Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome
Abstract
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 amongmore »
- Authors:
-
- University of Illinois at Urbana-Champaign, IL (United States)
- Publication Date:
- Research Org.:
- Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 2007154
- Grant/Contract Number:
- SC0018420
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Perennial plant microbiomes; Rhizosphere soil; Microbiome assembly; Microbial co-occurrence networks; Core microbiome; Host genetic variation
Citation Formats
Ji, Niuniu, Liang, Di, Clark, Lindsay V., Sacks, Erik J., and Kent, Angela D. Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome. United States: N. p., 2023.
Web. doi:10.1186/s40168-023-01646-3.
Ji, Niuniu, Liang, Di, Clark, Lindsay V., Sacks, Erik J., & Kent, Angela D. Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome. United States. https://doi.org/10.1186/s40168-023-01646-3
Ji, Niuniu, Liang, Di, Clark, Lindsay V., Sacks, Erik J., and Kent, Angela D. Sat .
"Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome". United States. https://doi.org/10.1186/s40168-023-01646-3. https://www.osti.gov/servlets/purl/2007154.
@article{osti_2007154,
title = {Host genetic variation drives the differentiation in the ecological role of the native Miscanthus root-associated microbiome},
author = {Ji, Niuniu and Liang, Di and Clark, Lindsay V. and Sacks, Erik J. and Kent, Angela D.},
abstractNote = {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.},
doi = {10.1186/s40168-023-01646-3},
journal = {Microbiome},
number = 1,
volume = 11,
place = {United States},
year = {Sat Sep 30 00:00:00 EDT 2023},
month = {Sat Sep 30 00:00:00 EDT 2023}
}
Works referenced in this record:
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018
- Sasse, Joelle; Martinoia, Enrico; Northen, Trent
- Trends in Plant Science, Vol. 23, Issue 1
Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome
journal, May 2021
- Deng, Siwen; Caddell, Daniel F.; Xu, Gen
- The ISME Journal
NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice
journal, April 2019
- Zhang, Jingying; Liu, Yong-Xin; Zhang, Na
- Nature Biotechnology, Vol. 37, Issue 6
A framework genetic map for Miscanthus sinensis from RNAseq-based markers shows recent tetraploidy
journal, January 2012
- Swaminathan, Kankshita; Chae, Won; Mitros, Therese
- BMC Genomics, Vol. 13, Issue 1
Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation
journal, April 2021
- Yu, Peng; He, Xiaoming; Baer, Marcel
- Nature Plants, Vol. 7, Issue 4
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
Adaptive linear step-up procedures that control the false discovery rate
journal, September 2006
- Benjamini, Yoav; Krieger, Abba M.; Yekutieli, Daniel
- Biometrika, Vol. 93, Issue 3
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood
journal, February 2021
- Moll, Julia; Heintz-Buschart, Anna; Bässler, Claus
- mSphere, Vol. 6, Issue 1
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010
- Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
Defining the core Arabidopsis thaliana root microbiome
journal, August 2012
- Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
- Nature, Vol. 488, Issue 7409
Core Microbiota in Agricultural Soils and Their Potential Associations with Nutrient Cycling
journal, March 2019
- Jiao, Shuo; Xu, Yiqin; Zhang, Jie
- mSystems, Vol. 4, Issue 2
Plant microbiome–an account of the factors that shape community composition and diversity
journal, September 2020
- Dastogeer, Khondoker M. G.; Tumpa, Farzana Haque; Sultana, Afruja
- Current Plant Biology, Vol. 23
Friends or foes? Emerging insights from fungal interactions with plants
journal, November 2015
- Zeilinger, Susanne; Gupta, Vijai K.; Dahms, Tanya E. S.
- FEMS Microbiology Reviews, Vol. 40, Issue 2
FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011
- Magoc, T.; Salzberg, S. L.
- Bioinformatics, Vol. 27, Issue 21
The importance of the microbiome of the plant holobiont
journal, February 2015
- Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie
- New Phytologist, Vol. 206, Issue 4
Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome
journal, September 2017
- Tian, Baoyu; Zhang, Cuijuan; Ye, Yuan
- Agriculture, Ecosystems & Environment, Vol. 247
The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
journal, February 2001
- Chelius, M. K.; Triplett, E. W.
- Microbial Ecology, Vol. 41, Issue 3
Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China
journal, January 2016
- Ma, Bin; Wang, Haizhen; Dsouza, Melissa
- The ISME Journal, Vol. 10, Issue 8
Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development
journal, August 2015
- Burns, Adam R.; Stephens, W. Zac; Stagaman, Keaton
- The ISME Journal, Vol. 10, Issue 3
Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization
journal, October 2019
- Chen, Shuaimin; Waghmode, Tatoba R.; Sun, Ruibo
- Microbiome, Vol. 7, Issue 1
A general framework for quantitatively assessing ecological stochasticity
journal, August 2019
- Ning, Daliang; Deng, Ye; Tiedje, James M.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 34
Root microbiota assembly and adaptive differentiation among European Arabidopsis populations
journal, December 2019
- Thiergart, Thorsten; Durán, Paloma; Ellis, Thomas
- Nature Ecology & Evolution, Vol. 4, Issue 1
The root microbiome: Community assembly and its contributions to plant fitness
journal, February 2022
- Bai, Bo; Liu, Weidong; Qiu, Xingyu
- Journal of Integrative Plant Biology, Vol. 64, Issue 2
The Plant Microbiota: Systems-Level Insights and Perspectives
journal, November 2016
- Müller, Daniel B.; Vogel, Christine; Bai, Yang
- Annual Review of Genetics, Vol. 50, Issue 1
Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants
journal, December 2008
- Franche, Claudine; Lindström, Kristina; Elmerich, Claudine
- Plant and Soil, Vol. 321, Issue 1-2
Core microbiota drive functional stability of soil microbiome in reforestation ecosystems
journal, December 2021
- Jiao, Shuo; Chen, Weimin; Wei, Gehong
- Global Change Biology, Vol. 28, Issue 3
Molecular ecological network analyses
journal, January 2012
- Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng
- BMC Bioinformatics, Vol. 13, Issue 1
Defining and quantifying the core microbiome: Challenges and prospects
journal, December 2021
- Neu, Alexander T.; Allen, Eric E.; Roy, Kaustuv
- Proceedings of the National Academy of Sciences, Vol. 118, Issue 51
Host selection shapes crop microbiome assembly and network complexity
journal, September 2020
- Xiong, Chao; Zhu, Yong‐Guan; Wang, Jun‐Tao
- New Phytologist, Vol. 229, Issue 2
Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases
journal, January 2009
- Brulc, Jennifer M.; Antonopoulos, Dionysios A.; Berg Miller, Margret E.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 6
Miscanthus as cellulosic biomass for bioethanol production
journal, May 2015
- Lee, Wen-Chien; Kuan, Wei-Chih
- Biotechnology Journal, Vol. 10, Issue 6
Culturable bacteria are more common than fungi in floral nectar and are more easily dispersed by thrips, a ubiquitous flower visitor
journal, November 2021
- Vannette, Rachel L.; McMunn, Marshall S.; Hall, Griffin W.
- FEMS Microbiology Ecology, Vol. 97, Issue 12
Microsatellites: simple sequences with complex evolution
journal, June 2004
- Ellegren, Hans
- Nature Reviews Genetics, Vol. 5, Issue 6
Towards an integrative biology research: a case study on adaptive and evolutionary trends of Miscanthus populations in Taiwan
journal, June 2001
- Chou, Chang-Hung; Chiang, Tseng-Yu; Chiang, Yu-Chung
- Weed Biology and Management, Vol. 1, Issue 2
Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests
journal, November 2008
- Christian, D. G.; Riche, A. B.; Yates, N. E.
- Industrial Crops and Products, Vol. 28, Issue 3
Host genetics regulate the plant microbiome
journal, April 2023
- Zhang, Jingying; Liu, Weidong; Bu, Jingshu
- Current Opinion in Microbiology, Vol. 72
Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype
journal, March 2021
- Stopnisek, Nejc; Shade, Ashley
- The ISME Journal, Vol. 15, Issue 9
Quantifying the roles of immigration and chance in shaping prokaryote community structure
journal, April 2006
- Sloan, William T.; Lunn, Mary; Woodcock, Stephen
- Environmental Microbiology, Vol. 8, Issue 4
Cohesion: a method for quantifying the connectivity of microbial communities
journal, July 2017
- Herren, Cristina M.; McMahon, Katherine D.
- The ISME Journal, Vol. 11, Issue 11
Field study reveals core plant microbiota and relative importance of their drivers: Core microbiota of field-grown sugarcane and their drivers
journal, January 2018
- Hamonts, Kelly; Trivedi, Pankaj; Garg, Anshu
- Environmental Microbiology, Vol. 20, Issue 1
Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula
journal, September 2020
- Brown, Shawn P.; Grillo, Michael A.; Podowski, Justin C.
- Microbiome, Vol. 8, Issue 1
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
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley
journal, March 2015
- Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C.
- Cell Host & Microbe, Vol. 17, Issue 3
Compartmentalization increases food-web persistence
journal, February 2011
- Stouffer, Daniel B.; Bascompte, Jordi
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 9
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Disease-induced assemblage of a plant-beneficial bacterial consortium
journal, March 2018
- Berendsen, Roeland L.; Vismans, Gilles; Yu, Ke
- The ISME Journal, Vol. 12, Issue 6
The influence of maize genotype on the rhizosphere eukaryotic community
journal, April 2021
- Matus-Acuña, Violeta; Caballero-Flores, Gustavo; Martínez-Romero, Esperanza
- FEMS Microbiology Ecology, Vol. 97, Issue 6
Chloroplast DNA markers (cpSSRs, SNPs) for Miscanthus, Saccharum and related grasses (Panicoideae, Poaceae)
journal, May 2010
- de Cesare, Mariateresa; Hodkinson, Trevor R.; Barth, Susanne
- Molecular Breeding, Vol. 26, Issue 3
Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics
book, January 1990
- White, T. J.; Bruns, T.; Lee, S.
- PCR Protocols
Core microbiomes for sustainable agroecosystems
journal, April 2018
- Toju, Hirokazu; Peay, Kabir G.; Yamamichi, Masato
- Nature Plants, Vol. 4, Issue 5
Microsatellites, from molecules to populations and back
journal, October 1996
- Jarne, Philippe; Lagoda, Pierre J. L.
- Trends in Ecology & Evolution, Vol. 11, Issue 10
Contribution of nitrogen fixation to first year Miscanthus × giganteus
journal, July 2013
- Keymer, Daniel P.; Kent, Angela D.
- GCB Bioenergy, Vol. 6, Issue 5
APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004
- Paradis, E.; Claude, J.; Strimmer, K.
- Bioinformatics, Vol. 20, Issue 2
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
PowerMarker: an integrated analysis environment for genetic marker analysis
journal, February 2005
- Liu, K.; Muse, S. V.
- Bioinformatics, Vol. 21, Issue 9
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
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
Climate warming enhances microbial network complexity and stability
journal, February 2021
- Yuan, Mengting Maggie; Guo, Xue; Wu, Linwei
- Nature Climate Change, Vol. 11, Issue 4
Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013
- Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn
- Annual Review of Plant Biology, Vol. 64, Issue 1
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
journal, July 2018
- Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma
- Nature Communications, Vol. 9, Issue 1