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Dedomestication of modern soybean is potentially revealed by variation in the root-associated bacterial community along a domestication gradient

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Abstract

Aims

The plant root-associated microbial community, which is influenced by plant species and environmental factors, supports host growth by providing nutrients and facilitating stress resistance. However, the effect of modern breeding technology on this community has not been thoroughly investigated.

Methods

In this study, the root-associated (rhizosphere and root endosphere) bacterial communities of four types (wild, semiwild, landrace, and modern) of soybean varieties distributed along an evolutionary transect were investigated using 16S rRNA gene amplicon sequencing.

Results

The alpha-diversity indices, composition and ecological assembly process based on null models of the root-associated bacterial community, especially the rhizosphere community, of modern soybean were more similar to those of the wild variety than to those of semiwild and landrace varieties. Patterns of co-occurrence showed that the root-associated bacterial communities of wild and modern soybeans were more complex than those of the other soybeans. The core bacterial taxa among the four types of soybean varieties mainly belonged to order Rhizobiales, which was most abundant in modern soybean. Source tracking analysis further revealed that the root-associated bacterial communities of the semiwild, landrace and modern varieties were mainly derived from those of the wild, semiwild and landrace varieties, respectively.

Conclusions

The similarity of root-associated bacterial community between modern and wild soybeans during domestication may reveal the dedomestication of modern soybean. The findings of this study expand our understanding of crop root-associated microbial selection under domestication and are highly significant for the advancement of modern breeding and understanding of biological evolution involving plant-microbe symbiosis.

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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.:PRJNA 841416).

References

  • Allito BB, Ewusi-Mensah N, Logah V (2020) Legume-rhizobium strain specificity enhances nutrition and nitrogen fixation in faba bean (Vicia faba L.). Agronomy 10:826

    Article  CAS  Google Scholar 

  • Alseekh S, Scossa F, Wen W, Luo J, Yan J, Beleggia R, Klee HJ, Huang S, Papa R, Fernie AR (2021) Domestication of crop metabolomes: desired and unintended consequences. Trends Plant Sci 26:650–661

    Article  CAS  PubMed  Google Scholar 

  • Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci U S A 115:6506–6511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. ICWSM 8:361–362

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Waghmode TR, Sun R, Kuramae E, Hu C, Liu B (2019) Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 7:136

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–6

  • Doebley JF, GauT BS, Smith BD (2007) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  Google Scholar 

  • 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 U S A 112:E911–E920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y (2015) Understanding crop genetic diversity under modern plant breeding. Theor Appl Genet 128:2131–2142

    Article  PubMed  PubMed Central  Google Scholar 

  • Funatsuki H, Suzuki M, Hirose A, Inaba H, Yamada T, Hajika M, Komatsu K, Katayama T, Sayama T, Ishimoto M, Fujino K (2014) Molecular basis of a shattering resistance boosting global dissemination of soybean. Proc Natl Acad Sci U S A 111:17797–17802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gepts P (2002) A comparison between crop domestication, classical plant breeding, and genetic engineering. Crop Sci 42:1780–1790

    Article  Google Scholar 

  • Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed Rev 24:1–44

    Google Scholar 

  • Gering E, Incorvaia D, Henriksen R, Conner J, Getty T, Wright D (2019) Getting back to nature: feralization in animals and plants. Trends Ecol Evol 34:1137–1151

  • Ginestet C (2011) Ggplot2: elegant graphics for data analysis. J Royal Stat Soc: Ser A (Stat Soc) 174:245–246

    Article  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Guo X, Feng J, Shi Z, Zhou X, Yuan M, Tao X, Hale L, Yuan T, Wang J, Qin Y, Zhou A, Fu Y, Wu L, He Z, Van Nostrand JD, Ning D, Liu X, Luo Y, Tiedje JM et al (2018) Climate warming leads to divergent succession of grassland microbial communities. Nat Clim Chang 8:813–818

    Article  Google Scholar 

  • Hammer K (1984) Das domestikationssyndrom. Die. Kulturpflanze 32:11–34

    Article  Google Scholar 

  • Hyten DL, Song QJ, Zhu YL, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci U S A 103:16666–16671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassambara A, Kassambara MA (2020) Package “ggpubr”. R package version 0.1 6. https://CRAN.R-project.org/package=ggpubr. Accessed 14 Nov 2017

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the core microbiota be functional. Trends Plant Sci 22:583–595

    Article  CAS  PubMed  Google Scholar 

  • Lenser T, Theißen G (2013) Molecular mechanisms involved in convergent crop domestication. Trends Plant Sci 18:704–714

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zhou G, Ma J, Jiang W, Jin L, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, Zhang S, Zuo Q, Shi X, Li Y, Zhang W, Hu Y, Kong G, Hong H, Tan B et al (2014) De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol 32:1045–1052

    Article  CAS  PubMed  Google Scholar 

  • Li E, de Jonge R, Liu C, Jiang H, Friman V, Pieterse CMJ, Bakker PAHM and Jousset A (2021) Rapid evolution of bacterial mutualism in the plant rhizosphere. Nat Commun 12:3829

  • Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME (2019) Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol 19:201

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466

    Article  CAS  PubMed  Google Scholar 

  • McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menéndez E, Paço A (2020) Is the application of plant probiotic bacterial consortia always beneficial for plants? Exploring synergies between Rhizobial and non-Rhizobial bacteria and their effects on agro-economically valuable crops. Life 10:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz N, Qi X, Li M, Xie M, Gao Y, Cheung M, Wong F, Lam H (2016) Improvement in nitrogen fixation capacity could be part of the domestication process in soybean. Heredity 117:84–93

    Article  PubMed  PubMed Central  Google Scholar 

  • Ning D, Deng Y, Tiedje JM, Zhou J (2019) A general framework for quantitatively assessing ecological stochasticity. Proc Natl Acad Sci U S A 116:16892–16898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, MHH S, Oksanen MJ, Suggests M (2007) The vegan package. Commun Ecol Pack 10:719

    Google Scholar 

  • Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2014) Selection on soil microbiomes reveals reproducible impacts on plant function. Isme J 9:980

    Article  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Jaramillo JE, Carrión VJ, de Hollander M, Raaijmakers JM (2018) The wild side of plant microbiomes. Microbiome 6:143

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu L, Chen P, Liu Z, Li Y, Guan R, Wang L, Chang R (2011) The worldwide utilization of the chinese soybean germplasm collection. Plant Genetic Resources 9:109–122

  • Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110:859–864

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41

    Article  CAS  PubMed  Google Scholar 

  • Scossa F, Fernie AR (2021) When a crop goes back to the wild: feralization. Trends Plant Sci 26:543–545

  • Sedivy EJ, Wu F, Hanzawa Y (2017) Soybean domestication: the origin, genetic architecture and molecular bases. New Phytol 214:539–553

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandenkoornhuyse P, Quaiser A, Duhamel M, Van AL, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206

    Article  PubMed  Google Scholar 

  • Walker R, Agapakis CM, Watkin E, Hirsch AM (2015) In: de Bruijn FJ (ed) Symbiotic nitrogen fixation in legumes: perspectives on the diversity and evolution of nodulation by Rhizobium and Burkholderia species. Wiley, Hoboken, pp 913–925

    Google Scholar 

  • Wang W, Chen L, Wang X, Duan J, Flynn RD, Wang Y, Clark CB, Sun L, Zhang D, Wang DR, Kessler SA, Ma J (2021) A transposon-mediated reciprocal translocation promotes environmental adaptation but compromises domesticability of wild soybeans. New Phytol 232:1765–1777

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Lao S, Fan L (2021) De-domestication: an extension of crop evolution. Trends Plant Sci 26:560–574

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yu G, Smith DK, Zhu H, Guan Y, Lam TTY (2017) Ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36

    Article  Google Scholar 

  • Zhang H, Mittal N, Leamy LJ, Barazani O, Song B (2017) Back into the wild-apply untapped genetic diversity of wild relatives for crop improvement. Evol Appl 10:5–24

    Article  PubMed  Google Scholar 

  • Zhang N, Nunan N, Hirsch PR, Sun B, Zhou J, Liang Y (2021) Theory of microbial coexistence in promoting soil-plant ecosystem health. Biol Fert Soils 57:897–911

    Article  Google Scholar 

  • Zheng Y, Gong X (2019) Niche differentiation rather than biogeography shapes the diversity and composition of microbiome of Cycas panzhihuaensis. Microbiome 7:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Ning D (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol R 81:e2–e17

    Article  Google Scholar 

  • Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH, Weinl S, Freschi L, Voytas DF, Kudla J, Peres LEP (2018) De novo domestication of wild tomato using genome editing. Nat Biotechnol 36:1211–1216

    Article  Google Scholar 

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Acknowledgments

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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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, 3 Taicheng Road, Yangling, Shaanxi, 712100, People’s Republic of China

    Wen Luo, Yuanli Li, Haofei Zhang, Tianjiao Lei, Jieli Wang, Gehong Wei & Weimin Chen

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  1. Wen Luo
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  2. Yuanli Li
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  3. Haofei Zhang
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Correspondence to Weimin Chen.

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Luo, W., Li, Y., Zhang, H. et al. Dedomestication of modern soybean is potentially revealed by variation in the root-associated bacterial community along a domestication gradient. Plant Soil 489, 507–522 (2023). https://doi.org/10.1007/s11104-023-06033-3

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