Abstract
Purpose
The root-associated microbiota is essential to plant health, fitness and productivity, but the effect of plant domestication on the ecological process of microbial community assembly is unclear.
Methods
High-throughput sequencing of the 16S rRNA genes was employed to investigated the the diversity, ecological assembly process and cooccurrence relationship of the bacterial communities of multiple root compartment niches (root zone, rhizosphere, and root endosphere) between wild and landrace accessions grown in three soil types.
Results
Our results showed that the domestication effect on bacterial community increased from the root zone to the rhizosphere and endosphere, while the soil type effect decreased. Compared with wild soybean, the root endosphere bacterial community of the landraces was more sensitive to soil environmental change. The deterministic process dominated the assembly of the bacterial community in the rhizosphere and root endosphere, and its relative contribution was higher in the landraces than in wild soybeans. In the two root compartments, the increased root system selection pressure in the landraces was indicated by a greater loss of bacteria at the same taxon level and lower bacterial diversity. Furthermore, the family Oxalobacteraceae and the class Actinobacteria were identified as important root-associated biomarker taxa for wild soybeans, while Enterobacteriaceae was such for the landraces.
Conclusions
Our findings provide crucial empirical evidence for the host selection and enrichment process of the microbial community under local domestication and are of great significance in understanding the coevolution of hosts and microbiota, which will aid in manipulating microbiota for future crop breeding.
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Data availability
The obtained raw data have been deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database (Accession No.: PRJNA806450).
References
Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S, Weigel D, Kemen EM (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. Plos Biol 14:e1002352
Álvarez-Pérez JM, González-García S, Cobos R, Olego MÁ, Ibañez A, Díez-Galán A, Garzón-Jimeno E, Coque JJR, Master ER (2017) Use of endophytic and rhizosphere actinobacteria from grapevine plants to reduce nursery fungal graft infections that lead to young grapevine decline. Appl Environ Microb 83:e1517–e1564
Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576
Barbosa Lima A, Cannavan FS, Navarrete AA, Teixeira WG, Kuramae EE, Tsai SM (2015) Amazonian dark earth and plant species from the amazon region contribute to shape rhizosphere bacterial communities. Microb Ecol 69:855–866
Bastian M, Heymann S, Jacomy M (2009) Gephi: An open source software for exploring and manipulating networks. In In International AAAI conference on weblogs and social media: San Jose, California
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Brenner DJ, Farmer JJ III (2015) Enterobacteriaceae. In: Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P, Rainey FA, Whitman WB (eds) Bergey’s manual of systematics of archaea and bacteria. Wiley, pp 1–24. https://doi.org/10.1002/9781118960608.fbm00222
Brown SP, Grillo MA, Podowski JC, Heath KD (2020) Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula. Microbiome 8:1–17
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Carter TE, Nelson RL, Sneller CH, Cui Z (2004) Genetic diversity in soybean. Soybeans: Improvement, Production, and Uses 16:303–416
Chen L, Xin X, Zhang J, Redmile-Gordon M, Nie G (2017) Soil characteristics overwhelm cultivar effects on the structure and assembly of root-associated microbiomes of modern maize. Pedosphere 29:360–373
DeHaan L, Larson S, López-Marqués RL, Wenkel S, Gao C, Palmgren M (2020) Roadmap for accelerated domestication of an emerging perennial grain crop. Trends Plant Sci 25:525–537
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-Gonzalez A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359:320–325
Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. Isme J 7:37–49
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Edgar RC (2013) UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920
Fan K, Delgado-Baquerizo M, Guo X, Wang D, Wu Y, Zhu M, Yu W, Yao H, Zhu Y, Chu H (2019) Suppressed N fixation and diazotrophs after four decades of fertilization. Microbiome 7:143
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. Plos Comput Biol 8:e1002606
Germida J, Siciliano S (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fert Soils 33:410–415
Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58
Kim MY, Van K, Kang YJ, Kim KH, Lee S (2012) Tracing soybean domestication history: From nucleotide to genome. Breeding Sci 61:445–452
Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG, Bushman FD, Knight R, Kelley ST (2011) Bayesian community-wide culture-independent microbial source tracking. Nat Methods 8:761–763
Koop-Jakobsen K, Giblin AE (2010) The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnol Oceanogr 55:789–802
Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina Del Rio T, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864
Leff JW, Lynch RC, Kane NC, Fierer N (2017) Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus. New Phytol 214:412–423
Letunic I, Bork P (2019) Interactive Tree of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res 47:W256–W259
Li Y, Guan R, Liu Z, Ma Y, Wang L, Li L, Lin F, Luan W, Chen P, Yan Z, Guan Y, Zhu L, Ning X, Smulders MJM, Li W, Piao R, Cui Y, Yu Z, Guan M, Chang R, Hou A, Shi A, Zhang B, Zhu S, Qiu L (2008) Genetic structure and diversity of cultivated soybean (Glycine max (L.) Merr.) landraces in China. Theor Appl Genet 117:857–871
Liu C, Zhuang X, Yu Z, Wang Z, Wang Y, Guo X, Xiang W, Huang S (2019a) Community structures and antifungal activity of root-associated endophytic actinobacteria of healthy and diseased soybean. Microorganisms 7:243
Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME (2019b) Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. Bmc Microbiol 19:201
Liu Y, Du H, Li P, Shen Y, Peng H, Liu S, Zhou G, Zhang H, Liu Z, Shi M, Huang X, Li Y, Zhang M, Wang Z, Zhu B, Han B, Liang C, Tian Z (2020) Pan-Genome of wild and cultivated soybeans. Cell 182:162–176
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277
Luo X, Qian H, Wang L, Han S, Wen S, Wang B, Huang Q, Chen W (2020) Fertilizer types shaped the microbial guilds driving the dissimilatory nitrate reduction to ammonia process in a Ferralic Cambisol. Soil Biol Biochem 141:107677
Mago T, Salzberg SL (2011) FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Martínez-Romero E, Aguirre-Noyola JL, Taco-Taype N, Martínez-Romero J, Zuñiga-Dávila D (2020) Plant microbiota modified by plant domestication. Syst Appl Microbiol 43:126106
Martín-Robles N, García-Palacios P, Rodríguez M, Rico D, Vigo R, Sánchez-Moreno S, De Deyn GB, Milla R (2020) Crops and their wild progenitors recruit beneficial and detrimental soil biota in opposing ways. Plant Soil 456:159–173
Mendes R, Kruijt M, De Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. Fems Microbiol Rev 37:634–663
Meyer RS, Purugganan MD (2013) Evolution of crop species: Genetics of domestication and diversification. Nat Rev Genet 14:840–852
Murphy KM, Edwards J, Louie KB, Bowen BP, Sundaresan V, Northen TR, Zerbe P (2021) Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays). Sci Rep-Uk 11:333
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecol Packag 10:719
Pagnoux C, Bouby L, Valamoti SM, Bonhomme V, Ivorra S, Gkatzogia E, Karathanou A, Kotsachristou D, Kroll H, Terral J (2021) Local domestication or diffusion? Insights into viticulture in Greece from Neolithic to Archaic times, using geometric morphometric analyses of archaeological grape seeds. J Archaeol Sci 125:105263
Pérez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 90:635–644
Pérez-Jaramillo JE, Carrión VJ, de Hollander M, Raaijmakers JM (2018) The wild side of plant microbiomes. Microbiome 6:143
Pérez-Jaramillo JE, de Hollander M, Ramírez CA, Mendes R, Raaijmakers JM, Carrión VJ (2019) Deciphering rhizosphere microbiome assembly of wild and modern common bean (Phaseolus vulgaris) in native and agricultural soils from Colombia. Microbiome 7:114
Perez-Jaramillo JE, Carrion VJ, Bosse M, Ferrao L, de Hollander M, Garcia A, Ramirez CA, Mendes R, Raaijmakers JM (2017) Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. Isme J 11:2244–2257
Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140
Rodríguez-Blanco A, Sicardi M, Frioni L (2015) Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fert Soils 51:391–402
Rüger L, Feng K, Dumack K, Freudenthal J, Chen Y, Sun R, Wilson M, Yu P, Sun B, Deng Y (2021) Assembly patterns of the rhizosphere microbiome along the longitudinal root axis of maize (Zea mays L.). Front Microbiol 12:237
Salas-González I, Reyt G, Flis P, Custódio V, Gopaulchan D, Bakhoum N, Dew TP, Suresh K, Franke RB, Dangl JL, Salt DE, Castrillo G (2021) Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis. Science 371:d695
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:1–18
Shenton M, Iwamoto C, Kurata N, Ikeo K (2016) Effect of wild and cultivated rice genotypes on rhizosphere bacterial community composition. Rice 9:1–11
Shi S, Tian L, Nasir F, Li X, Li W, Tran LP, Tian C (2018) Impact of domestication on the evolution of rhizomicrobiome of rice in response to the presence of Magnaporthe oryzae. Plant Physiol Bioch 132:156–165
Singer E, Bonnette J, Kenaley SC, Woyke T, Juenger TE (2019) Plant compartment and genetic variation drive microbiome composition in switchgrass roots. Env Microbiol Rep 11:185–195
Singh DP, Patil HJ, Prabha R, Yandigeri MS, Siddegowda RP (2018) Actinomycetes as potential plant growth-promoting microbial communities. Crop Improv Microb Biotechnol 2018:27–38
Soldan R, Fusi M, Cardinale M, Daffonchio D, Preston GM (2021) The effect of plant domestication on host control of the microbiota. Commun Biol 4:936
Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. Isme J 7:2069–2079
Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, Chougule K, Gao D, Iwata A, Goicoechea JL, Wei S, Wang J, Liao Y, Wang M, Jacquemin J, Becker C, Kudrna D, Zhang J, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu C, Kao S, Zeng J, Wei F, Zhao Q, Feng Q, El Baidouri M, Carpentier M, Lasserre E, Cooke R, Rosa Farias DD, Da Maia LC, Dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan C, Weigel D, Jena KK, Wicker T, Chen M, Han B, Henry R, Hsing YC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long M, Ware D, Wing RA (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50:285–296
Stopnisek N, Shade A (2021) Persistent microbiome members in the common bean rhizosphere: An integrated analysis of space, time, and plant genotype. Isme J 15:2708–2722
Sugawara M, Umehara Y, Kaga A, Hayashi M, Minamisawa K (2019) Symbiotic incompatibility between soybean and Bradyrhizobium arises from one amino acid determinant in soybean Rj2 protein. PLoS One 14:e222469
Tian L, Shi S, Ma L, Nasir F, Li X, Tran LP, Tian C (2018a) Co-evolutionary associations between root-associated microbiomes and root transcriptomes in wild and cultivated rice varieties. Plant Physiol Bioch 128:134–141
Tian L, Shi S, Nasir F, Chang C, Li W, Tran LP, Tian C (2018b) Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses. Rice 11:26
Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant-microbiome interactions: From community assembly to plant health. Nat Rev Microbiol 18:607–621
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206
Veach AM, Morris R, Yip DZ, Yang ZK, Engle NL, Cregger MA, Tschaplinski TJ, Schadt CW (2019) Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin. Microbiome 7:76
Wagner MR (2021) Prioritizing host phenotype to understand microbiome heritability in plants. New Phytol 232:502–509
Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151
Wemheuer F, Taylor JA, Daniel R, Johnston EL, Wemheuer B (2020) Tax4Fun2: Prediction of habitat-specific functional profiles and functional redundancy based on 16S rRNA gene sequences. Environ Microbiome 15:11
Xiao X, Chen W, Zong L, Yang J, Jiao S, Lin Y, Wang E, Wei G (2017) Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Mol Ecol 26:1641–1651
Xiong C, Zhu YG, Wang JT, Singh B, Han LL, Shen JP, Li PP, Wang GB, Wu CF, Ge AH, Zhang LM, He JZ (2021) Host selection shapes crop microbiome assembly and network complexity. New Phytol 229:1091–1104
Yu P, He X, Baer M, Beirinckx S, Tian T, Moya YAT, Zhang X, Deichmann M, Frey FP, Bresgen V, Li C, Razavi BS, Schaaf G, von Wirén N, Su Z, Bucher M, Tsuda K, Goormachtig S, Chen X, Hochholdinger F (2021) Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nat Plants 7:481–499
Zhang F, Xu T, Mao L, Yan S, Chen X, Wu Z, Chen R, Luo X, Xie J, Gao S (2016) Genome-wide analysis of Dongxiang wild rice (Oryza rufipogon Griff.) to investigate lost/acquired genes during rice domestication. Bmc Plant Biol 16:103
Zhang Y, Xu J, Riera N, Jin T, Li J, Wang N (2017) Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome. Microbiome 5:97
Zheng Y, Feng Z, Wang J, Huang X, Lei L, Zhang X, Cao H, Fan D, Yao M, Han D, Li X (2021) Wheat-root associated prokaryotic community: Interplay between plant selection and location. Plant Soil 464:183–197
Zhou J, Deng Y, Zhang P, Xue K, Liang Y, Van Nostrand JD, Yang Y, He Z, Wu L, Stahl DA, Hazen TC, Tiedje JM, Arkin AP (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc Natl Acad Sci USA 111:E836–E845
Acknowledgements
This work was supported by National Natural Science Foundation of China (31870476, 42177106 and 41830755). We gratefully acknowledge the help of all the members from different authoritative institutions for collecting soybean seeds.
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Luo, W., Wang, J., Li, Y. et al. Local domestication of soybean leads to strong root selection and diverse filtration of root-associated bacterial communities. Plant Soil 480, 439–455 (2022). https://doi.org/10.1007/s11104-022-05592-1
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DOI: https://doi.org/10.1007/s11104-022-05592-1