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Domestication of Lima Bean (Phaseolus lunatus) Changes the Microbial Communities in the Rhizosphere

  • Plant Microbe Interactions
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Abstract

Plants modulate the soil microbiota and select a specific microbial community in the rhizosphere. However, plant domestication reduces genetic diversity, changes plant physiology, and could have an impact on the associated microbiome assembly. Here, we used 16S rRNA gene sequencing to assess the microbial community in the bulk soil and rhizosphere of wild, semi-domesticated, and domesticated genotypes of lima bean (Phaseolus lunatus), to investigate the effect of plant domestication on microbial community assembly. In general, rhizosphere communities were more diverse than bulk soil, but no differences were found among genotypes. Our results showed that the microbial community’s structure was different from wild and semi-domesticated as compared to domesticated genotypes. The community similarity decreased 57.67% from wild to domesticated genotypes. In general, the most abundant phyla were Actinobacteria (21.9%), Proteobacteria (20.7%), Acidobacteria (14%), and Firmicutes (9.7%). Comparing the different genotypes, the analysis showed that Firmicutes (Bacillus) was abundant in the rhizosphere of the wild genotypes, while Acidobacteria dominated semi-domesticated plants, and Proteobacteria (including rhizobia) was enriched in domesticated P. lunatus rhizosphere. The domestication process also affected the microbial community network, in which the complexity of connections decreased from wild to domesticated genotypes in the rhizosphere. Together, our work showed that the domestication of P. lunatus shaped rhizosphere microbial communities from taxonomic to a functional level, changing the abundance of specific microbial groups and decreasing the complexity of interactions among them.

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Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Abdelfattah A, Tack AJM, Wasserman B et al (2021) Evidence for host–microbiome co‐evolution in apple. New Phytol.https://doi.org/10.1111/NPH.17820

  2. Abdullaeva Y, Manirajan BA, Honermeier B, Schnell S, Cardinale M (2021) Domestication affects the composition, diversity, and co-occurrence of the cereal seed microbiota. J. Adv. Res. 31:75–86. https://doi.org/10.1016/j.jare.2020.12.008

    Article  CAS  PubMed  Google Scholar 

  3. Abdullaeva Y, Ratering S, Manirajan BA, Rosado-Porto D, Schnell S, Cardinale M (2022) Domestication impacts the wheat-associated microbiota and the rhizosphere colonization by seed- and soil-originated microbiomes, across different fields. Front. Plant Sci. 12:806915. https://doi.org/10.3389/fpls.2021.806915

    Article  PubMed  PubMed Central  Google Scholar 

  4. Aguilar OM, Riva O, Peltzer E (2004) Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc. Natl. Acad. Sci. 101:13548–13553. https://doi.org/10.1073/pnas.0405321101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Anderson MJ (2001) A new method for non parametric multivariate analysis of variance. Austral. Ecol. 26:32–46

    Google Scholar 

  6. Andueza-Noh RH, Martha L, Serrano-Serrano MI et al (2013) Multiple domestications of the Mesoamerican gene pool of lima bean (Phaseolus lunatus L.): evidence from chloroplast DNA sequences. Gen. Res. Crop. Evol. 60:1069–1086

    Article  CAS  Google Scholar 

  7. Araujo FF, Bonifacio A, Bavaresco LG et al (2021) Bacillus subtilis changes the root architecture of soybean grown on nutrient-poor substrate. Rhizosphere 18:16–19. https://doi.org/10.1016/j.rhisph.2021.100348

    Article  Google Scholar 

  8. Assunção IP, Nascimento LD, Ferreira MF et al (2011) Reaction of faba bean genotypes to Rhizoctonia solani and resistance stability. Hortic. Bras. 29:492–497. https://doi.org/10.1590/S0102-05362011000400008

    Article  Google Scholar 

  9. Bastian M, Heymann S, Jacomy M (2009) Gephi: An open source software for exploring and manipulating networks. In Proceedings of the Third International ICWSM Conference. California, USA. 361– 362

  10. Bellucci E, Bitocchi E, Ferrarini A et al (2014) Decreased nucleotide and expression diversity and modified coexpression patterns characterize domestication in the common bean. Plant Cell 26:1901–1912. https://doi.org/10.1105/TPC.114.124040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bitocchi E, Rau D, Bellucci E, Rodriguez M et al (2017) Beans (Phaseolus ssp.) as a model for understanding crop evolution. Front. Pl. Sci. 8:722. https://doi.org/10.3389/fpls.2017.00722

  12. Brisson VL, Schmidt JE, Northen TR (2019) Impacts of maize domestication and breeding on rhizosphere microbial community recruitment from a nutrient depleted agricultural soil. Sci Rep 9:15611. https://doi.org/10.1038/s41598-019-52148-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bulgarelli D, Garrido-Oter R, Münch PC et al (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microb 17:392–403

    Article  CAS  Google Scholar 

  14. Chacón-Sánchez MI, Martínez-Castillo J (2017) Testing domestication scenarios of lima bean (Phaseolus lunatus L.) in Mesoamerica: insights from genome-wide genetic markers. Front. Plant Sci. 8:1551. https://doi.org/10.3389/fpls.2017.01551.

  15. Chouhan GK, Verma JP, Jaiswal DK et al (2021) Phytomicrobiome for promoting sustainable agriculture and food security: Opportunities, challenges, and solutions. Microbiol Res 248:126763

    Article  CAS  PubMed  Google Scholar 

  16. Costa CN, Antunes JEL, Lopes ACA, Freitas ADS, Araujo ASF (2020) Inoculation of rhizobia increases lima bean (Phaseolus lunatus) yield in soils from Piauí and Ceará states, Brazil. Rev Ceres 67:419–423

    Article  Google Scholar 

  17. Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  CAS  PubMed  Google Scholar 

  18. Ferguson SJ, Richardson DJ, Van Spanning RJM (2007) Biochemistry and molecular biology of nitrification. Biol. Nitrogen Cycle 209–222https://doi.org/10.1016/B978-044452857-5.50015-1

  19. Fernie AR, Yan J (2019) De Novo domestication: an alternative route toward new crops for the future. Mol. Plant 12:615–631

    Article  CAS  PubMed  Google Scholar 

  20. Freytag GF, Debouck DG (2002) Taxonomy, distribution, and ecology of the genus Phaseolus (Leguminosae-Papilionoideae) in North America, Mexico and Central America. Bot. Res. Ins. Texas.

  21. Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput. Biol. 8:e1002687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Goss-Souza D, Mendes LW, Rodrigues JLM, Tsai SM (2019) Ecological processes sha** bulk soil and rhizosphere microbiome assembly in a long-term Amazon Forest-to-agriculture conversion. Microb. Ecol. 79:110–122

    Article  PubMed  Google Scholar 

  23. Gray DA, Dugar G, Gamba P et al (2019) Extreme slow growth as alternative strategy to survive deep starvation in bacteria. Nat. Commun. 101:1–12. https://doi.org/10.1038/s41467-019-08719-8

    Article  CAS  Google Scholar 

  24. Gross BL, Olsen KM (2010) Genetic perspectives on crop domestication. Trends Plant Sci. 15:529–537. https://doi.org/10.1016/j.tplants.2010.05.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol. Electron. 4:1–9

    Google Scholar 

  26. Kalam S, Basu A, Ahmad I et al (2020) Recent understanding of soil Acidobacteria and their ecological significance: a critical review. Front. Microbiol. 11:580024. https://doi.org/10.3389/fmicb.2020.580024

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ladygina N, Hedlund K (2010) Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol. Biochem. 42:162–168. https://doi.org/10.1016/j.soilbio.2009.10.009

    Article  CAS  Google Scholar 

  28. López-Mondéjar R, Zühlke D, Becher D et al (2016) Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci. Rep. 6:1–12. https://doi.org/10.1038/srep25279

    Article  CAS  Google Scholar 

  29. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 8:1577–1587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mendes LW, Mendes R, Raaijmakers JM, Tsai SM (2018a) Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean. ISME J.https://doi.org/10.1038/s41396-018-0234-6

  31. Mendes LW, Raaijmakers JM, Hollander M, Mendes R, Tsai SM (2018) Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME J. 12:212–224

    Article  PubMed  Google Scholar 

  32. Mendes R, Kruijt M, De Bruijn I et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    Article  CAS  PubMed  Google Scholar 

  33. Mitter B, Pfaffenbichler N, Flavell R et al (2017) A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front. Microbiol. 8:1–10. https://doi.org/10.3389/fmicb.2017.00011

    Article  Google Scholar 

  34. Moroenyane I, Mendes LW, Trembley J, Tripathi B, Yergeau É (2021) Plant compartments and developmental stages modulate the balance between niche-based and neutral processes in soybean microbiome. Microbial. Ecol. 82:416–428

    Article  CAS  Google Scholar 

  35. Motta-Aldana JR, Serrano-Serrano ML, Hernández-Torres J et al (2010) Multiple Origins of Lima Bean Landraces in the Americas: Evidence from Chloroplast and Nuclear DNA Polymorphisms. Crop Sci. 50:1773

    Article  CAS  Google Scholar 

  36. Oliveiros JC (2007) VENNY. An interactive tool for comparing lists with Venn diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html.

  37. Pérez-Jaramillo J, Carrión V, Bosse M et al (2017) Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J. 11:2244–2257. https://doi.org/10.1038/ismej.2017.85

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pérez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol. Biol. 90:635–644. https://doi.org/10.1007/S11103-015-0337-7

    Article  PubMed  Google Scholar 

  39. Pérez-Jaramillo HM, 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 

  40. Pickersgill B (2007) Domestication of plants in the Americas: insights from mendelian and molecular genetics. Ann. Botany 100:925–940. https://doi.org/10.1093/aob/mcm193

    Article  Google Scholar 

  41. Praeg N, Illmer P (2020) Microbial community composition in the rhizosphere of Larix decidua under different light regimes with additional focus on methane cycling microorganisms. Sci. Rep. 10:22324. https://doi.org/10.1038/s41598-020-79143-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Preece C, Livarda A, Christin PA et al (2017) How did the domestication of Fertile Crescent grain crops increase their yields? Funct. Ecol. 31:387–397. https://doi.org/10.1111/1365-2435.12760

    Article  PubMed  Google Scholar 

  43. Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848. https://doi.org/10.1038/nature07895

    Article  CAS  PubMed  Google Scholar 

  44. Rossmann M, Pérez-Jaramillo JE, Kavamura VN et al (2020) Multitrophic interactions in the rhizosphere microbiome of wheat: from bacteria and fungi to protists. FEMS Microbiol. Ecol. 96:fiaa032.

  45. Sansinenea E (2019) Bacillus spp.: As plant growth-promoting bacteria. Secondary Metabolites of Plant Growth Promoting Rhizomicroorganisms. 225–237. https://doi.org/10.1007/978-981-13-5862-3_11

  46. Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol. 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  47. Singh J, Sun M, Cannon SB et al (2021) An accumulation of genetic variation and selection across the disease-related genes during apple domestication. Tree Genet. Genomes 17:1–11. https://doi.org/10.1007/S11295-021-01510-1/FIGURES/5

    Article  Google Scholar 

  48. Soldan R, Fusi M, Cardinale M et al (2021) The effect of plant domestication on host control of the microbiota. Commun. Biol. 4:1–9. https://doi.org/10.1038/s42003-021-02467-6

    Article  Google Scholar 

  49. Spor A, Roucou A, Mounier A (2020) Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat. Sci. Rep. 10:12234. https://doi.org/10.1038/s41598-020-69175-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Van Elsas JD, Chiurazzi M, Mallon CA et al (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. USA 109:1159–1164

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wei Z, Jousset A (2017) Plant breeding goes microbial. Trends Plant Sci. 22:555–558. https://doi.org/10.1016/j.tplants.2017.05.009

    Article  CAS  PubMed  Google Scholar 

  52. Wei Z, Yang T, Friman VP et al (2015) Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6:8413

    Article  CAS  PubMed  Google Scholar 

  53. **ong W, Song Y, Yang K et al (2020) Rhizosphere protists are key determinants of plant health. Microbiome 8:1–9. https://doi.org/10.1186/s40168-020-00799-9

    Article  Google Scholar 

  54. Yadav A, Borrelli JC, Elshahed MS, Youssef NH (2021) Genomic analysis of family UBA6911 (Group 18 Acidobacteria) expands the metabolic capacities of the phylum and highlights adaptations to terrestrial habitats. Appl. Environ. Microbiol. 87:1–19. https://doi.org/10.1128/AEM.00947-21

    Article  Google Scholar 

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Acknowledgements

This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnologico–CNPq (grant 305069/2018-1). and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES (Code 001). The authors thank to the Centro de Genética e Bioinformática (CeGenBio) from the Unit of Research (NPDM/UFC). Josieli Lima da Silva, Sandra Mara Barbosa Rocha, Jadson Emanuel Lopes Antunes, and Veronica Brito Silva thank CAPES for their fellowship. Ademir Sergio Ferreira de Araujo, Vania Maria Maciel Melo, Regina Lucia Ferreira Gomes, and Angela Celis de Almeida Lopes thank CNPq for their fellowship of research. Lucas William Mendes thanks FAPESP for his fellowship.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnologico – CNPq (grant 305069/2018–1).

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Authors and Affiliations

  1. Plant Genetic Resource Group, Agricultural Science Center, Federal University of Piauí, Teresina, PI, Brazil

    Josieli Lima da Silva, Gérson do Nascimento Costa, Veronica Brito da Silva, Regina Lucia Ferreira Gomes & Angela Celis de Almeida Lopes

  2. Center for Nuclear Energy in Agriculture, University of Sao Paulo, Piracicaba, SP, Brazil

    Lucas William Mendes

  3. Soil Microbial Ecology Group, Agricultural Science Center, Federal University of Piauí, Teresina, PI, Brazil

    Sandra Mara Barbosa Rocha, Jadson Emanuel Lopes Antunes, Louise Melo de Souza Oliveira & Ademir Sérgio Ferreira Araujo

  4. Laboratório de Ecologia Microbiana E Biotecnologia, Federal University of Ceará, Fortaleza, CE, Brazil

    Vania Maria Maciel Melo & Francisca Andrea Silva Oliveira

  5. Soil Science Department, Federal University of Ceará, Fortaleza, CE, Brazil

    Arthur Prudêncio de Araujo Pereira

  6. Plant Science Department, Agricultural Science Center, Federal University of Piauí, Teresina, PI, Brazil

    Francisco de Alcantara Neto

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  1. Josieli Lima da Silva
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  2. Lucas William Mendes
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  5. Louise Melo de Souza Oliveira
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Contributions

ASFA, ACAL, and RLFG conceived this study. JLS, SMBR, JELA, and LMSO conducted the experiment, collected samples, and proceeded DNA extraction. VMMM and FASO provided the sequencing. APAP and LWM provided the bioinformatic and the 16S rRNA gene data. LWM, APAP, GNC, and VBS performed the statistical, network analyses and generate the results. ASFA, APAP, LWM, VMMM, ACAL, and FAN interpreted the results and elaborated the main arguments. All authors wrote and reviewed and the final manuscript.

Corresponding author

Correspondence to Ademir Sérgio Ferreira Araujo.

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da Silva, J.L., Mendes, L.W., Rocha, S.M.B. et al. Domestication of Lima Bean (Phaseolus lunatus) Changes the Microbial Communities in the Rhizosphere. Microb Ecol 85, 1423–1433 (2023). https://doi.org/10.1007/s00248-022-02028-2

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