Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

Beschoren da Costa, Pedro; Benucci, Gian Niccolò; Chou, Ming-Yi; Van Wyk, Judson; Chretien, Morgane; Bonito, Gregory

doi:10.1128/mbio.00079-22

Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

Journal Article · Wed Apr 06 00:00:00 EDT 2022 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.00079-22· OSTI ID:1863550

^[1]; ^[2]; ^[2]; ^[2]; Chretien, Morgane ^[3]; ^[2]

DOE Great Lakes Bioenergy Research Center, East Lansing, MI (United States); Michigan State Univ., East Lansing, MI (United States); Michigan State University, Department of Plant, Soil, and Microbial Sciences
DOE Great Lakes Bioenergy Research Center, East Lansing, MI (United States); Michigan State Univ., East Lansing, MI (United States)
DOE Great Lakes Bioenergy Research Center, East Lansing, MI (United States)

Switchgrass (Panicum virgatum) is a model perennial grass for bioenergy production that can be productive in agricultural lands that are not suitable for food production. There is growing interest in whether its associated microbiome may be adaptive in low- or no-input cultivation systems. However, the relative impact of plant genotype and soil factors on plant microbiome and biomass are a challenge to decouple. To address this, a common garden greenhouse experiment was carried out using six common switchgrass genotypes, which were each grown in four different marginal soils collected from long-term bioenergy research sites in Michigan and Wisconsin. We characterized the fungal and bacterial root communities with high-throughput amplicon sequencing of the ITS and 16S rDNA markers, and collected phenological plant traits during plant growth, as well as soil chemical traits. At harvest, we measured the total plant aerial dry biomass. Significant differences in richness and Shannon diversity across soils but not between plant genotypes were found. Generalized linear models showed an interaction between soil and genotype for fungal richness but not for bacterial richness. Community structure was also strongly shaped by soil origin and soil origin × plant genotype interactions. Overall, plant genotype effects were significant but low. Random Forest models indicate that important factors impacting switchgrass biomass included NO₃^–, Ca²⁺, PO₄^3–, and microbial biodiversity. We identified 54 fungal and 52 bacterial predictors of plant aerial biomass, which included several operational taxonomic units belonging to Glomeraceae and Rhizobiaceae, fungal and bacterial lineages that are involved in provisioning nutrients to plants.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018409

OSTI ID:: 1863550

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 13; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (74)

Plant Growth–Promoting Bacteria (PGPB): Isolation and Screening of PGP Activities Ambrosini, Adriana; Passaglia, Luciane M. P. Current Protocols in Plant Biology, Vol. 2, Issue 3 https://doi.org/10.1002/pb.20054	journal	September 2017
Widespread co‐occurrence of Sebacinales and arbuscular mycorrhizal fungi in switchgrass roots and soils has limited dependence on soil carbon or nutrients Lee, Marissa R.; Hawkes, Christine V. PLANTS, PEOPLE, PLANET, Vol. 3, Issue 5 https://doi.org/10.1002/ppp3.10181	journal	January 2021
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Not quite dead enough: on bacterial life, culturability, senescence, and death Nyström, Thomas Archives of Microbiology, Vol. 176, Issue 3 https://doi.org/10.1007/s002030100314	journal	September 2001
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
Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms Richardson, Alan E.; Barea, José-Miguel; McNeill, Ann M. Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-9895-2	journal	February 2009
The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists Baldani, José Ivo; Reis, Veronica Massena; Videira, Sandy Sampaio Plant and Soil, Vol. 384, Issue 1-2 https://doi.org/10.1007/s11104-014-2186-6	journal	July 2014
Soil Carbon Storage by Switchgrass Grown for Bioenergy Liebig, M. A.; Schmer, M. R.; Vogel, K. P. BioEnergy Research, Vol. 1, Issue 3-4 https://doi.org/10.1007/s12155-008-9019-5	journal	September 2008
The Mycorrhizal Fungus, Sebacina vermifera, Enhances Seed Germination and Biomass Production in Switchgrass (Panicum virgatum L) Ghimire, Sita R.; Charlton, Nikki D.; Craven, Kelly D. BioEnergy Research, Vol. 2, Issue 1-2 https://doi.org/10.1007/s12155-009-9033-2	journal	April 2009
Microbiota and Host Nutrition across Plant and Animal Kingdoms Hacquard, Stéphane; Garrido-Oter, Ruben; González, Antonio Cell Host & Microbe, Vol. 17, Issue 5 https://doi.org/10.1016/j.chom.2015.04.009	journal	May 2015
Soil bacterial taxonomic diversity is critical to maintaining the plant productivity Chen, Qing-Lin; Ding, Jing; Zhu, Yong-Guan Environment International, Vol. 140 https://doi.org/10.1016/j.envint.2020.105766	journal	July 2020
Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Frey, Serita D.; Knorr, Melissa; Parrent, Jeri L. Forest Ecology and Management, Vol. 196, Issue 1 https://doi.org/10.1016/j.foreco.2004.03.018	journal	July 2004
A survey of endophytic fungi of switchgrass (Panicum virgatum) in the Midwest, and their putative roles in plant growth Kleczewski, N. M.; Bauer, J. T.; Bever, J. D. Fungal Ecology, Vol. 5, Issue 5 https://doi.org/10.1016/j.funeco.2011.12.006	journal	October 2012
Abundance-occupancy distributions to prioritize plant core microbiome membership Shade, Ashley; Stopnisek, Nejc Current Opinion in Microbiology, Vol. 49 https://doi.org/10.1016/j.mib.2019.09.008	journal	June 2019
Successive plant growth amplifies genotype-specific assembly of the tomato rhizosphere microbiome Cordovez, Viviane; Rotoni, Cristina; Dini-Andreote, Francisco Science of The Total Environment, Vol. 772 https://doi.org/10.1016/j.scitotenv.2020.144825	journal	June 2021
Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.) Roley, Sarah S.; Xue, Chao; Hamilton, Stephen K. Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.11.006	journal	February 2019
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
Soil bacterial and fungal communities across a pH gradient in an arable soil Rousk, Johannes; Bååth, Erland; Brookes, Philip C. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.58	journal	May 2010
Host genotype and age shape the leaf and root microbiomes of a wild perennial plant Wagner, Maggie R.; Lundberg, Derek S.; del Rio, Tijana G. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12151	journal	July 2016
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Practical innovations for high-throughput amplicon sequencing Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2634	journal	September 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
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
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives Schlaeppi, K.; Dombrowski, N.; Oter, R. G. Proceedings of the National Academy of Sciences, Vol. 111, Issue 2 https://doi.org/10.1073/pnas.1321597111	journal	December 2013
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
Assembly and ecological function of the root microbiome across angiosperm plant species Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1717617115	journal	January 2018
Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection Morella, Norma M.; Weng, Francis Cheng-Hsuan; Joubert, Pierre M. Proceedings of the National Academy of Sciences, Vol. 117, Issue 2 https://doi.org/10.1073/pnas.1908600116	journal	December 2019
Conceptual Synthesis in Community Ecology Vellend, Mark The Quarterly Review of Biology, Vol. 85, Issue 2 https://doi.org/10.1086/652373	journal	June 2010
CONSTAX2: improved taxonomic classification of environmental DNA markers Liber, Julian A.; Bonito, Gregory; Benucci, Gian Maria Niccolò Bioinformatics, Vol. 37, Issue 21 https://doi.org/10.1093/bioinformatics/btab347	journal	May 2021
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
Error filtering, pair assembly and error correction for next-generation sequencing reads Edgar, Robert C.; Flyvbjerg, Henrik Bioinformatics, Vol. 31, Issue 21 https://doi.org/10.1093/bioinformatics/btv401	journal	July 2015
Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils Simonin, Marie; Dasilva, Cindy; Terzi, Valeria FEMS Microbiology Ecology, Vol. 96, Issue 6 https://doi.org/10.1093/femsec/fiaa067	journal	April 2020
The Sequence Read Archive Leinonen, R.; Sugawara, H.; Shumway, M. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1019	journal	November 2010
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
GenBank Clark, Karen; Karsch-Mizrachi, Ilene; Lipman, David J. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1276	journal	November 2015
The Switchgrass Microbiome: A Review of Structure, Function, and Taxonomic Distribution Hestrin, Rachel; Lee, Marissa R.; Whitaker, Briana K. Phytobiomes Journal, Vol. 5, Issue 1 https://doi.org/10.1094/PBIOMES-04-20-0029-FI	journal	January 2021
Monosporascus eutypoides , a Cause of Root Rot and Vine Decline in Tunisia, and Evidence that M. cannonballus and M. eutypoides Are Distinct Species Salem, I. Ben; Correia, K. C.; Boughalleb, N. Plant Disease, Vol. 97, Issue 6 https://doi.org/10.1094/PDIS-05-12-0464-RE	journal	June 2013
UCHIME2: improved chimera prediction for amplicon sequencing Edgar, Robert C. https://doi.org/10.1101/074252	posted_content	January 2016
Soil Microorganisms Mediating Phosphorus Availability Update on Microbial Phosphorus Richardson, Alan E.; Simpson, Richard J. Plant Physiology, Vol. 156, Issue 3 https://doi.org/10.1104/pp.111.175448	journal	May 2011
Utilizing ITS1 and ITS2 to study environmental fungal diversity using pyrosequencing Monard, Cécile; Gantner, Stephan; Stenlid, Jan FEMS Microbiology Ecology, Vol. 84, Issue 1 https://doi.org/10.1111/1574-6941.12046	journal	December 2012
Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro Ray, Prasun; Abraham, Paul E.; Guo, Yingqing Environmental Microbiology Reports, Vol. 11, Issue 4 https://doi.org/10.1111/1758-2229.12757	journal	May 2019
Deciphering bacterial mechanisms of root colonization Knights, Hayley E.; Jorrin, Beatriz; Haskett, Timothy L. Environmental Microbiology Reports, Vol. 13, Issue 4 https://doi.org/10.1111/1758-2229.12934	journal	February 2021
The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems van der Heijden, Marcel G. A.; Bardgett, Richard D.; van Straalen, Nico M. Ecology Letters, Vol. 11, Issue 3 https://doi.org/10.1111/j.1461-0248.2007.01139.x	journal	March 2008
Belowground biodiversity effects of plant symbionts support aboveground productivity: Biodiversity effects of soil symbionts Wagg, Cameron; Jansa, Jan; Schmid, Bernhard Ecology Letters, Vol. 14, Issue 10 https://doi.org/10.1111/j.1461-0248.2011.01666.x	journal	July 2011
Quantifying the roles of immigration and chance in shaping prokaryote community structure Sloan, William T.; Lunn, Mary; Woodcock, Stephen Environmental Microbiology, Vol. 8, Issue 4 https://doi.org/10.1111/j.1462-2920.2005.00956.x	journal	April 2006
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
Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere: Plant species, soil type and rhizosphere communities Berg, Gabriele; Smalla, Kornelia FEMS Microbiology Ecology, Vol. 68, Issue 1 https://doi.org/10.1111/j.1574-6941.2009.00654.x	journal	April 2009
Improving indicator species analysis by combining groups of sites De Cáceres, Miquel; Legendre, Pierre; Moretti, Marco Oikos, Vol. 119, Issue 10 https://doi.org/10.1111/j.1600-0706.2010.18334.x	journal	September 2010
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars Bálint, Miklós; Bartha, László; O'Hara, Robert B. Molecular Ecology, Vol. 24, Issue 1 https://doi.org/10.1111/mec.13018	journal	December 2014
Influence of Soil Characteristics on the Diversity of Bacteria in the Southern Brazilian Atlantic Forest Faoro, H.; Alves, A. C.; Souza, E. M. Applied and Environmental Microbiology, Vol. 76, Issue 14 https://doi.org/10.1128/AEM.03025-09	journal	May 2010
Enhancement of Switchgrass (Panicum virgatum L.) Biomass Production under Drought Conditions by the Ectomycorrhizal Fungus Sebacina vermifera Ghimire, Sita R.; Craven, Kelly D. Applied and Environmental Microbiology, Vol. 77, Issue 19 https://doi.org/10.1128/AEM.05225-11	journal	August 2011
Structure and Functions of the Bacterial Microbiota of Plants Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120106	journal	April 2013
Physiological Interactions Between Symbionts in Vesicular-Arbuscular Mycorrhizal Plants Smith, S. E.; Gianinazzi-Pearson, V. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.pp.39.060188.001253	journal	June 1988
The plant microbiome Turner, Thomas R.; James, Euan K.; Poole, Philip S. Genome Biology, Vol. 14, Issue 6 https://doi.org/10.1186/gb-2013-14-6-209	journal	June 2013
Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly Liu, Fang; Hewezi, Tarek; Lebeis, Sarah L. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1572-x	journal	September 2019
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome Cregger, M. A.; Veach, A. M.; Yang, Z. K. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0413-8	journal	February 2018
Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data Davis, Nicole M.; Proctor, Diana M.; Holmes, Susan P. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0605-2	journal	December 2018
Correction to: Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula Brown, Shawn P.; Grillo, Michael A.; Podowski, Justin C. Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01080-3	journal	May 2021
What is the hologenome concept of evolution? Morris, J. Jeffrey F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.14385.1	journal	January 2018
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible McMurdie, Paul J.; Holmes, Susan PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003531	journal	April 2014
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient Roley, Sarah S.; Duncan, David S.; Liang, Di PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197320	journal	June 2018
Patient propagules: Do soil archives preserve the legacy of fungal and prokaryotic communities? Benucci, Gian Maria Niccolò; Rennick, Bryan; Bonito, Gregory PLOS ONE, Vol. 15, Issue 8 https://doi.org/10.1371/journal.pone.0237368	journal	August 2020
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
UNITE general FASTA release Community, Unite UNITE Community https://doi.org/10.15156/bio/587475	dataset	January 2017
The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass ( Panicum virgatum) Milano, Elizabeth R.; Lowry, David B.; Juenger, Thomas E. G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 11 https://doi.org/10.1534/g3.116.032763	journal	September 2016
Genomic Analysis of Diverse Members of the Fungal Genus Monosporascus Reveals Novel Lineages, Unique Genome Content and a Potential Bacterial Associate Robinson, Aaron J.; Natvig, Donald O.; Chain, Patrick S. G. G3 Genes\|Genomes\|Genetics, Vol. 10, Issue 8 https://doi.org/10.1534/g3.120.401489	journal	August 2020
Thirty years of viable but nonculturable state research: Unsolved molecular mechanisms Pinto, Daniela; Santos, Mário A.; Chambel, Lélia Critical Reviews in Microbiology, Vol. 41, Issue 1 https://doi.org/10.3109/1040841X.2013.794127	journal	May 2013
Crop Management Impacts the Soybean (Glycine max) Microbiome Longley, Reid; Noel, Zachary A.; Benucci, Gian Maria Niccolò Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01116	journal	June 2020
The Microbe-Free Plant: Fact or Artifact? Partida-Martínez, Laila P.; Heil, Martin Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00100	journal	January 2011
Generic hyper-diversity in Stachybotriaceae Lombard, L.; Houbraken, J.; Decock, C. Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 36, Issue 1 https://doi.org/10.3767/003158516X691582	journal	June 2016
Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data Palmer, Jonathan M.; Jusino, Michelle A.; Banik, Mark T. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4925	journal	January 2018
Microbial communities associated with the black morel Morchella sextelata cultivated in greenhouses Benucci, Gian Maria Niccolò; Longley, Reid; Zhang, Peng PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7744	journal	January 2019

Similar Records

Intraspecific variability in root traits and edaphic conditions influence soil microbiomes across 12 switchgrass cultivars

Journal Article · Thu Aug 13 00:00:00 EDT 2020 · Phytobiomes Journal · OSTI ID:1682258

Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype

Journal Article · Fri Mar 29 00:00:00 EDT 2019 · Frontiers in Microbiology · OSTI ID:1505327

Genetic modification of the shikimate pathway to reduce lignin content in switchgrass (Panicum virgatum L.) significantly impacts plant microbiomes

Journal Article · Mon Nov 25 23:00:00 EST 2024 · Microbiology Spectrum · OSTI ID:2506754

Related Subjects

plant biomass
16S rRNA
59 BASIC BIOLOGICAL SCIENCES
ITS
bioenergy crops
random forest
rhizobiome
sustainability

Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

Citation Formats

References (74)

Similar Records

Related Subjects