M.; Mallaiah, K. V. Indian Journal of Microbiology, Vol. 49, Issue 1 https://doi.org/10.1007/s12088-009-0005-1	journal	March 2009
A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system Barillot, Cindy D. C.; Sarde, Claude-Olivier; Bert, Valerie Annals of Microbiology, Vol. 63, Issue 2 https://doi.org/10.1007/s13213-012-0491-y	journal	June 2012
Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics White, T. J.; Bruns, T.; Lee, S. PCR Protocols https://doi.org/10.1016/B978-0-12-372180-8.50042-1	book	January 1990
Phosphate solubilizing bacteria and their role in plant growth promotion Rodrı́guez, Hilda; Fraga, Reynaldo Biotechnology Advances, Vol. 17, Issue 4-5 https://doi.org/10.1016/S0734-9750(99)00014-2	journal	October 1999
Dealing with the unknown: Metabolomics and Metabolite Atlases Bowen, Benjamin P.; Northen, Trent R. Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9 https://doi.org/10.1016/j.jasms.2010.04.003	journal	September 2010
The importance and ecology of yeasts in soil Botha, Alfred Soil Biology and Biochemistry, Vol. 43, Issue 1 https://doi.org/10.1016/j.soilbio.2010.10.001	journal	January 2011
Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars Szoboszlay, Márton; Lambers, Julie; Chappell, Janet Soil Biology and Biochemistry, Vol. 80 https://doi.org/10.1016/j.soilbio.2014.09.001	journal	January 2015
Impacts of directed evolution and soil management legacy on the maize rhizobiome Schmidt, Jennifer E.; Mazza Rodrigues, Jorge L.; Brisson, Vanessa L. Soil Biology and Biochemistry, Vol. 145 https://doi.org/10.1016/j.soilbio.2020.107794	journal	June 2020
Symbiotic phosphate transport in arbuscular mycorrhizas Karandashov, Vladimir; Bucher, Marcel Trends in Plant Science, Vol. 10, Issue 1 https://doi.org/10.1016/j.tplants.2004.12.003	journal	January 2005
Agriculture and the Disruption of Plant–Microbial Symbiosis Porter, Stephanie S.; Sachs, Joel L. Trends in Ecology & Evolution, Vol. 35, Issue 5 https://doi.org/10.1016/j.tree.2020.01.006	journal	May 2020
Phosphorus Stress-Induced Changes in Plant Root Exudation Could Potentially Facilitate Uranium Mobilization from Stable Mineral Forms Edayilam, Nimisha; Montgomery, Dawn; Ferguson, Brennan Environmental Science & Technology, Vol. 52, Issue 14 https://doi.org/10.1021/acs.est.7b05836	journal	May 2018
Mechanism of Absorption of Phosphate from Soil by Endogone Mycorrhizas Sanders, F. E.; Tinker, P. B. Nature, Vol. 233, Issue 5317 https://doi.org/10.1038/233278c0	journal	September 1971
The evolution of apical dominance in maize Doebley, John; Stec, Adrian; Hubbard, Lauren Nature, Vol. 386, Issue 6624 https://doi.org/10.1038/386485a0	journal	April 1997
Root microbiota drive direct integration of phosphate stress and immunity Castrillo, Gabriel; Teixeira, Paulo José Pereira Lima; Paredes, Sur Herrera Nature, Vol. 543, Issue 7646 https://doi.org/10.1038/nature21417	journal	March 2017
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Plant–microbiome interactions: from community assembly to plant health Trivedi, Pankaj; Leach, Jan E.; Tringe, Susannah G. Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0412-1	journal	August 2020
Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil Brisson, Vanessa L.; Schmidt, Jennifer E.; Northen, Trent R. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-52148-y	journal	October 2019
Alternaria spp.: from general saprophyte to specific parasite Thomma, Bart P. H. J. Molecular Plant Pathology, Vol. 4, Issue 4 https://doi.org/10.1046/j.1364-3703.2003.00173.x	journal	July 2003
Diversity and heritability of the maize rhizosphere microbiome under field conditions Peiffer, J. A.; Spor, A.; Koren, O. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1302837110	journal	April 2013
Large-scale replicated field study of maize rhizosphere identifies heritable microbes Walters, William A.; Jin, Zhao; Youngblut, Nicholas Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1800918115	journal	June 2018
Digestion of plant tissue for analysis by ICP emission spectroscopy Huang, Chao‐Yong Luh; Schulte, E. E. Communications in Soil Science and Plant Analysis, Vol. 16, Issue 9 https://doi.org/10.1080/00103628509367657	journal	September 1985
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. Desjardins, A. E.; Plattner, R. D. Canadian Journal of Plant Pathology, Vol. 25, Issue 1 https://doi.org/10.1080/07060660309507045	journal	March 2003
Has agricultural intensification impacted maize root traits and rhizosphere interactions related to organic N acquisition? Schmidt, Jennifer E.; Poret-Peterson, Amisha; Lowry, Carolyn J. AoB PLANTS, Vol. 12, Issue 4 https://doi.org/10.1093/aobpla/plaa026	journal	June 2020
Root-Associated Microbiome of Maize Genotypes with Contrasting Phosphorus Use Efficiency Gomes, Eliane A.; Lana, Ubiraci G. P.; Quensen, John F. Phytobiomes Journal, Vol. 2, Issue 3 https://doi.org/10.1094/PBIOMES-03-18-0012-R	journal	January 2018
Massilia phosphatilytica sp. nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil Zheng, Bang-Xiao; Bi, Qing-Fang; Hao, Xiu-Li International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 8 https://doi.org/10.1099/ijsem.0.001916	journal	August 2017
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 Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Xanthomonas oryzae pathovars: model pathogens of a model crop NiÑO-Liu, David O.; Ronald, Pamela C.; Bogdanove, Adam J. Molecular Plant Pathology, Vol. 7, Issue 5 https://doi.org/10.1111/j.1364-3703.2006.00344.x	journal	September 2006
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning: Phosphate and Petunia mycorrhiza development and functioning Breuillin, Florence; Schramm, Jonathan; Hajirezaei, Mohammad The Plant Journal, Vol. 64, Issue 6 https://doi.org/10.1111/j.1365-313X.2010.04385.x	journal	November 2010
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Functional biology of plant phosphate uptake at root and mycorrhiza interfaces: Tansley review Bucher, Marcel New Phytologist, Vol. 173, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01935.x	journal	December 2006
An efficient microbiological growth medium for screening phosphate solubilizing microorganisms Nautiyal, C. Shekhar FEMS Microbiology Letters, Vol. 170, Issue 1 https://doi.org/10.1111/j.1574-6968.1999.tb13383.x	journal	January 1999
The Statistical Analysis of Compositional Data Aitchison, J. Journal of the Royal Statistical Society: Series B (Methodological), Vol. 44, Issue 2 https://doi.org/10.1111/j.2517-6161.1982.tb01195.x	journal	January 1982
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali New Phytologist, Vol. 209, Issue 2 https://doi.org/10.1111/nph.13697	journal	October 2015
Global maize production, utilization, and consumption: Maize production, utilization, and consumption Ranum, Peter; Peña-Rosas, Juan Pablo; Garcia-Casal, Maria Nieves Annals of the New York Academy of Sciences, Vol. 1312, Issue 1 https://doi.org/10.1111/nyas.12396	journal	March 2014
A specialized metabolic network selectively modulates Arabidopsis root microbiota Huang, Ancheng C.; Jiang, Ting; Liu, Yong-Xin Science, Vol. 364, Issue 6440 https://doi.org/10.1126/science.aau6389	journal	May 2019
Solubilization of Phosphates and Micronutrients by the Plant-Growth-Promoting and Biocontrol Fungus Trichoderma harzianum Rifai 1295-22 Altomare, C.; Norvell, W. A.; Björkman, T. Applied and Environmental Microbiology, Vol. 65, Issue 7 https://doi.org/10.1128/AEM.65.7.2926-2933.1999	journal	July 1999
Solubilization of insoluble phosphates by some soil fungi isolated from nursery seedbeds Agnihotri, V. P. Canadian Journal of Microbiology, Vol. 16, Issue 9 https://doi.org/10.1139/m70-148	journal	September 1970
Fusarium Pathogenomics Ma, Li-Jun; Geiser, David M.; Proctor, Robert H. Annual Review of Microbiology, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-micro-092412-155650	journal	September 2013
Current knowledge and perspectives of Paenibacillus: a review Grady, Elliot Nicholas; MacDonald, Jacqueline; Liu, Linda Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0603-7	journal	December 2016
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Physiological and genetic analysis for maize root characters and yield in response to low phosphorus stress Liu, Zhigang; Liu, Xiangsheng; Craft, Eric J. Breeding Science, Vol. 68, Issue 2 https://doi.org/10.1270/jsbbs.17083	journal	January 2018
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes Zeffa, Douglas Mariani; Perini, Luiz Júnior; Silva, Mayara Barbosa PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0215332	journal	April 2019
Plant- and microbial-based mechanisms to improve the agronomic effectiveness of phosphate rock: a review Arcand, Melissa M.; Schneider, Kim D. Anais da Academia Brasileira de Ciências, Vol. 78, Issue 4 https://doi.org/10.1590/S0001-37652006000400013	journal	December 2006
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton Apprill, A.; McNally, S.; Parsons, R. Aquatic Microbial Ecology, Vol. 75, Issue 2 https://doi.org/10.3354/ame01753	journal	June 2015
Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates Oteino, Nicholas; Lally, Richard D.; Kiwanuka, Samuel Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00745	journal	July 2015
Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture Alori, Elizabeth T.; Glick, Bernard R.; Babalola, Olubukola O. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00971	journal	June 2017
Long-Term Rock Phosphate Fertilization Impacts the Microbial Communities of Maize Rhizosphere Silva, Ubiana C.; Medeiros, Julliane D.; Leite, Laura R. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01266	journal	July 2017
Microbiome Datasets Are Compositional: And This Is Not Optional Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02224	journal	November 2017
Using Ancient Traits to Convert Soil Health into Crop Yield: Impact of Selection on Maize Root and Rhizosphere Function Schmidt, Jennifer E.; Bowles, Timothy M.; Gaudin, Amélie C. M. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00373	journal	March 2016
The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions Jacoby, Richard; Peukert, Manuela; Succurro, Antonella Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01617	journal	September 2017
Mortierella Species as the Plant Growth-Promoting Fungi Present in the Agricultural Soils Ozimek, Ewa; Hanaka, Agnieszka Agriculture, Vol. 11, Issue 1 https://doi.org/10.3390/agriculture11010007	journal	December 2020
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015

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59 BASIC BIOLOGICAL SCIENCES
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Phosphate Availability Modulates Root Exudate Composition and Rhizosphere Microbial Community in a Teosinte and a Modern Maize Cultivar

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