The microbiota of the grapevine holobiont: A key component of plant health

Abstract

Background: Grapevine is a woody, perennial plant of high economic importance worldwide. Like other plants, it lives in close association with large numbers of microorganisms. Bacteria, fungi and viruses are structured in communities, and each individual can be beneficial, neutral or harmful to the plant. In this sense, microorganisms can interact with each other and regulate plant functions (including immunity) and even provide new ones. Thus, the grapevine associated with its microbial communities constitutes a supra-organism, also called a holobiont, whose functioning is linked to established plant-microorganism interactions.

Aim of review: The overall health of the plant may be conditioned by the diversity and structure of microbial communities. Consequently, an optimal microbial composition will consist of a microbial balance allowing the plant to be healthy. Conversely, an imbalance of microbial populations could lead to (or be generated by) a decline of the plant. The microbiome is an active component of the host also responsive to biotic and abiotic changes; in that respect, a better understanding of the most important drivers of the composition of plant microbiomes is needed.

Key scientific concepts of review: This article presents the current state of the art about the grapevine microbiota and its composition according to the plant compartments and the influencing factors. We also focus on situations of imbalance, in particular during plant disease or decline. Finally, we discuss the possible interest of microbial engineering in an agrosystem such as viticulture.

Keywords: Decline; Grapevine; Holobiont; Microbial balance; Microbiota.

Graphical abstract

Fig. 1

Factors known to affect the composition and the structure of grapevine microbiota.

Fig. 2

Above‐ground parts of white grapevine Vitis vinifera cv. Furmint share core members of the fungal microbiome. Four different compartments (young leaf, old leaf, grape and rachis) have been sampled in 6 different vineyards (STT, BET, NEG, URA, KIR, HAN) in Hungary, at three different developmental stages (spring, summer, autumn) within the same growing year. The fungal endophytic microbiome is dominated by Aureobasidium pullulans, Cladosporium spp. and Alternaria alternata at every site, season and plant organ, according to Knapp et al., 2021 .

Fig. 3

Meta-barcoding analysis of fungal (A) and bacterial (B) microbiota colonizing non-necrotic woody tissues from healthy and esca-diseased young grapevines. DNAs were extracted from different organs: rootstock, trunk and cordon. Only the 10 most abundant orders are displayed. In this experimental context, fungal and bacterial microbiota varied according to organs but not diseased plant status (according to Bruez et al., 2020[146]).

Fig. 4

Grapevine-microorganism and microorganism-microorganism relationships in the soil. Such types of interactions are multiple and complex: 1 Root exudates recruit and feed microorganisms. 2 Some microorganisms are nitrogen or phosphorus fixators and mineralize organic matter. Arbuscular mycorrhizal fungi (AMF) supply the host with nutrient resources that are inaccessible to the roots because of their location (biofertilization). 3 Some pathogenic agents can induce declines. 4 In addition to their ability to induce the production of phytohormones by plants, certain plant-growth-promoting bacteria (PGPB) can synthesize them directly. Certain phytohormones regulate plant growth and increase plant tolerance to biotic and abiotic stresses (biostimulation). 5 Some PGPB and AMF participate in the inhibition or suppression of pathogens via competition for ecological niches or for resources through antagonism, by inducing plant resistance, by interfering with the pathogen signaling systems or by suppressing pathogen virulence factors (biocontrol/bioprotection). 6 The mycelium and the mucilage of certain microorganisms enhance the cohesion between soil particles and create microaggregates; as a result, the soil structure is improved (inspired from [161]).