Abstract
Background and aims
Considering the plant microbiota, temporal changes are expected depending on plant development stages and environmental pressures because of modifications in plant requirements and available soil microbial reservoir.
Methods
Herein, we analyzed the composition of root endosphere microbiota of grafted vine plants using two grapevine cultivars (Merlot and Cabernet-Sauvignon as scion grafted on rootstocks of different clones) as models both sampled in a single vineyard at three dates over a period of two growing years.
Results
Highly conserved temporal patterns were found in the two cultivars. Intra-annual changes in microbial community composition were recorded whereas convergent microbial communities were observed on the two September dates. In particular, the increase in Actinobacteria and decrease in Glomeromycota in September were interpreted as shifts in the microbiota community patterns related to plant physiological requirements (e.g. water supply). A high proportion of non-random assembly of the root endospheric bacterial community confirmed the deterministic influence of the plant or/and the environment in microbial recruitment over time. The modified normalized stochasticity ratio (MST) showed that deterministic processes of assembly (MST < 50%) were commonplace despite the changes in the root microbiota composition observed among sampling dates.
Conclusion
Our study suggests an intra-annual rhythm of microbiota shifts, marginally random, with a succession within the root-microbiota endosphere likely governed by active plant filtering. A better knowledge of microbial-recruitment at work, seems important for both fundamental and applied perspectives.
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Data availability
Data are available on Figshare https://figshare.com/s/6c6ca1fee254f88e0598.
Sequence data are available at European Nucleotide Archive (ENA) under accession number PRJEB47615.
References
Andreo-Jimenez B, Vandenkoornhuyse P, Van Lê A, Heutinck A, Duhamel M, Kadam N, Jagadish K, Ruyter-Spira C, Bouwmeester H (2019) Plant host and drought shape the root associated fungal microbiota in rice. Peer J 7:e7463. https://doi.org/10.7717/peerj.7463
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:201–210. https://doi.org/10.18637/jss.v067.i01
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bennett AE, Daniell TJ, Öpik M, Davison J, Moora M, Zobel M, Selosse M-A, Evans D (2013) Arbuscular mycorrhizal fungal networks vary throughout the growing season and between successional stages. PloS One 8:e83241. https://doi.org/10.1371/journal.pone.0083241
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x
Berlanas C, Berbegal M, Elena G, Laidani M, Cibriain JF, Sagües A, Gramaje D (2019) The fungal and bacterial rhizosphere microbiome associated with grapevine rootstock genotypes in mature and young vineyards. Front Microbiol 10:1142. https://doi.org/10.3389/fmicb.2019.01142
Bettenfeld P, i Cadena JC, Jacquens L, Fernandez O, Fontaine F, van Schaik E, Courty P-E, Trouvelot S (2022) The microbiota of the grapevine holobiont: A key component of plant health. J Adv Res 40:1–15. https://doi.org/10.1016/j.jare.2021.12.008
Biget M, Wang T, Mony C, Xu Q, Lecoq L, Chable V, Theis KR, Ling N, Vandenkoornhuyse P (2023) Evaluating the hologenome concept by analyzing the root-endosphere microbiota of chimeric plants. iScience 26:106. https://doi.org/10.1016/j.isci.2023.106031
Bokulich NA, Thorngate JH, Richardson PM, Mills DA (2014) Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci USA 111:E139–E148. https://doi.org/10.1073/pnas.1317377110
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. https://doi.org/10.1128/AEM.02188-07
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. https://doi.org/10.1146/annurev-arplant-050312-120106
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664. https://doi.org/10.1038/ismej.2015.142
Carper DL, Carrell AA, Kueppers LM, Frank AC (2018) Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors. Plant Soil 428:335–352. https://doi.org/10.1007/s11104-018-3682-x
Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PloS One 8:e55731. https://doi.org/10.1371/journal.pone.0055731
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196
Compant S, Samad A, Faist H, Sessitsch A (2019) A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J Adv Res 19:29–37. https://doi.org/10.1016/j.jare.2019.03.004
Copeland JK, Yuan L, Layeghifard M, Wang PW, Guttman DS (2015) Seasonal community succession of the phyllosphere microbiome. Mol Plant Microbe Interact 28:274–285. https://doi.org/10.1094/MPMI-10-14-0331-FI
Cotton TEA, Pétriacq P, Cameron DD, Meselmani MA, Schwarzenbacher R, Rolfe SA, Ton J (2019) Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME J 13:1647–1658. https://doi.org/10.1038/s41396-019-0375-2
Dang H, Zhang T, Wang Z, Li G, Zhao W, Lv X, Zhuang L (2021) Succession of endophytic fungi and arbuscular mycorrhizal fungi associated with the growth of plant and their correlation with secondary metabolites in the roots of plants. BMC Plant Biol 21:165. https://doi.org/10.1186/s12870-021-02942-6
Deyett E, Rolshausen PE (2020) Endophytic microbial assemblage in grapevine. FEMS Microbiol Ecol 96:fiaa053. https://doi.org/10.1093/femsec/fiaa053
Doumbou CL, Hamby Salove MK, Crawford DL, Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85–102. https://doi.org/10.7202/706219ar
Dries L, Bussotti S, Pozzi C, Kunz R, Schnell S, Lohnertz O, Vortkamp A (2021) Rootstocks shape their microbiome-bacterial communities in the rhizosphere of different grapevine rootstocks. Microorganisms 9:822. https://doi.org/10.3390/microorganisms9040822
Elzhov TV, Mullen KM, Spiess A, Bolker B (2010) Minpack. lm: R interface to the Levenberg-Marquardt nonlinear least-squares algorithm found in MINPACK. Plus support for bounds. R package version 1.2.1. http://CRAN.R-project.org/package=minpack.lm
Escudié F, Auer L, Bernard M, Mariadassou M, Cauquil L, Vidal K, Maman S, Hernandez-Raquet G, Combes S, Pascal G (2018) FROGS: find, rapidly, OTUs with galaxy solution. Bioinformatics 34:1287–1294. https://doi.org/10.1093/bioinformatics/btx791
Fox J, Weisberg S (2018) An R companion to applied regression. Sage publications
Govindasamy V, Franco CMM, Gupta VVSR (2014) Endophytic actinobacteria: diversity and ecology. In: Verma V, Gange A (eds) Advances in Endophytic Research, Springer, New Delhi, pp 27–59. https://doi.org/10.1007/978-81-322-1575-2_2
Guo J, Ling N, Li Y, Li K, Ning H, Shen Q, Guo S, Vandenkoornhuyse P (2021) Seed-borne, endospheric and rhizospheric core microbiota as predictors of plant functional traits across rice cultivars are dominated by deterministic processes. New Phytol 230:2047–2060. https://doi.org/10.1111/nph.17297
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hervé M, Hervé MM (2020) RVAideMemoire: testing and plotting procedures for biostatistics. The R Foundation. https://cran.r-project.org/package=RVAideMemoire.
Iannucci A, Canfora L, Nigro F, De Vita P, Beleggia R (2021) Relationships between root morphology, root exudate compounds and rhizosphere microbial community in durum wheat. Appl Soil Ecol 158:103781. https://doi.org/10.1016/j.apsoil.2020.103781
Jacoby RP, Chen L, Schwier M, Koprivova A, Kopriva S (2020) Recent advances in the role of plant metabolites in shaping the root microbiome. F1000Res 9:151. https://doi.org/10.12688/f1000research.21796.1
Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513. https://doi.org/10.1111/j.1469-8137.2010.03197.x
Kaur S, Suseela V (2020) Unraveling arbuscular mycorrhiza-induced changes in plant primary and secondary metabolome. Metabolites 10:335. https://doi.org/10.3390/metabo10080335
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. https://doi.org/10.1126/science.1208473
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. https://doi.org/10.1007/s004420100716
Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the core microbiota be functional. Trends Plant Sci 22:583–595. https://doi.org/10.1016/j.tplants.2017.04.008
Lidbury IDEA, Borsetto C, Murphy ARJ, Bottrill A, Jones AME, Bending GD, Hammond JP, Chen Y, Wellington EMH, Scanlan DJ (2021) Niche-adaptation in plant-associated Bacteroidetes favours specialisation in organic phosphorus mineralisation. ISME J 15:1040–1055. https://doi.org/10.1038/s41396-020-00829-2
Liu D, Howell K (2021) Community succession of the grapevine fungal microbiome in the annual growth cycle. Environ Microbiol 23:1842–1857. https://doi.org/10.1111/1462-2920.15172
Mahé S, Duhamel M, Le Calvez T, Guillot L, Sarbu L, Bretaudeau A, Collin O, Dufresne A, Kiers ET, Vandenkoornhuyse P (2012) PHYMYCO-DB: a curated database for analyses of fungal diversity and evolution. PloS One 7:e43117. https://doi.org/10.1371/journal.pone.0043117
Marasco R, Rolli E, Fusi M, Michoud G, Daffonchio D (2018) Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome 6:3. https://doi.org/10.1186/s40168-017-0391-2
Marasco R, Alturkey H, Fusi M, Brandi M, Ghiglieno I, Valenti L, Daffonchio D (2022) Rootstock-scion combination contributes to shape diversity and composition of microbial communities associated with grapevine root system. Environ Microbiol 24:3791–3808. https://doi.org/10.1111/1462-2920.16042
McRose DL, Li J, Newman DK (2023) The chemical ecology of coumarins and phenazines affects iron acquisition by pseudomonads. Proc Natl Acad Sci 120:e2217951120. https://doi.org/10.1073/pnas.2217951120
Morrison-Whittle P, Goddard MR (2015) Quantifying the relative roles of selective and neutral processes in defining eukaryotic microbial communities. ISME J 9:2003–2011. https://doi.org/10.1038/ismej.2015.18
Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170:165–175. https://doi.org/10.1111/j.1469-8137.2006.01650.x
Müller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50:211–234. https://doi.org/10.1146/annurev-genet-120215-034952
Ning D, Deng Y, Tiedje James M, Zhou J (2019) A general framework for quantitatively assessing ecological stochasticity. Proc Natl Acad Sci USA 116:16892–16898. https://doi.org/10.1073/pnas.1904623116
Pérez-Jaramillo JE, Carrión VJ, Bosse M, Ferrão LFV, De Hollander M, Garcia AAF, Ramírez 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. https://doi.org/10.1038/ismej.2017.85
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315. https://doi.org/10.1146/annurev-phyto-080508-081831
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Renouf V, Claisse O, Lonvaud-Funel A (2005) Understanding the microbial ecosystem on the grape berry surface through numeration and identification of yeast and bacteria. Austral J Grape Wine Res 11:316–327. https://doi.org/10.1111/j.1755-0238.2005.tb00031.x
Saleem M, Law AD, Sahib MR, Pervaiz ZH, Zhang Q (2018) Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6:47–51. https://doi.org/10.1016/j.rhisph.2018.02.003
Schrey SD, Tarkka MT (2008) Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie Van Leeuwenhoek 94:11–19. https://doi.org/10.1007/s10482-008-9241-3
Searle SR, Speed FM, Milliken GA (1980) Population marginal means in the linear model: an alternative to least squares means. Am Stat 34:216–221. https://doi.org/10.1080/00031305.1980.10483031
Sloan WT, Lunn M, Woodcock S, Head IM, Nee S, Curtis TP (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8:732–740. https://doi.org/10.1111/j.1462-2920.2005.00956.x
Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, London, UK. https://doi.org/10.1097/00010694-198403000-00011
Swift JF, Hall ME, Harris ZN, Kwasniewski MT, Miller AJ (2021) Grapevine microbiota reflect diversity among compartments and complex interactions within and among root and shoot systems. Microorganisms 9:92. https://doi.org/10.3390/microorganisms9010092
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)
Van Lê A, Quaiser A, Duhamel M, Michon-Coudouel S, Dufresne A, Vandenkoornhuyse P (2017) Ecophylogeny of the endospheric root fungal microbiome of co-occurring Agrostis stolonifera. PeerJ 5:e3454. https://doi.org/10.7717/peerj.3454
Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564. https://doi.org/10.1046/j.1365-294x.2002.01538.x)
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. https://doi.org/10.1111/nph.13312
Vannier N, Mony C, Bittebière A-K, Vandenkoornhuyse P (2015) Epigenetic mechanisms and microbiota as a toolbox for plant phenotypic adjustment to environment. Front Plant Sci 6:1159. https://doi.org/10.3389/fpls.2015.01159
Vannier N, Mony C, Bittebiere A-K, Michon-Coudouel S, Biget M, Vandenkoornhuyse P (2018) A microorganisms’ journey between plant generations. Microbiome 6:79. https://doi.org/10.1186/s40168-018-0459-7
Venkataraman A, Bassis CM, Beck JM, Young VB, Curtis JL, Huffnagle GB, Schmidt TM (2015) Application of a neutral community model to assess structuring of the human lung microbiome. mBio 6:e02284-14. https://doi.org/10.1128/mBio.02284-14
Vink SN, Dini-Andreote F, Höfle R, Kicherer A, Salles JF (2021) Interactive effects of scion and rootstock genotypes on the root microbiome of grapevines (Vitis spp. L.). Appl Sci 11:1615. https://doi.org/10.3390/app11041615
Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente RM (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39:3–17. https://doi.org/10.1007/s00299-019-02447-5
Voges MJEEE, Bai Y, Schulze-Lefert P, Sattely ES (2019) Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proc Natl Acad Sci USA 116:12558–12565. https://doi.org/10.1073/pnas.1820691116
Werner GDA, Kiers ET (2015) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–1524. https://doi.org/10.1111/nph.13092
Xiong C, Zhu YG, Wang JT, Singh B, Han LL, Shen JP, Li PP, Wang GB, Wu CF, Ge AH (2021) Plant developmental stage drives the differentiation in ecological role of the maize microbiome. Microbiome 9:171. https://doi.org/10.1186/s40168-021-01118-6
Yang T, Chen Y, Wang X-X, Dai C-C (2013) Plant symbionts: keys to the phytosphere. Symbiosis 59:1–14. https://doi.org/10.1007/s13199-012-0190-2
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S (2015) The soil microbiome influences grapevine-associated microbiota. mBio 6:e02527-02514. https://doi.org/10.1128/mBio.02527-14
Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, Cho H, Karaoz U, Loqué D, Bowen BP (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480. https://doi.org/10.1038/s41564-018-0129-3
Zhang J, Wang ET, Singh RP, Guo C, Shang Y, Chen J, Liu C (2019) Grape berry surface bacterial microbiome: impact from the varieties and clones in the same vineyard from central China. J Appl Microbiol 126:204–214. https://doi.org/10.1111/jam.14124
Acknowledgements
This work was supported by a grant from the CNRS-EC2CO program (HOLOBIONT project), CNRS-IRP program (M-AGRI project) and by the "Agence Nationale de la Recherche et de la Technologie” (ANRT) through an industrial CIFRE agreement between Château Palmer, Château Latour, Sovivins, Pépinière de Salettes and the University of Rennes 1 (Agreement N° 2017/1579). We are grateful to the GENTYANE and, within the ANAEE-France research infrastructure, to the EcogenO platforms for help with DNA extraction and amplicon sequencing, respectively. We are also grateful to the Genotoul platform Toulouse Midi-Pyrenees and GenOuest for access to their bioinformatics pipeline and storage facilities and the Ecolex platform for help during sampling. We deeply acknowledge all the trainees and people at Château Palmer for their help during the sampling campaigns, especially Sylvain Fries, Oriane Heulliet, Hélène Sarkis for their help performing this work. We are also very grateful to July Hémon (EcogenO, molecular analysis) and Achim Quaiser (sampling). We finally acknowledge Daphne Goodfellow for English editing.
Funding
This work was supported by a grant from the CNRS-EC2CO program (HOLOBIONT project), CNRS-IRP program (M-AGRI project) and by the "Agence Nationale de la Recherche et de la Technologie” (ANRT) through an industrial CIFRE agreement between Château Palmer, Château Latour, Sovivins, Pépinière de Salettes and the University of Rennes 1 (Agreement N° 2017/1579).
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MB, CM, SP, VC and PV conceived the project. PV, CM and MB set up the methodology of the study. MB, CM, OJ, NL and PV conducted the sampling. MB conducted lab experiments with the help of AM. RCV and SMC performed the sequencing and MB and TW analyzed the sequence data. MB and TW performed the statistical analyses with advice from CM, MH and NL. MB wrote the first draft of the paper. All the authors gave their final approval for publication.
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Biget, M., Mony, C., Wang, T. et al. Intra- and inter-annual changes in root endospheric microbial communities of grapevine are mainly deterministic. Plant Soil 494, 217–233 (2024). https://doi.org/10.1007/s11104-023-06262-6
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DOI: https://doi.org/10.1007/s11104-023-06262-6