Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome

Ji, Niuniu; Liang, Di; Clark, Lindsay V.; Sacks, Erik J.; Kent, Angela D.

doi:10.1186/s40168-023-01646-3

Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome

Journal Article · Sat Sep 30 00:00:00 EDT 2023 · Microbiome

DOI:https://doi.org/10.1186/s40168-023-01646-3· OSTI ID:2007154

Ji, Niuniu ^[1]; Liang, Di ^[2]; Clark, Lindsay V. ^[2]; Sacks, Erik J. ^[2]; Kent, Angela D. ^[2]

University of Illinois at Urbana-Champaign, IL (United States); CABBI
University of Illinois at Urbana-Champaign, IL (United States)

Microbiome recruitment is influenced by plant host, but how host plant impacts the assembly, functions, and interactions of perennial plant root microbiomes is poorly understood. Here we examined prokaryotic and fungal communities between rhizosphere soils and the root endophytic compartment in two native Miscanthus species (Miscanthus sinensis and Miscanthus floridulus) of Taiwan and further explored the roles of host plant on root-associated microbiomes. Our results suggest that host plant genetic variation, edaphic factors, and site had effects on the root endophytic and rhizosphere soil microbial community compositions in both Miscanthus sinensis and Miscanthus floridulus, with a greater effect of plant genetic variation observed for the root endophytic communities. Host plant genetic variation also exerted a stronger effect on core prokaryotic communities than on non-core prokaryotic communities in each microhabitat of two Miscanthus species. From rhizosphere soils to root endophytes, prokaryotic co-occurrence network stability increased, but fungal co-occurrence network stability decreased. Furthermore, we found root endophytic microbial communities in two Miscanthus species were more strongly driven by deterministic processes rather than stochastic processes. Root-enriched prokaryotic OTUs belong to Gammaproteobacteria, Alphaproteobacteria, Betaproteobacteria, Sphingobacteriia, and [Saprospirae] both in two Miscanthus species, while prokaryotic taxa enriched in the rhizosphere soil are widely distributed among different phyla. We provide empirical evidence that host genetic variation plays important roles in root-associated microbiome in Miscanthus. The results of this study have implications for future bioenergy crop management by providing baseline data to inform translational research to harness the plant microbiome to sustainably increase agriculture productivity.

View Accepted Manuscript (DOE)

Research Organization:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

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

Grant/Contract Number:: SC0018420

OSTI ID:: 2007154

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 11; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Miscanthus as cellulosic biomass for bioethanol production Lee, Wen-Chien; Kuan, Wei-Chih Biotechnology Journal, Vol. 10, Issue 6 https://doi.org/10.1002/biot.201400704	journal	May 2015
The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L. Chelius, M. K.; Triplett, E. W. Microbial Ecology, Vol. 41, Issue 3 https://doi.org/10.1007/s002480000087	journal	February 2001
Chloroplast DNA markers (cpSSRs, SNPs) for Miscanthus, Saccharum and related grasses (Panicoideae, Poaceae) de Cesare, Mariateresa; Hodkinson, Trevor R.; Barth, Susanne Molecular Breeding, Vol. 26, Issue 3 https://doi.org/10.1007/s11032-010-9451-z	journal	May 2010
Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants Franche, Claudine; Lindström, Kristina; Elmerich, Claudine Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-008-9833-8	journal	December 2008
Microsatellites, from molecules to populations and back Jarne, Philippe; Lagoda, Pierre J. L. Trends in Ecology & Evolution, Vol. 11, Issue 10 https://doi.org/10.1016/0169-5347(96)10049-5	journal	October 1996
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
Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome Tian, Baoyu; Zhang, Cuijuan; Ye, Yuan Agriculture, Ecosystems & Environment, Vol. 247 https://doi.org/10.1016/j.agee.2017.06.041	journal	September 2017
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C. Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.01.011	journal	March 2015
Plant microbiome–an account of the factors that shape community composition and diversity Dastogeer, Khondoker M. G.; Tumpa, Farzana Haque; Sultana, Afruja Current Plant Biology, Vol. 23 https://doi.org/10.1016/j.cpb.2020.100161	journal	September 2020
Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests Christian, D. G.; Riche, A. B.; Yates, N. E. Industrial Crops and Products, Vol. 28, Issue 3 https://doi.org/10.1016/j.indcrop.2008.02.009	journal	November 2008
Host genetics regulate the plant microbiome Zhang, Jingying; Liu, Weidong; Bu, Jingshu Current Opinion in Microbiology, Vol. 72 https://doi.org/10.1016/j.mib.2023.102268	journal	April 2023
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Trends in Plant Science, Vol. 23, Issue 1 https://doi.org/10.1016/j.tplants.2017.09.003	journal	January 2018
Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development Burns, Adam R.; Stephens, W. Zac; Stagaman, Keaton The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.142	journal	August 2015
Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China Ma, Bin; Wang, Haizhen; Dsouza, Melissa The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2015.261	journal	January 2016
Cohesion: a method for quantifying the connectivity of microbial communities Herren, Cristina M.; McMahon, Katherine D. The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.91	journal	July 2017
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
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
Microsatellites: simple sequences with complex evolution Ellegren, Hans Nature Reviews Genetics, Vol. 5, Issue 6 https://doi.org/10.1038/nrg1348	journal	June 2004
Disease-induced assemblage of a plant-beneficial bacterial consortium Berendsen, Roeland L.; Vismans, Gilles; Yu, Ke The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0093-1	journal	March 2018
Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype Stopnisek, Nejc; Shade, Ashley The ISME Journal, Vol. 15, Issue 9 https://doi.org/10.1038/s41396-021-00955-5	journal	March 2021
Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome Deng, Siwen; Caddell, Daniel F.; Xu, Gen The ISME Journal https://doi.org/10.1038/s41396-021-00993-z	journal	May 2021
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05122-7	journal	July 2018
Core microbiomes for sustainable agroecosystems Toju, Hirokazu; Peay, Kabir G.; Yamamichi, Masato Nature Plants, Vol. 4, Issue 5 https://doi.org/10.1038/s41477-018-0139-4	journal	April 2018
Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation Yu, Peng; He, Xiaoming; Baer, Marcel Nature Plants, Vol. 7, Issue 4 https://doi.org/10.1038/s41477-021-00897-y	journal	April 2021
Climate warming enhances microbial network complexity and stability Yuan, Mengting Maggie; Guo, Xue; Wu, Linwei Nature Climate Change, Vol. 11, Issue 4 https://doi.org/10.1038/s41558-021-00989-9	journal	February 2021
Root microbiota assembly and adaptive differentiation among European Arabidopsis populations Thiergart, Thorsten; Durán, Paloma; Ellis, Thomas Nature Ecology & Evolution, Vol. 4, Issue 1 https://doi.org/10.1038/s41559-019-1063-3	journal	December 2019
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
NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice Zhang, Jingying; Liu, Yong-Xin; Zhang, Na Nature Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1038/s41587-019-0104-4	journal	April 2019
Towards an integrative biology research: a case study on adaptive and evolutionary trends of Miscanthus populations in Taiwan Chou, Chang-Hung; Chiang, Tseng-Yu; Chiang, Yu-Chung Weed Biology and Management, Vol. 1, Issue 2 https://doi.org/10.1046/j.1445-6664.2001.00018.x	journal	June 2001
Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases Brulc, Jennifer M.; Antonopoulos, Dionysios A.; Berg Miller, Margret E. Proceedings of the National Academy of Sciences, Vol. 106, Issue 6 https://doi.org/10.1073/pnas.0806191105	journal	January 2009
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
Compartmentalization increases food-web persistence Stouffer, Daniel B.; Bascompte, Jordi Proceedings of the National Academy of Sciences, Vol. 108, Issue 9 https://doi.org/10.1073/pnas.1014353108	journal	February 2011
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
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
A general framework for quantitatively assessing ecological stochasticity Ning, Daliang; Deng, Ye; Tiedje, James M. Proceedings of the National Academy of Sciences, Vol. 116, Issue 34 https://doi.org/10.1073/pnas.1904623116	journal	August 2019
Defining and quantifying the core microbiome: Challenges and prospects Neu, Alexander T.; Allen, Eric E.; Roy, Kaustuv Proceedings of the National Academy of Sciences, Vol. 118, Issue 51 https://doi.org/10.1073/pnas.2104429118	journal	December 2021
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
PowerMarker: an integrated analysis environment for genetic marker analysis Liu, K.; Muse, S. V. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti282	journal	February 2005
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Adaptive linear step-up procedures that control the false discovery rate Benjamini, Yoav; Krieger, Abba M.; Yekutieli, Daniel Biometrika, Vol. 93, Issue 3 https://doi.org/10.1093/biomet/93.3.491	journal	September 2006
The influence of maize genotype on the rhizosphere eukaryotic community Matus-Acuña, Violeta; Caballero-Flores, Gustavo; Martínez-Romero, Esperanza FEMS Microbiology Ecology, Vol. 97, Issue 6 https://doi.org/10.1093/femsec/fiab066	journal	April 2021
Culturable bacteria are more common than fungi in floral nectar and are more easily dispersed by thrips, a ubiquitous flower visitor Vannette, Rachel L.; McMunn, Marshall S.; Hall, Griffin W. FEMS Microbiology Ecology, Vol. 97, Issue 12 https://doi.org/10.1093/femsec/fiab150	journal	November 2021
Friends or foes? Emerging insights from fungal interactions with plants Zeilinger, Susanne; Gupta, Vijai K.; Dahms, Tanya E. S. FEMS Microbiology Reviews, Vol. 40, Issue 2 https://doi.org/10.1093/femsre/fuv045	journal	November 2015
Field study reveals core plant microbiota and relative importance of their drivers: Core microbiota of field-grown sugarcane and their drivers Hamonts, Kelly; Trivedi, Pankaj; Garg, Anshu Environmental Microbiology, Vol. 20, Issue 1 https://doi.org/10.1111/1462-2920.14031	journal	January 2018
Core microbiota drive functional stability of soil microbiome in reforestation ecosystems Jiao, Shuo; Chen, Weimin; Wei, Gehong Global Change Biology, Vol. 28, Issue 3 https://doi.org/10.1111/gcb.16024	journal	December 2021
Contribution of nitrogen fixation to first year Miscanthus × giganteus Keymer, Daniel P.; Kent, Angela D. GCB Bioenergy, Vol. 6, Issue 5 https://doi.org/10.1111/gcbb.12095	journal	July 2013
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
The root microbiome: Community assembly and its contributions to plant fitness Bai, Bo; Liu, Weidong; Qiu, Xingyu Journal of Integrative Plant Biology, Vol. 64, Issue 2 https://doi.org/10.1111/jipb.13226	journal	February 2022
The importance of the microbiome of the plant holobiont Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13312	journal	February 2015
Host selection shapes crop microbiome assembly and network complexity Xiong, Chao; Zhu, Yong‐Guan; Wang, Jun‐Tao New Phytologist, Vol. 229, Issue 2 https://doi.org/10.1111/nph.16890	journal	September 2020
The ecology of the microbiome: Networks, competition, and stability Coyte, K. Z.; Schluter, J.; Foster, K. R. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aad2602	journal	November 2015
Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood Moll, Julia; Heintz-Buschart, Anna; Bässler, Claus mSphere, Vol. 6, Issue 1 https://doi.org/10.1128/mSphere.00856-20	journal	February 2021
Core Microbiota in Agricultural Soils and Their Potential Associations with Nutrient Cycling Jiao, Shuo; Xu, Yiqin; Zhang, Jie mSystems, Vol. 4, Issue 2 https://doi.org/10.1128/mSystems.00313-18	journal	March 2019
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
The Plant Microbiota: Systems-Level Insights and Perspectives Müller, Daniel B.; Vogel, Christine; Bai, Yang Annual Review of Genetics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-genet-120215-034952	journal	November 2016
Molecular ecological network analyses Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-113	journal	January 2012
WGCNA: an R package for weighted correlation network analysis Langfelder, Peter; Horvath, Steve BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-559	journal	December 2008
A framework genetic map for Miscanthus sinensis from RNAseq-based markers shows recent tetraploidy Swaminathan, Kankshita; Chae, Won; Mitros, Therese BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-142	journal	January 2012
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
Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization Chen, Shuaimin; Waghmode, Tatoba R.; Sun, Ruibo Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0750-2	journal	October 2019
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. 8, Issue 1 https://doi.org/10.1186/s40168-020-00915-9	journal	September 2020
Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization Chen, Shuaimin; Waghmode, Tatoba; Sun, Ruibo figshare https://doi.org/10.6084/m9.figshare.c.4708817.v1	collection	January 2019
Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula Brown, Shawn P.; Grillo, Michael A.; Podowski, Justin C. figshare https://doi.org/10.6084/m9.figshare.c.5135614.v1	collection	January 2020

Cited By (1)

Additional file 1 of Host genotype-specific rhizosphere fungus enhances drought resistance in wheat Yue, Hong; Sun, Xuming; Wang, Tingting figshare https://doi.org/10.6084/m9.figshare.25333388	dataset	January 2024

Similar Records

Chronic drought differentially alters the belowground microbiome of drought tolerant and drought susceptible genotypes of Populus trichocarpa

Journal Article · Tue Jul 12 20:00:00 EDT 2022 · Phytobiomes Journal · OSTI ID:1879964

Time-series RNA metabarcoding of the active Populus tremuloides root microbiome reveals hidden temporal dynamics and dormant core members

Journal Article · Thu Nov 06 19:00:00 EST 2025 · mSystems · OSTI ID:3001733

Related Subjects

54 ENVIRONMENTAL SCIENCES
Core microbiome
Host genetic variation
Microbial co-occurrence networks
Microbiome assembly
Perennial plant microbiomes
Rhizosphere soil

Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome

Citation Formats

References (63)

Cited By (1)

Similar Records

Related Subjects