Abstract
Background and aims
Seed associated microbial communities are an important part of the plant microbiota. However, for legumes, seed microbiota and their life cycle including colonization and vertical transmission to nodule remain largely unknown. Here we explored the sources of seed microbes and tested the hypothesis that the plant microbiota is partially inherited through vertical transmission.
Methods
Nodules, rhizosphere soil and seeds were collected from Sophora davidii grown in fields, and from inoculation test with fermentation broth of nodule endophytes. Additionally, structure of seed microbial communities and vertical transmission of seed microbes across one plant generations were assessed through amplicon sequencing of bacterial 16S rRNA gene.
Results
A total of 4074 endophytic OTUs were detected from S. davidii seeds, in which 233 shared with rhizosphere and nodules were defined as core microbiota of this plant, including various rhizobia. The core microbiota of S. davidii seeds was vertically transmitted to the nodules of upcoming generation of plants. Moreover, Firmicutes was the dominant phylum in S. davidii seeds. Notably, the dominant bacteria changed from Mesorhizobium in the field nodules to Sinorhizobium in the passage nodules in pot culture with inoculation.
Conclusions
Diverse microbial community habited in S. davidii seeds, including various rhizobia. The core microbiota could be transmitted from seeds to nodules, including the rhizobial endophytes, which made S. davidii plants potential to nodulated with distinct rhizobia in different environments, as revealed by the changed of dominant genus from Mesorhizobium to Sinorhizobium in an artificial condition. This study gives empirical evidence for the source, colonization and vertical transmission routes of S. davidii seed bacterial communities.
Similar content being viewed by others
Data availability
All data have been uploaded to NCBI and can be provided according to the needs of readers.
References
Abdelfattah A, Wisniewski M, Schena L, Tack AJM (2021) Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environ Microbiol 23:2199–2214. https://doi.org/10.1111/1462-2920.15392
Bender FR, Alves LC, da Silva JFM, Ribeiro RA, Pauli G, Nogueira MA, Hungria M (2022) Microbiome of nodules and roots of soybean and common bean: searching for differences associated with contrasting performances in symbiotic nitrogen fixation. Int J Mol Sci 23. https://doi.org/10.3390/ijms231912035
Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276
Bragina A, Berg C, Cardinale M, Shcherbakov A, Chebotar V, Berg G (2012) Sphagnum mosses harbour highly specific bacterial diversity during their whole lifecycle. ISME J 6:802–813. https://doi.org/10.1038/ismej.2011.151
Burns M, Epstein B, Burghardt LT (2021) Comparison of nodule endophyte composition, diversity, and gene content between medicago truncatula genotypes. Phytobiomes J 5:400–407. https://doi.org/10.1094/PBIOMES-10-20-0077-R
Cao Y, Tie D, Zhao JL, Wang XB, Yi JJ, Chai YF, Wang KF, Wang ET, Yue M (2021) Diversity and distribution of Sophora davidii rhizobia in habitats with different irradiances and soil traits in Loess Plateau area of China. Syst Appl Microbiol 44:126224. https://doi.org/10.1016/j.syapm.2021.126224
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. https://doi.org/10.1038/nmeth.f.303
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522. https://doi.org/10.1073/pnas.1000080107
Chen T, Zhang H, Liu Y, Liu Y-X, Huang L (2021) EVenn: Easy to create repeatable and editable Venn diagrams and Venn networks online. J Genet Genomics 48:863–866. https://doi.org/10.1016/j.jgg.2021.07.007
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. https://doi.org/10.1128/aem.71.9.4951-4959.2005
Dai Y, Li XY, Wang Y, Li CX, He Y, Lin HH, Wang T, Ma XR (2020) The differences and overlaps in the seed-resident microbiome of four Leguminous and three Gramineous forages. Microb Biotechnol 13:1461–1476. https://doi.org/10.1111/1751-7915.13618
de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033. https://doi.org/10.1038/s41467-018-05516-7
Deng ZS, Kong ZY, Zhang BC, Zhao LF (2020) Insights into non-symbiotic plant growth promotion bacteria associated with nodules of Sphaerophysa salsula growing in northwestern China. Arch Microbiol 202:399–409. https://doi.org/10.1007/s00203-019-01752-7
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Fang D, Wu A, Huang L, Shen Q, Zhang Q, Jiang L, Ji F (2020) Polymer substrate reshapes the microbial assemblage and metabolic patterns within a biofilm denitrification system. Chem Eng J 387:124128. https://doi.org/10.1016/j.cej.2020.124128
Ferguson BJ, Mens C, Hastwell AH, Zhang M, Su H, Jones CH, Chu X, Gresshoff PM (2019) Legume nodulation: The host controls the party. Plant Cell Environ 42:41–51. https://doi.org/10.1111/pce.13348
Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14. https://doi.org/10.1111/j.1574-6968.2008.01258.x
Fort T, Pauvert C, Zanne AE, Ovaskainen O, Caignard T, Barret M, Compant S, Hampe A, Delzon S, Vacher C (2021) Maternal effects shape the seed mycobiome in Quercus petraea. New Phytol 230:1594–1608. https://doi.org/10.1111/nph.17153
Gandolfi I, Bertolini V, Ambrosini R, Bestetti G, Franzetti A (2013) Unravelling the bacterial diversity in the atmosphere. Appl Microbiol Biotechnol 97:4727–4736. https://doi.org/10.1007/s00253-013-4901-2
Gopal M, Gupta A (2016) Microbiome selection could spur next-generation plant breeding strategies. Front Microbiol 7:1971. https://doi.org/10.3389/fmicb.2016.01971
Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. https://doi.org/10.1101/gr.112730.110
Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PloS one 7:e30438. https://doi.org/10.1371/journal.pone.0030438
Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58. https://doi.org/10.1186/s40168-018-0445-0
Hodgson S, de Cates C, Hodgson J, Morley NJ, Sutton BC, Gange AC (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208. https://doi.org/10.1002/ece3.953
Jiao YS, Liu YH, Yan H, Wang ET, Tian CF, Chen WX, Guo BL, Chen WF (2015) Rhizobial diversity and nodulation characteristics of the extremely promiscuous legume Sophora flavescens. Mol Plant-Microbe Interact: MPMI 28:1338–1352. https://doi.org/10.1094/mpmi-06-15-0141-r
Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PloS one 6:e20396. https://doi.org/10.1371/journal.pone.0020396
Khalaf EM, Raizada MN (2018) Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Front Microbiol 9:42. https://doi.org/10.3389/fmicb.2018.00042
Klaedtke S, Jacques MA, Raggi L, Préveaux A, Bonneau S, Negri V, Chable V, Barret M (2016) Terroir is a key driver of seed-associated microbial assemblages. Environ Microbiol 18:1792–1804. https://doi.org/10.1111/1462-2920.12977
Li J, Jia-Min A, Xiao-Dong L, Ying-Ying J, Chao-Chao Z, Rui-Hua Z, Zhen-Shan D (2022) Environmental filtering drives the establishment of the distinctive rhizosphere, bulk, and root nodule bacterial communities of Sophora davidii in hilly and gully regions of the Loess Plateau of China. Front Microbiol 13:945127. https://doi.org/10.3389/fmicb.2022.945127
Links MG, Demeke T, Gräfenhan T, Hill JE, Hemmingsen SM, Dumonceaux TJ (2014) Simultaneous profiling of seed-associated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds. New Phytol 202:542–553. https://doi.org/10.1111/nph.12693
López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327. https://doi.org/10.1016/j.syapm.2010.07.005
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/aem.71.12.8228-8235.2005
Luo JR, Li BB, Zhang FB, Cong PJ, Wang WH, Yang MY (2021) Responses of soil erosion to changes in landscape pattern and its evolution in watershed in the loess hilly region under characteristic management and development. J Appl Ecol 32:4165–4176. https://doi.org/10.13287/j.1001-9332.202112.006
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England) 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L, Petric A, Berninger T, Naveed M, Sheibani-Tezerji R, von Maltzahn G, Sessitsch A (2017) A new approach to modify plant microbiomes and traits by introducing beneficial Bacteria at flowering into Progeny Seeds. Front Microbiol 8:11. https://doi.org/10.3389/fmicb.2017.00011
Newcombe G, Harding A, Ridout M, Busby PE (2018) A hypothetical bottleneck in the plant microbiome. Front Microbiol 9:1645. https://doi.org/10.3389/fmicb.2018.01645
Pérez-Ramírez NO, Rogel MA, Wang E, Castellanos JZ, Martínez-Romero E (1998) Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol Ecol 26:289–296. https://doi.org/10.1016/S0168-6496(98)00043-9
Pham VH, Kim J (2012) Cultivation of unculturable soil bacteria. Trends Biotechnol 30:475–484. https://doi.org/10.1016/j.tibtech.2012.05.007
Pitzschke A (2016) Developmental peculiarities and seed-borne endophytes in Quinoa: omnipresent, robust Bacilli contribute to plant fitness. Front Microbiol 7:2. https://doi.org/10.3389/fmicb.2016.00002
Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408. https://doi.org/10.1016/j.envexpbot.2009.04.007
Ringelberg D, Foley K, Reynolds CM (2012) Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol 58:67–80. https://doi.org/10.1139/w11-122
Rosenberg E, Zilber-Rosenberg I (2018) The hologenome concept of evolution after 10 years. Microbiome 6:78. https://doi.org/10.1186/s40168-018-0457-9
Rybakova D, Mancinelli R, Wikström M, Birch-Jensen AS, Postma J, Ehlers RU, Goertz S, Berg G (2017) The structure of the Brassica napus seed microbiome is cultivar-dependent and affects the interactions of symbionts and pathogens. Microbiome 5:104. https://doi.org/10.1186/s40168-017-0310-6
Samreen T, Naveed M, Nazir MZ, Asghar HN, Khan MI, Zahir ZA, Kanwal S, Jeevan B, Sharma D, Meena VS, Meena SK, Sarkar D, Devika OS, Parihar M, Choudhary M (2021) Seed associated bacterial and fungal endophytes: Diversity, life cycle, transmission, and application potential. Appl Soil Ecol 168:104191. https://doi.org/10.1016/j.apsoil.2021.104191
Schauer S, Kutschera U (2011) A novel growth-promoting microbe, Methylobacterium funariae sp. nov., isolated from the leaf surface of a common moss. Plant Signal Behav 6:510–515. https://doi.org/10.4161/psb.6.4.14335
Shade A, Jacques MA, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22. https://doi.org/10.1016/j.mib.2017.03.010
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Sharaf H, Rodrigues RR, Moon J, Zhang B, Mills K, Williams MA (2019) Unprecedented bacterial community richness in soybean nodules vary with cultivar and water status. Microbiome 7:63. https://doi.org/10.1186/s40168-019-0676-8
Simonin M, Briand M, Chesneau G, Rochefort A, Marais C, Sarniguet A, Barret M (2022) Seed microbiota revealed by a large-scale meta-analysis including 50 plant species. New Phytol 234:1448–1463. https://doi.org/10.1111/nph.18037
Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160. https://doi.org/10.1128/jb.00345-12
Tan HW, Heenan PB, De Meyer SE, Willems A, Andrews M (2015) Diverse novel mesorhizobia nodulate New Zealand native Sophora species. Syst Appl Microbiol 38:91–98. https://doi.org/10.1016/j.syapm.2014.11.003
Thomas P, Shaik SP (2020) Molecular profiling on surface-disinfected Tomato seeds reveals high diversity of cultivation-recalcitrant endophytic Bacteria with low shares of spore-forming Firmicutes. Microb Ecol 79:910–924. https://doi.org/10.1007/s00248-019-01440-5
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. https://doi.org/10.1038/s41579-020-0412-1
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol (Stuttg) 15:971–981. https://doi.org/10.1111/j.1438-8677.2012.00711.x
Truyens S, Jambon I, Croes S, Janssen J, Weyens N, Mench M, Carleer R, Cuypers A, Vangronsveld J (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int J Phytorem 16:643–659. https://doi.org/10.1080/15226514.2013.837027
Wang ET, Tan ZY, Guo XW, Rodríguez-Duran R, Boll G, Martínez-Romero E (2006) Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch Microbiol 186:251–259. https://doi.org/10.1007/s00203-006-0141-5
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. https://doi.org/10.1111/mec.14027
Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R, Ragan MA, Schmidt S, Hugenholtz P (2017) Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat Commun 8:215. https://doi.org/10.1038/s41467-017-00262-8
Yin C, Casa Vargas JM, Schlatter DC, Hagerty CH, Hulbert SH, Paulitz TC (2021) Rhizosphere community selection reveals bacteria associated with reduced root disease. Microbiome 9:86. https://doi.org/10.1186/s40168-020-00997-5
Zhao L, Deng Z, Yang W, Cao Y, Wang E, Wei G (2010) Diverse rhizobia associated with Sophora alopecuroides grown in different regions of Loess Plateau in China. Syst Appl Microbiol 33:468–477. https://doi.org/10.1016/j.syapm.2010.08.004
Zhao L, Xu Y, Lai X (2018) Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Braz J Microbiol : [publication of the Brazilian Society for Microbiology] 49:269–278. https://doi.org/10.1016/j.bjm.2017.06.007
Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2. https://doi.org/10.1128/mBio.00122-11
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 32160003).
Funding
This work was supported by the National Natural Science Foundation of China (Grant No. 32160003).
Author information
Authors and Affiliations
Contributions
Jiamin Ai: Experimentation, Writing–original draft. Tianfei Yu: Data curation, Software. Xiaodong Liu: Conceptualization, Methodology. Yingying Jiang: Conceptualization, Methodology. Entao Wang: Writing–review & editing. ZhenShan Deng: Methodology, Project administration, Writing–review & editing.
Corresponding author
Ethics declarations
Disclosure of potential conflicts of interest
The authors declare that there is no conflict of interest.
Additional information
Responsible Editor: Ulrike Mathesius.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Highlights
1. Diverse microbial community in S. davidii seeds were revealed.
2. Various rhizobia were a part of the seed microbiota.
3. Core microbiota in seeds could be transmitted to nodules.
4. Dominant rhizobial taxa in nodules changed in different habitats.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ai, J., Yu, T., Liu, X. et al. Seed associated microbiota and vertical transmission of bacterial communities from seed to nodule in Sophora davidii. Plant Soil 491, 285–302 (2023). https://doi.org/10.1007/s11104-023-06115-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06115-2