Chapter Two - The functional microbiome of grapevine throughout plant evolutionary history and lifetime

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Abstract

European grapevine is a complex holobiont composed of two plant genomes, that of the scion (Vitis vinifera L.) and the rootstock (Vitis spp.), and a multitude of microbial genomes that collectively form the microbiome. The grapevine microbiome has been extensively described over the last decade, primarily using metabarcoding approaches. Unfortunately, metabarcoding data alone provide little information on microbial functions and outcomes of plant-microbe interactions. Here we review knowledge about the microorganisms that have a demonstrated influence, positive or negative, on the performance of the grapevine holobiont. Our review encompasses bacteria, filamentous fungi, yeasts, oomycetes and viruses. It covers aboveground and belowground microorganisms, including arbuscular mycorrhizal and ectomycorrhizal fungi. We focus on taxa and functions that protect the plant against pathogens and pests, promote growth, increase tolerance to abiotic stresses and highlight those involved in disease and decline. As the outcomes of plant-microbe interactions are labile, we examine the dynamics and functions of grapevine-microbiome interactions over both the plant lifetime and the plant evolutionary history, beginning with plant domestication. Based on the knowledge and gaps we identify, we suggest field sampling designs, culture-based experiments, molecular tools and theoretical analysis methods, including shotgun metagenomics and network models, that could be used in future research to uncover and leverage the full functional potential of the grapevine microbiome.

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.

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