Abstract
Background and aims
While our understanding of seed microbiota has lagged far behind that of the rhizosphere and phyllosphere, many advances are now being made, particularly based on metagenomics studies. Today, our knowledge of seed microbiome assembly remains incomplete and the connections between seed and soil microbiomes are not yet fully understood, especially where hyperaccumulating plants are concerned. In this work, we assessed the structure and composition of the Noccaea caerulescens rhizosphere and endosphere-associated microbiota.
Methods
A pot experiment was conducted for 6 months in a growth chamber, using two populations of the hyperaccumulator Noccaea caerulescens growing on their original soil (calamine or nonmetalliferous) and vice versa. The diversity of rhizosphere soil bacteria and bacterial endophytic communities present in the different habitats (initial seed, root, stem, leaves and new seed generation) was characterized by high-throughput 16S rRNA amplicon sequencing.
Results
Bacterial communities from root endosphere, stem endosphere and leaf endosphere appeared to be soil-type dependent, contrary to the bacterial communities associated with seed endosphere habitats (initial seeds and new seed generation). Moreover, the seed endophytic bacterial communities of Noccaea caerulescens display a strong heritability across one plant generation. Indeed, a bacterial endophytic core-genome globally appeared to be constant between initial seeds and those obtained after the first generation.
Conclusion
Our results suggest that Noccaea caerulescens may carry a selected bacterial community in its seeds across generations, despite soil environment changes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asaf S, Khan MA, Khan AL, Waqas M, Shahzad R, Kim AY, Kang SM, Lee IJ (2017) Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. J Plant Interactions 12:31–38. https://doi.org/10.1080/17429145.2016.1274060
Assunção AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360. https://doi.org/10.1046/j.1469-8137.2003.00820.xAna
Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM (2013) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–273. https://doi.org/10.1111/nph.12124
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements: a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Barret M, Briand M, Bonneau S, Préveaux A, Valière S, Bouchez O, Hunault G, Simoneau P, Jacques M-A (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81:1257–1266. https://doi.org/10.1128/AEM.03722-14
Benizri E, Lopez S, Durand A, Kidd PS (2021) Diversity and role of endophytic and rhizosphere microbes associated with hyperaccumulator plants during metal accumulation. In: Agromining: Farming for metals. Springer, Cham, pp 239–279
Berg G, Kusstatscher P, Abdelfattah A, Cernava T, Smalla K (2021) Microbiome modulation: toward a better understanding of plant microbiome response to microbial inoculants. Front Microbiol 12:1–12. https://doi.org/10.3389/fmicb.2021.650610
Berg G, Rybakova D, Fischer D, Cernava T, Vergès MCC, Charles T, Chen X, Cocolin L, Eversole K, Corral GH, Kazou M, Kinkel L, Lange L, Lima N, Loy A, Macklin JA, Maguin E, Mauchline T, McClure R et al (2020) Microbiome definition re-visited: old concepts and new challenges. Microbiome 8:1–22. https://doi.org/10.1186/s40168-020-00875-0
Bosch TCG, McFall-Ngai MJ (2011) Metaorganisms as the new frontier. Zoology 114:185–190. https://doi.org/10.1016/j.zool.2011.04.001
Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annual Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Busby PE, Ridout M, Newcombe G (2016) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90:645–655. https://doi.org/10.1007/s11103-015-0412-0
Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chao A (1949) On the estimation of the number of classes in a population. Annals Mathematical Statistics 20:572–579. https://doi.org/10.1214/aoms/1177729949
Chee-Sanford JC, Williams MM, Davis AS, Sims GK (2006) Do microorganisms influence seed-bank dynamics? Weed Sci 54:575–587. https://doi.org/10.1614/WS-05-055R.1
Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Marine Ecol Progress Series 92:205–219. https://doi.org/10.3354/meps092205
Defez R, Andreozzi A, Bianco C (2017) The overproduction of indole-3-acetic acid (IAA) in endophytes upregulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microbial Ecol 74:441–452. https://doi.org/10.1007/s00248-017-0948-4
Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162. https://doi.org/10.1016/j.soilbio.2008.10.010
Dombrowski N, Schlaeppi K, Agler MT, Hacquard S, Kemen E, Garrido-Oter R, Wunder J, Coupland G, Schulze-Lefert P (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11:43–55. https://doi.org/10.1038/ismej.2016.109
Durand A, Leglize P, Benizri E (2021a) Are endophytes essential partners for plants and what are the prospects for metal phytoremediation? Plant Soil 460:1–30. https://doi.org/10.1007/s11104-020-04820-w
Durand A, Sterckeman T, Gonnelli C, Coppi A, Bacci G, Leglize P, Benizri E (2021b) A core seed endophytic bacterial community in the hyperaccumulator Noccaea caerulescens across 14 sites in France. Plant Soil 459:203–216. https://doi.org/10.1007/s11104-020-04743-6
Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Current Opinion Microbiol 32:103–112. https://doi.org/10.1016/j.mib.2016.05.008
Frank A, Saldierna Guzmán J, Shay J (2017) Transmission of bacterial endophytes. Microorganisms 5:70. https://doi.org/10.3390/microorganisms5040070
Glick B, Penrose D, Li J (1997) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theoretic Biol 190:63–68. https://doi.org/10.1006/jtbi.1997.0532
Gonneau C, Noret N, Godé C, Frérot H, Sirguey C, Sterckeman T, Pauwels M (2017) Demographic history of the trace metal hyperaccumulator Noccaea caerulescens (J. Presl and C. Presl) F. K. Mey. In Western Europe. Mol Ecol 26:904–922. https://doi.org/10.1111/mec.13942
Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264. https://doi.org/10.1093/biomet/40.3-4.237
Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907. https://doi.org/10.1046/j.1462-2920.2003.00484.x
Hamayun M, Hussain A, Khan SA, Kim HY, Khan AL, Waqas M, Irshad M, Iqbal A, Rehman G, Jan S, Lee IJ (2017) Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt affected soybean. Front Microbiol 8:686. https://doi.org/10.3389/fmicb.2017.00686
Hardoim PR (2011) Bacterial endophytes of rice: Their diversity, characteristics and perspectives. University of Groningen
Healey A, Furtado A, Cooper T, Henry RJ (2014) Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species. Plant Methods 10:21. https://doi.org/10.1186/1746-4811-10-21
Herrera Paredes S, Lebeis SL (2016) Giving back to the community: microbial mechanisms of plant–soil interactions. Funct Ecol 30:1043–1052. https://doi.org/10.1111/1365-2435.12684
Herrmann M, Wegner CE, Taubert M, Geesink P, Lehmann K, Yan L, Lehmann R, Totsche KU, Küsel K (2019) Predominance of Cand. Patescibacteria in groundwater is caused by their preferential mobilization. Front Microbiol 10:1–15. https://doi.org/10.3389/fmicb.2019.01407
Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677. https://doi.org/10.1128/AEM.70.5.2667-2677.2004
Johnston-Monje D, Lundberg DS, Lazarovits G, Reis VM, Raizada MN (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405:337–355. https://doi.org/10.1007/s11104-016-2826-0
Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN (2014) Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol 14:233. https://doi.org/10.1186/s12870-014-0233-3
Kandel S, Joubert P, Doty S (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77. https://doi.org/10.3390/microorganisms5040077
Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci U S A 111:13715–13720. https://doi.org/10.1073/pnas.1216057111
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
Kluepfel DA (1993) The behavior and tracking of bacteria in the rhizosphere. Annu Rev Phytopathol 31:441–472. https://doi.org/10.1146/ANNUREV.PY.31.090193.002301
Kopecky J, Samkova Z, Sarikhani E, Kyselková M, Omelka M, Kristufek V, Divis J, Grundmann GG, Moënne-Loccoz Y, Sagova-Mareckova M (2019) Bacterial, archaeal and micro-eukaryotic communities characterize a disease-suppressive or conducive soil and a cultivar resistant or susceptible to common scab. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-019-51570-6
Krämer U (2010) Metal hyperaccumulation in plants. Annual Rev Plant Biol 61:517–534. https://doi.org/10.1146/annurev-arplant-042809-112156
Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484. https://doi.org/10.1111/j.1365-2672.2010.04670.x
Lodewyckx C, Mergeay M, Vangronsveld J, Clijsters H, Van Der Lelie D (2002a) Isolation, characterization, and identification of bacteria associated with the zinc hyperaccumulator Thlaspi caerulescens subsp. calaminaria. Int J Phytoremediation 4:101–115. https://doi.org/10.1080/15226510208500076
Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, Van der Lelie D (2002b) Endophytic bacteria and their potential applications. Critical Rev Plant Sci 21:583–606. https://doi.org/10.1080/0735-260291044377
Lòpez-Fernàndez S, Mazzoni V, Pedrazzoli F, Pertot I, Campisano A (2017) A phloem-feeding insect transfers bacterial endophytic communities between grapevine plants. Front Microbiol 8:1–17. https://doi.org/10.3389/fmicb.2017.00834
Lopez-Velasco G, Carder PA, Welbaum GE, Ponder MA (2013) Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities. FEMS Microbiol Lett 346:146–154. https://doi.org/10.1111/1574-6968.12216
Lopez S, Piutti S, Vallance J, Morel JL, Echevarria G, Benizri E (2017) Nickel drives bacterial community diversity in the rhizosphere of the hyperaccumulator Alyssum murale. Soil Biol Biochem 114:121–130. https://doi.org/10.1016/j.soilbio.2017.07.010
Luo J, Tao Q, Jupa R, Liu Y, Wu K, Song Y, Li J, Huang Y, Zou L, Liang Y, Li T (2019) Role of vertical transmission of shoot endophytes in root-associated microbiome assembly and heavy metal hyperaccumulation in Sedum alfredii. Environ Sci Technol 53:6954–6963. https://doi.org/10.1021/acs.est.9b01093
Luo SL, Chen L, Liang CJ, Xiao X, Ying XT, Wan Y, Rao C, Bin LC, Tang LY, Lai C, Ming ZG (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138. https://doi.org/10.1016/j.chemosphere.2011.07.053
Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015a) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69. https://doi.org/10.1016/j.jenvman.2015.03.024
Ma Y, Rajkumar M, Moreno A, Zhang C, Freitas H (2017) Serpentine endophytic bacterium Pseudomonas azotoformans ASS1 accelerates phytoremediation of soil metals under drought stress. Chemosphere 185:75–85. https://doi.org/10.1016/j.chemosphere.2017.06.135
Ma Y, Rajkumar M, Rocha I, Oliveira RS, Freitas H (2015b) Serpentine bacteria influence metal translocation and bioconcentration of Brassica juncea and Ricinus communis. Front Plant Sci 5:757. https://doi.org/10.3389/fpls.2014.00757
Mastretta C, Taghavi S, Van Der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267. https://doi.org/10.1080/15226510802432678
McCully M (2001) Niches for bacterial endophytes in crop plants: a plant biologist’s view. Aust J Plant Physiol 28:983–990
McEnroe NA, Helmisaari HS (2001) Decomposition of coniferous forest litter along a heavy metal pollution gradient, south-West Finland. Environ Pollution 113:11–18. https://doi.org/10.1016/S0269-7491(00)00163-9
Mirecki N, Agič R, Šunić L, Milenković L, Ilić ZS (2015) Transfer factor as indicator of heavy metals content in plants. Fresenius Environ Bull 24:4212–4219
Müller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annual Rev Genetics 50:211–234. https://doi.org/10.1146/annurev-genet-120215-034952
Mundt OJ, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32:694–698. https://doi.org/10.1128/aem.32.5.694-698.1976
Nelson EB (2017) The seed microbiome: origins, interactions, and impacts. Plant Soil 422:7–34. https://doi.org/10.1007/s11104-017-3289-7
Nelson EB, Simoneau P, Barret M, Mitter B, Compant S (2018) Editorial special issue: the soil, the seed, the microbes and the plant. Plant Soil 422:1–5. https://doi.org/10.1007/s11104-018-3576-y
Nimaichand S, Devi AM, Li W-J (2016) Direct plant growth-promoting ability of Actinobacteria in grain legumes. In: Plant growth promoting Actinobacteria: a new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, Singapore, pp 1–16
Nimnoi P, Pongsilp N, Lumyong S (2010) Endophytic actinomycetes isolated from Aquilaria crassna Pierre ex Lec and screening of plant growth promoters production. World J Microbiol Biotechnol 26:193–203. https://doi.org/10.1007/s11274-009-0159-3
Niu X, Zhou J, Wang X, Su X, Du S, Zhu Y, Yang J, Huang D (2020) Indigenous bacteria have high potential for promoting Salix integra thunb. Remediation of lead-contaminated soil by adjusting soil properties. Front Microbiol 11:1–13. https://doi.org/10.3389/fmicb.2020.00924
Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–989. https://doi.org/10.1038/ismej.2014.196
Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430. https://doi.org/10.1046/j.1469-8137.2003.00822.x
Peng A, Liu J, Ling W, Chen Z, Gao Y (2015) Diversity and distribution of 16S rRNA and phenol monooxygenase genes in the rhizosphere and endophytic bacteria isolated from PAH-contaminated sites. Sci Rep 5:1–12. https://doi.org/10.1038/srep12173
Perotti R (1926) On the limits of biological enquiry in soil science. Proc Int Soc Soil Sci 2:146–161
Preite V, Sailer C, Syllwasschy L, Bray S, Ahmadi H, Krämer U, Yant L (2019) Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils. Philos Trans Royal Soc B: Biol Sci 374:20180243. https://doi.org/10.1098/rstb.2018.0243
Qiong W, Fengshan P, Xiaomeng X, Rafiq MT, Xiao’e Y, Bao C, Ying F (2021) Cadmium level and soil type played a selective role in the endophytic bacterial community of hyperaccumulator Sedum alfredii Hance. Chemosphere 263:127986. https://doi.org/10.1016/j.chemosphere.2020.127986
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing
Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748. https://doi.org/10.1016/j.chemosphere.2005.04.117
Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407–411. https://doi.org/10.1111/nph.14907
Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172. https://doi.org/10.1080/15226510108500054
Reeves RD, van der Ent A, Baker AJM (2021) Global distribution and ecology of hyperaccumulator plants. In: Agromining: farming for metals. Springer, Cham, pp 133–154
Rezki S, Campion C, Simoneau P, Jacques MA, Shade A, Barret M (2018) Assembly of seed-associated microbial communities within and across successive plant generations. Plant Soil 422:67–79. https://doi.org/10.1007/s11104-017-3451-2
Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Metraux JP, L’Haridon F (2016) The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol 210:1033–1043. https://doi.org/10.1111/nph.13808
Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. https://doi.org/10.1111/1462-2920.12439
Sánchez-López AS, Pintelon I, Stevens V, Imperato V, Timmermans J-P, González-Chávez MDCA, Carrillo-González R, Van Hamme J, Vangronsveld J, Thijs S (2018a) Seed endophyte microbiome of Crotalaria pumila unpeeled: identification of plant-beneficial methylobacteria. Int J Mol Sci 19:291. https://doi.org/10.3390/IJMS19010291
Sánchez-López AS, Thijs S, Beckers B, Gonzalez-Chavez MC, Weyens N, Carrillo-Gonzalez R, Vangronsveld J (2018b) Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues. Plant Soil 422:51–66. https://doi.org/10.1007/s11104-017-3176-2
Santoyo G, Moreno-Hagelsieb G, del Carmen O-MM, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482. https://doi.org/10.1128/AEM.70.3.1475-1482.2004
Shade A, Jacques M-A, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Current Opinion Microbiol 37:15–22. https://doi.org/10.1016/j.mib.2017.03.010
Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303.metabolite
Smith EF (1911) Bacteria in relation to plant diseases. Carnegie Institute, Washington
Syranidou E, Thijs S, Avramidou M, Weyens N, Venieri D, Pintelon I, Vangronsveld J, Kalogerakis N (2018) Responses of the endophytic bacterial communities of Juncus acutus to pollution with metals, emerging organic pollutants and to bioaugmentation with indigenous strains. Front Plant Sci 871:1–14. https://doi.org/10.3389/fpls.2018.01526
Tannenbaum I, Kaur J, Mann R, Sawbridge T, Rodoni B, Spangenberg G (2020) Profiling the Lolium perenne microbiome: from seed to seed. Phytobiomes J 4:281–289. https://doi.org/10.1094/PBIOMES-03-20-0026-R
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Reports 7:40–50. https://doi.org/10.1111/1758-2229.12181
van Overbeek LS, Franke AC, Nijhuis EHM, Groeneveld RMW, da Rocha UN, Lotz LAP (2011) Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microbial Ecol 62:257–264. https://doi.org/10.1007/s00248-011-9845-4
Visioli G, D’Egidio S, Vamerali T, Mattarozzi M, Sanangelantoni AM (2014) Culturable endophytic bacteria enhance Ni translocation in the hyperaccumulator Noccaea caerulescens. Chemosphere 117:538–544. https://doi.org/10.1016/j.chemosphere.2014.09.014
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 7:1–15. https://doi.org/10.1038/ncomms12151
Walitang DI, Sunyoung CK, Yeongyeong J, Sa T (2018) Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations. Microbiol Open 8:e006. https://doi.org/10.1002/mbo3.662
Wang Q, Ge C, Xu S, Wu Y, Sahito ZA, Ma L, Pan F, Zhou Q, Huang L, Feng Y, Yang X (2020) The endophytic bacterium Sphingomonas SaMR12 alleviates cd stress in oilseed rape through regulation of the GSH-AsA cycle and antioxidative enzymes. BMC Plant Biol 20:1–14. https://doi.org/10.1186/s12870-020-2273-1
Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965. https://doi.org/10.1007/s00253-015-6487-3
Weyens N, Van Der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant– endophyte partnerships take the challenge. Current Opinion Biotechnol 20:248–254. https://doi.org/10.1016/j.copbio.2009.02.012
Wolfgang A, Zachow C, Müller H, Grand A, Temme N, Tilcher R, Berg G (2020) Understanding the impact of cultivar, seed origin, and substrate on bacterial diversity of the sugar beet rhizosphere and suppression of soil-borne pathogens. Front Plant Sci 11:1–15. https://doi.org/10.3389/fpls.2020.560869
Worsley SF, Newitt J, Rassbach J, Batey SFD, Holmes NA, Murrell JC, Wilkinson B, Hutchings MI (2020) Streptomyces endophytes promote host health and enhance growth across plant species. Appl Environ Microbiol 86:1–17. https://doi.org/10.1128/AEM.01053-20
Yadav A (2017) Exploring the potential of endophytes in agriculture: a minireview. Advancesn Plants Agric Res 6:00221. https://doi.org/10.15406/apar.2017.06.00221
Yamada T, Sekiguchi Y, Imachi H, Kamagata Y, Ohashi A, Harada H (2005) Diversity, localization, and physiological properties of filamentous microbes belonging to Chloroflexi subphylum I in mesophilic and thermophilic methanogenic sludge granules. 71:7493–7503. https://doi.org/10.1128/AEM.71.11.7493
Zhang YF, Yan HL, Jin CZ, Ya WQ, Qian M, Fang SX (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62. https://doi.org/10.1016/j.chemosphere.2011.01.041
Zhou T, Li L, Zhang X, Zheng J, Zheng J, Joseph S, Pan G (2016) Changes in organic carbon and nitrogen in soil with metal pollution by cd, cu, Pb and Zn: a meta-analysis. Eur J Soil Sci 67:237–246. https://doi.org/10.1111/ejss.12327
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Stéphane Compant
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Supplementary Fig. 1
Mean relative abundances (%) of bacterial classes from the various modalities. All classes corresponding to less than 0.5% relative abundance are regrouped in ‘Rare classes’ corresponding to the 16 following classes: Abditibacteria, Unclassified Acidibacteriota, MB-A2–108 Actinobacteria, Unclassified Actinobacteriota, Fimbriimonadia, Unclassified Bacteroidota, Unclassified Bdellovibrionota, OLB14 Chloroflexi, Bacilli, Unclassified Firmicutes, Unclassified Gemmatimonadota, Latescibacteria, Unclassified Myxococcota, Nitrospiria, Chlamydiae and Verrucomicrobiae. Modalities names are given in Table 5. (PPTX 123 kb)
Rights and permissions
About this article
Cite this article
Durand, A., Leglize, P., Lopez, S. et al. Noccaea caerulescens seed endosphere: a habitat for an endophytic bacterial community preserved through generations and protected from soil influence. Plant Soil 472, 257–278 (2022). https://doi.org/10.1007/s11104-021-05226-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05226-y