Rootstock–scion combination contributes to shape diversity and composition of microbial communities associated with grapevine root system

Summary To alleviate biotic and abiotic stresses and enhance fruit yield, many crops are cultivated in the form of grafted plants, in which the shoot (scion) and root (rootstock) systems of different species are joined together. Because (i) the plant species determines the microbial recruitment from the soil to the root and (ii) both scion and rootstock impact the physiology, morphology and biochemistry of the grafted plant, it can be expected that their different combinations should affect the recruitment and assembly of plant microbiome. To test our hypothesis, we investigated at a field scale the bacterial and fungal communities associated with the root system of seven grapevine rootstock–scion combinations cultivated across 10 different vineyards. Following the soil type, which resulted in the main determinant of the grapevine root microbial community diversity, the rootstock–scion combination resulted more important than the two components taken alone. Notably, the microbiome differences among the rootstock–scion combinations were mainly dictated by the changes in the relative abundance of microbiome members rather than by their presence/absence. These results reveal that the microbiome of grafted grapevine root systems is largely influenced by the combination of rootstock and scion, which affects the microbial diversity uptaken from soil.

[1]  Yahai Lu,et al.  Rare Species-Driven Diversity–Ecosystem Multifunctionality Relationships are Promoted by Stochastic Community Assembly , 2022, mBio.

[2]  L. Mommer,et al.  Deciphering the role of specialist and generalist plant-microbial interactions as drivers of plant-soil feedback. , 2022, The New phytologist.

[3]  R. Ortiz-Álvarez,et al.  A global microbiome survey of vineyard soils highlights the microbial dimension of viticultural terroirs , 2022, Communications Biology.

[4]  V. Lauvergeat,et al.  Grapevine rootstock and soil microbiome interactions: Keys for a resilient viticulture , 2022, Horticulture research.

[5]  F. Bak,et al.  Back to our roots: exploring the role of root morphology as a mediator of beneficial plant–microbe interactions , 2022, Environmental microbiology.

[6]  P. Courty,et al.  The microbiota of the grapevine holobiont: A key component of plant health , 2021, Journal of advanced research.

[7]  N. Belfiore,et al.  Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs , 2021, Biology and Fertility of Soils.

[8]  M. Hendgen,et al.  Rhizosphere engineering: leading towards a sustainable viticulture? , 2021 .

[9]  S. Kaul,et al.  Engineering Host Microbiome for Crop Improvement and Sustainable Agriculture , 2021, Frontiers in Microbiology.

[10]  Eoin L. Brodie,et al.  Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop , 2021, Microbiome.

[11]  Nicholas A. Bokulich,et al.  Sources and Assembly of Microbial Communities in Vineyards as a Functional Component of Winegrowing , 2021, Frontiers in Microbiology.

[12]  O. Löhnertz,et al.  Rootstocks Shape Their Microbiome—Bacterial Communities in the Rhizosphere of Different Grapevine Rootstocks , 2021, Microorganisms.

[13]  K. Eversole,et al.  Enabling sustainable agriculture through understanding and enhancement of microbiomes. , 2021, The New phytologist.

[14]  J. Salles,et al.  Interactive Effects of Scion and Rootstock Genotypes on the Root Microbiome of Grapevines (Vitis spp. L.) , 2021, Applied Sciences.

[15]  A. Chrysargyris,et al.  Bacterial community dynamics varies with soil management and irrigation practices in grapevines (Vitis vinifera L.) , 2021, Applied Soil Ecology.

[16]  Allison J. Miller,et al.  Grapevine Microbiota Reflect Diversity among Compartments and Complex Interactions within and among Root and Shoot Systems , 2020, bioRxiv.

[17]  B. Singh,et al.  Crop microbiome and sustainable agriculture , 2020, Nature Reviews Microbiology.

[18]  G. Lorenzis,et al.  How Do Novel M-Rootstock (Vitis Spp.) Genotypes Cope with Drought? , 2020, Plants.

[19]  Zhenhai Han,et al.  Apple Scion Cultivars Regulate the Rhizosphere Microbiota of Scion/rootstock Combinations , 2020, Applied Soil Ecology.

[20]  Shiwei Guo,et al.  Plant Grafting Shapes Complexity and Co-occurrence of Rhizobacterial Assemblages , 2020, Microbial Ecology.

[21]  F. Mignone,et al.  Discovering the bacteriome of Vitis vinifera cv. Pinot Noir in a conventionally managed vineyard , 2020, Scientific Reports.

[22]  P. Rolshausen,et al.  Endophytic Microbial Assemblage in Grapevine. , 2020, FEMS microbiology ecology.

[23]  A. Bano,et al.  Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses , 2020 .

[24]  B. Cook,et al.  Diversity buffers winegrowing regions from climate change losses , 2020, Proceedings of the National Academy of Sciences.

[25]  P. Reich,et al.  Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems , 2019, Science Advances.

[26]  M. Delgado‐Baquerizo,et al.  Cross-Biome Drivers of Soil Bacterial Alpha Diversity on a Worldwide Scale , 2019, Ecosystems.

[27]  A. Gómez-Cadenas,et al.  Root exudates: from plant to rhizosphere and beyond , 2019, Plant Cell Reports.

[28]  D. Gramaje,et al.  The Fungal and Bacterial Rhizosphere Microbiome Associated With Grapevine Rootstock Genotypes in Mature and Young Vineyards , 2019, Front. Microbiol..

[29]  J. Boursiquot,et al.  Genetic diversity and parentage analysis of grape rootstocks , 2019, Theoretical and Applied Genetics.

[30]  N. Vitulo,et al.  Bark and Grape Microbiome of Vitis vinifera: Influence of Geographic Patterns and Agronomic Management on Bacterial Diversity , 2019, Front. Microbiol..

[31]  O. Babalola,et al.  Plant health: feedback effect of root exudates-rhizobiome interactions , 2018, Applied Microbiology and Biotechnology.

[32]  D. Daffonchio,et al.  Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host , 2018, Microbiome.

[33]  S. Delrot,et al.  Merging genotypes: graft union formation and scion–rootstock interactions , 2018, Journal of experimental botany.

[34]  S. Rampelli,et al.  The Rootstock Regulates Microbiome Diversity in Root and Rhizosphere Compartments of Vitis vinifera Cultivar Lambrusco , 2018, Front. Microbiol..

[35]  Katrina M. Dlugosch,et al.  Chloroplast sequence variation and the efficacy of peptide nucleic acids for blocking host amplification in plant microbiome studies , 2018, Microbiome.

[36]  M. V. D. van der Heijden,et al.  Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota , 2018, Nature Communications.

[37]  F. Dini-Andreote,et al.  Embracing Community Ecology in Plant Microbiome Research. , 2018, Trends in plant science.

[38]  Audrey D. Law,et al.  Impact of root system architecture on rhizosphere and root microbiome , 2018, Rhizosphere.

[39]  Y. Onoda,et al.  Core microbiomes for sustainable agroecosystems , 2018, Nature Plants.

[40]  S. Hacquard,et al.  Microbial interactions within the plant holobiont , 2018, Microbiome.

[41]  Eoin L. Brodie,et al.  Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly , 2018, Nature Microbiology.

[42]  H. de Kroon,et al.  Lost in diversity: the interactions between soil‐borne fungi, biodiversity and plant productivity , 2018, The New phytologist.

[43]  D. Daffonchio,et al.  The stage of soil development modulates rhizosphere effect along a High Arctic desert chronosequence , 2018, The ISME Journal.

[44]  D. Daffonchio,et al.  Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality , 2018, Microbiome.

[45]  L. T. Braz,et al.  Grafting in Vegetable Crops: A Great Technique for Agriculture , 2018 .

[46]  A. Hashem,et al.  Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness , 2017, Front. Microbiol..

[47]  Thomas J. Hardcastle,et al.  Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration , 2017, Proceedings of the National Academy of Sciences.

[48]  M. Gardiman,et al.  Long- term grapevine cultivation and agro-environment affect rhizosphere microbiome rather than plant age , 2017 .

[49]  P. Poole,et al.  Understanding the holobiont: the interdependence of plants and their microbiome. , 2017, Current opinion in microbiology.

[50]  A. Aharoni,et al.  Small molecules below‐ground: the role of specialized metabolites in the rhizosphere , 2017, The Plant journal : for cell and molecular biology.

[51]  Jesse R. Zaneveld,et al.  Normalization and microbial differential abundance strategies depend upon data characteristics , 2017, Microbiome.

[52]  Nicholas A. Bokulich,et al.  Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: Differentiation by vineyard management , 2016 .

[53]  Iko T. Koevoets,et al.  Roots Withstanding their Environment: Exploiting Root System Architecture Responses to Abiotic Stress to Improve Crop Tolerance , 2016, Front. Plant Sci..

[54]  E. Gomès,et al.  Roostocks/Scion/Nitrogen Interactions Affect Secondary Metabolism in the Grape Berry , 2016, Front. Plant Sci..

[55]  N. Ollat,et al.  Grapevine rootstocks: origins and perspectives , 2016 .

[56]  David A. Mills,et al.  Associations among Wine Grape Microbiome, Metabolome, and Fermentation Behavior Suggest Microbial Contribution to Regional Wine Characteristics , 2016, mBio.

[57]  Allison J. Miller,et al.  Rootstocks: Diversity, Domestication, and Impacts on Shoot Phenotypes. , 2016, Trends in plant science.

[58]  E. Rosenberg,et al.  Microbes Drive Evolution of Animals and Plants: the Hologenome Concept , 2016, mBio.

[59]  H. Bouwmeester,et al.  Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication. , 2016, Trends in plant science.

[60]  G. Valle,et al.  Grapevine Rootstocks Differentially Affect the Rate of Ripening and Modulate Auxin-Related Genes in Cabernet Sauvignon Berries , 2016, Front. Plant Sci..

[61]  G. Moreno-Hagelsieb,et al.  Plant growth-promoting bacterial endophytes. , 2016, Microbiological research.

[62]  U. Mueller,et al.  Engineering Microbiomes to Improve Plant and Animal Health. , 2015, Trends in microbiology.

[63]  C. Abdelly,et al.  Influence of the Rootstock/Scion Combination on the GrapevinesBehavior under Salt Stress , 2015 .

[64]  Sur Herrera Paredes,et al.  Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa , 2015, Science.

[65]  Philippe Vandenkoornhuyse,et al.  The importance of the microbiome of the plant holobiont. , 2015, The New phytologist.

[66]  F. Ausubel,et al.  Associations with rhizosphere bacteria can confer an adaptive advantage to plants , 2015, Nature Plants.

[67]  E. Gomès,et al.  Water limitation and rootstock genotype interact to alter grape berry metabolism through transcriptome reprogramming , 2015, Horticulture Research.

[68]  David A. Mills,et al.  The Soil Microbiome Influences Grapevine-Associated Microbiota , 2015, mBio.

[69]  M. V. D. van der Heijden,et al.  Root surface as a frontier for plant microbiome research , 2015, Proceedings of the National Academy of Sciences.

[70]  C. Sorlini,et al.  Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. , 2015, Environmental microbiology.

[71]  F. D. Andreote,et al.  Bacterial communities in the rhizosphere of Vitis vinifera L. cultivated under distinct agricultural practices in Argentina , 2015, Antonie van Leeuwenhoek.

[72]  Richard D. Bardgett,et al.  Belowground biodiversity and ecosystem functioning , 2014, Nature.

[73]  M. Pindo,et al.  Bacterial Endophytic Communities in the Grapevine Depend on Pest Management , 2014, PloS one.

[74]  U. Baumann,et al.  Shoot chloride exclusion and salt tolerance in grapevine is associated with differential ion transporter expression in roots , 2014, BMC Plant Biology.

[75]  H. Bais,et al.  Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem1[C] , 2014, Plant Physiology.

[76]  Daniel Karcher,et al.  Horizontal genome transfer as an asexual path to the formation of new species , 2014, Nature.

[77]  G. Brader,et al.  An abundant ‘Candidatus Phytoplasma solani’ tuf b strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus , 2014, European Journal of Plant Pathology.

[78]  A. Wallingford,et al.  Grapevine rootstock effects on scion sap phenolic levels, resistance to Xylella fastidiosa infection, and progression of Pierce's disease , 2013, Front. Plant Sci..

[79]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[80]  C. Sorlini,et al.  Plant Growth Promotion Potential Is Equally Represented in Diverse Grapevine Root-Associated Bacterial Communities from Different Biopedoclimatic Environments , 2013, BioMed research international.

[81]  P. Poole,et al.  The plant microbiome , 2013, Genome Biology.

[82]  P. Schulze-Lefert,et al.  Structure and functions of the bacterial microbiota of plants. , 2013, Annual review of plant biology.

[83]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[84]  N. Ollat,et al.  Mapping genetic loci for tolerance to lime-induced iron deficiency chlorosis in grapevine rootstocks (Vitis sp.) , 2013, Theoretical and Applied Genetics.

[85]  A. Klindworth,et al.  Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies , 2012, Nucleic acids research.

[86]  C. Pieterse,et al.  The rhizosphere microbiome and plant health. , 2012, Trends in plant science.

[87]  Yi Wang,et al.  mvabund– an R package for model‐based analysis of multivariate abundance data , 2012 .

[88]  S. Yousaf,et al.  Fungal Endophytic Communities in Grapevines (Vitis vinifera L.) Respond to Crop Management , 2012, Applied and Environmental Microbiology.

[89]  M. Carvajal,et al.  Physiological aspects of rootstock-scion interactions , 2010 .

[90]  R. Cohen,et al.  Hormonal signaling in rootstock–scion interactions , 2010 .

[91]  Tom Beeckman,et al.  Auxin control of root development. , 2010, Cold Spring Harbor perspectives in biology.

[92]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[93]  S. Cookson,et al.  Scion genotype controls biomass allocation and root development in grafted grapevine , 2009 .

[94]  E. Rosenberg,et al.  Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. , 2008, FEMS microbiology reviews.

[95]  R. Costa,et al.  Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. , 2006, FEMS microbiology ecology.

[96]  N. Battey,et al.  Phylloxera and the grapevine: a sense of common purpose? , 2005, Journal of experimental botany.

[97]  P. Ciais,et al.  Europe-wide reduction in primary productivity caused by the heat and drought in 2003 , 2005, Nature.

[98]  Andrés Zurita-Silva,et al.  Rootstock: Scion combinations and nutrient uptake in grapevines , 2020 .

[99]  Muhammad Saleem,et al.  More Than the Sum of Its Parts: Microbiome Biodiversity as a Driver of Plant Growth and Soil Health , 2019, Annual Review of Ecology, Evolution, and Systematics.

[100]  T. Northen,et al.  Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? , 2018, Trends in plant science.

[101]  S. Cookson,et al.  Physiological and molecular mechanisms underlying graft compatibility. , 2017 .

[102]  I. Dodd,et al.  Rootstock-Scion Signalling: Key Factors Mediating Scion Performance , 2017 .

[103]  C. Sorlini,et al.  Root-associated bacteria promote grapevine growth: from the laboratory to the field , 2016, Plant and Soil.

[104]  D. Daffonchio,et al.  The plant growth promoting microbiome increases grapevine resistance to drought stress : a collaborative study between Fondazione Bussolera Branca, Le Fracce farm and Milan Universities , 2012 .

[105]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[106]  L. Nussaume,et al.  Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas , 2001, Planta.