Chapter Two - The functional microbiome of grapevine throughout plant evolutionary history and lifetime
Introduction
European cultivated grapevine is a complex and dynamic system of plant-microbe interactions that has been shaped by humankind to produce grapes and wine. Each plant individual is typically composed of two plant genomes, that of the rootstock (Vitis spp.) and the scion (Vitis vinifera L.), onto which are linked a multitude of microbial and viral genomes. The set of microbial genomes forms the microbiome (Berg et al., 2020; Compant et al., 2019; Saikkonen et al., 2020), while the set of viral genomes forms the virome (Roossinck, 2010). The whole, including the plant genomes, forms the hologenome (Bettenfeld et al., 2021; Theis et al., 2016; Zilber-Rosenberg and Rosenberg, 2008). This concept of each grapevine individual as being a complex and dynamic system of plant-microbe interactions (i.e., an holobiont; Bettenfeld et al., 2021; Vandenkoornhuyse et al., 2015) has not been necessary, for most of human history, to grow vines and produce wine. It could provide solutions in the future, however, to maintain grapevine cultivation in a context of climate change (Gambetta et al., 2020) and pesticide-free agriculture (Jacquet et al., 2022; Pertot et al., 2017).
The objective of this chapter is to present the state of art about the dynamics of grapevine-microbiome interactions, from the evolutionary time scale to the seasonal scale, and to propose some research avenues to increase knowledge on the functions of the grapevine microbiome. The chapter first gives an overview of the evolution of the grapevine microbiome, starting with grapevine domestication (Section 2), and then describes the microbiome dynamics during the lifetime of each plant, from the grafting stage in the nursery through to decline in the vineyard (Section 3). In both sections, we specifically highlight those microorganisms and viruses that have a demonstrated influence, positive or negative, on the performance of the grapevine holobiont (health, growth and berry quality). Based on this state of art, we suggest experimental and theoretical approaches that could lead to a better understanding of the functions of the grapevine microbiome (Section 4). We propose some experiments to identify the microbial taxa and functions that play a key role in grapevine performance under drought conditions and in agro-ecological settings. We describe how to decipher the microbial interaction networks to which these key taxa belong, to understand how they maintain in the system and regulate grapevine performance. We also provide recommendations about the biogeographic regions that could be explored in the future to isolate beneficial microbial taxa, which could then be inoculated to drive the system.
Section snippets
The grapevine functional microbiome throughout evolutionary history
This section reviews the knowledge and gaps regarding microbiome evolution during grapevine domestication and breeding, as well as the microbiome dynamics triggered by microbial dispersal across geographic regions and between members of the Vitis genus. Based on this state of art we hypothesise which geographic regions and plant genetic material are most likely to be associated with beneficial microbial taxa and functions (Fig. 1, Fig. 2).
The grapevine functional microbiome throughout plant lifetime
This section describes how the microbiome assembles, functions and changes over the course of grapevine life. It highlights the plant-microbe interactions that have a proven, direct and significant influence on the grapevine performance (growth, health and berries quality) at every life stage (Fig. 3). The section deals with both the microbiome (bacteria, filamentous fungi, yeasts and oomycetes) and the virome, including phytoviruses (plant-infecting viruses), mycoviruses (fungi-infecting
Let's make the grapevine microbiome more functional
This section proposes experimental and computational approaches that could help uncover the functioning of the grapevine microbiome, with the goal of integrating it into a more sustainable viticulture. We propose field sampling designs and statistical approaches that exploit what we know of the evolution and dynamics of the grapevine microbiome (2 The grapevine functional microbiome throughout evolutionary history, 3 The grapevine functional microbiome throughout plant lifetime) and aim to
Conclusion and perspectives
The grapevine microbiome has developed over thousands of years, integrating taxa from Asia, Europe and America, under the pressures of human selection and pathogen invasions. There are many gaps in this history, but the numerous studies of the grapevine microbiome show that it contains beneficial microorganisms (plant growth-promoting bacteria, mycorrhizae, biocontrol agents, microorganisms of oenological interest) whose mode of action is sometimes well documented. These beneficial
Acknowledgements
We are very grateful to Maureen Pellan for the design of Fig. 3. The authors acknowledge the support of the French National Research Agency (ANR) under the grants 20-PCPA-0010 (PPR VITAE) and ANR-17-CE32-0011 (NGB), and of FranceAgrimer and CNIV under the grant n°2018-52537 (Vitirhizobiome). LP received funding from Fondation Bordeaux Université.
References (415)
- et al.
The microbial ecology of wine grape berries
Int. J. Food Microbiol.
(2012) - et al.
All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices
Ecol. Model.
(2002) The life-cycle of Plasmopara viticola, cause of downy mildew of vine
Mycologist
(2000)- et al.
Vineyard microbiome variations during different fertilisation practices revealed by 16s rRNA gene sequencing
Appl. Soil Ecol.
(2018) - et al.
A review on the plant microbiome: ecology, functions, and emerging trends in microbial application
J. Adv. Res.
(2019) - et al.
Revealing cues for fungal interplay in the plant–air interface in vineyards
Front. Plant Sci.
(2019) - et al.
Accounting for environmental variation in co-occurrence modelling reveals the importance of positive interactions in root-associated fungal communities
Mol. Ecol.
(2020) - et al.
The biodiversity of grapevine bacterial endophytes of Vitis amurensis Rupr
Plan. Theory
(2022) - et al.
Biological, molecular, and serological studies of a novel strain of grapevine leafroll-associated virus 2
Virus Genes
(2011) - et al.
Which Winegrape Varieties are Grown Where? A Global Empirical Picture
(2013)
KBase: The United States department of energy systems biology knowledgebase
Nat. Biotechnol.
Grapevine pathogenic microorganisms: understanding infection strategies and host response scenarios
Front. Plant Sci.
How sample heterogeneity can obscure the signal of microbial interactions
ISME J.
Is there a future for wild grapevine (Vitis vinifera subsp. silvestris) in the Rhine Valley?
Biodivers. Conserv.
Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms
Mol. Ecol.
Predictive microbial-based modelling of wheat yields and grain baking quality across a 500 km transect in Québec
FEMS Microbiol. Ecol.
Screening of endophytic bacteria isolated from domesticated and wild growing grapevines as potential biological control agents against crown gall disease
BioControl
Induction of systemic resistance to Agrobacterium tumefaciens by endophytic bacteria in grapevine
Plant Pathol.
Feasibility of applying shotgun metagenomic analyses to grapevine leaf, rhizosphere and soil microbiome characterisation
Aust. J. Grape Wine Res.
Effectiveness of beneficial bacteria to promote systemic resistance of grapevine to gray mold as related to phytoalexin production in vineyards
Plant and Soil
Editorial: recent advances on grapevine-microbe interactions: from signal perception to resistance response
Front. Plant Sci.
The role of root exudates in rhizosphere interactions with plants and other organisms
Annu. Rev. Plant Biol.
TITAN2: Threshold Indicator Taxa Analysis. R Package Version 2.1
Isolation and characterization of a cold-tolerant strain of Fusarium proliferatum, a biocontrol agent of grape downy mildew
Phytopathology
Beneficial bacteria isolated from grapevine inner tissues shape Arabidopsis thaliana roots
Plos one
Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop: cohorts of AM fungi in vineyards
Environ. Microbiol. Rep.
Grape cultivar features differentiate the grape rhizosphere microbiota
Plants
Microbial networks inferred from environmental DNA data for biomonitoring ecosystem change: Strengths and pitfalls
Mol. Ecol. Resour.
Machine learning of microbial interactions using abductive ILP and hypothesis frequency/compression estimation
Diversity and interactomics of bacterial communities associated with dominant trees during tropical forest recovery
Curr. Microbiol.
Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3
Elife
Evaluation of different phyllosphere sample types for parallel metabarcoding of fungi and oomycetes in Vitis vinifera
Phytobiomes J.
Grapevine wood microbiome analysis identifies key fungal pathogens and potential interactions with the bacterial community implicated in grapevine trunk disease appearance
Environ. Microbiome
Metage2Metabo, microbiota-scale metabolic complementarity for the identification of key species
Elife
EsMeCaTa: Estimating metabolic capabilities from taxonomic affiliations
bioRxiv
The effect of vine variety and vintage on wine yeast community structure of grapes and ferments
J. Appl. Microbiol.
Microbiome definition re-visited: old concepts and new challenges
Microbiome
The fungal and bacterial rhizosphere microbiome associated with grapevine rootstock genotypes in mature and young vineyards
Front. Microbiol.
Grapevine trunk diseases: complex and still poorly understood: Grapevine trunk diseases
Plant Pathol.
The microbiota of the grapevine holobiont: a key component of plant health
J. Adv. Res.
Transmission of phage by glassy-winged sharpshooters, a vector of Xylella fastidiosa
Bacteriophage
Generating lineage-resolved, complete metagenome-assembled genomes from complex microbial communities
Nat. Biotechnol.
La vigne comme holobionte: validité du concept, dynamique temporelle, déterminants environnementaux et application à la définition du terroir microbiologique. Doctoral dissertation
University of Rennes
Metabolic network modeling of microbial communities
Wiley Interdiscip. Rev. Syst. Biol. Med.
The contribution of culturomics to the repertoire of isolated human bacterial and archaeal species
Microbiome
The relative susceptibility of grapevine rootstocks to black foot disease is dependent on inoculum pressure
N. Z. Plant Prot.
Grapevine stimulation: a multidisciplinary approach to investigate the effects of biostimulants and a plant defense stimulator
J. Agric. Food Chem.
Climate vs grapevine pests and diseases worldwide: the first results of a global survey
OENO One
Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate
Proc. Natl. Acad. Sci. U. S. A.
Metaproteomic characterization of Vitis vinifera rhizosphere
FEMS Microbiol. Ecol.
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