Confronting stresses affecting olive cultivation from the holobiont perspective

Abstract

The holobiont concept has revolutionized our understanding of plant-associated microbiomes and their significance for the development, fitness, growth and resilience of their host plants. The olive tree holds an iconic status within the Mediterranean Basin. Innovative changes introduced in olive cropping systems, driven by the increasing demand of its derived products, are not only modifying the traditional landscape of this relevant commodity but may also imply that either traditional or emerging stresses can affect it in ways yet to be thoroughly investigated. Incomplete information is currently available about the impact of abiotic and biotic pressures on the olive holobiont, what includes the specific features of its associated microbiome in relation to the host's structural, chemical, genetic and physiological traits. This comprehensive review consolidates the existing knowledge about stress factors affecting olive cultivation and compiles the information available of the microbiota associated with different olive tissues and organs. We aim to offer, based on the existing evidence, an insightful perspective of diverse stressing factors that may disturb the structure, composition and network interactions of the olive-associated microbial communities, underscoring the importance to adopt a more holistic methodology. The identification of knowledge gaps emphasizes the need for multilevel research approaches and to consider the holobiont conceptual framework in future investigations. By doing so, more powerful tools to promote olive's health, productivity and resilience can be envisaged. These tools may assist in the designing of more sustainable agronomic practices and novel breeding strategies to effectively face evolving environmental challenges and the growing demand of high quality food products.

Keywords: Olea europaea; Xylella fastidiosa; biocontrol; co-occurrence network analysis; olive microbiome; plant functional traits; root architecture; verticillium wilt of olive.

Figure 1

Acreage and productions of olive oil and table olives at world scale in 2020. The image was created with data from FAOSTAT 2021 (production quantities of olives by country). The tree drawings on the right show, in descending order, the percentages of the different olive cultivation systems: traditional (less than 140 tress/ha), medium-density (from 140 to 399 trees/ha) and high-density (over 400 trees/ha) (Russo et al., 2016). The drawings of the oil bottle and the olive below represent the percentages of olive production dedicated to oil and table olives, respectively.

Figure 2

Schematic summary of the most relevant abiotic and biotic stresses that can affect olive trees. Arrows point to the plant parts that can be affected by the particular stress (i.e. leaf, flower, fruit, trunk, stem, root). The figure was created with BioRender.com.

Figure 3

Schematic representation of the interactions between the olive plant and its associated microbial communities present in above- and belowground compartments. Based on Bettenfeld et al. (2020).

Figure 4

Schematic representation of the analysis of the interaction between the root system of VWO-tolerant (left) and VWO-susceptible (right) olive cultivars and Verticillium dahliae under the holobiont perspective. The differences in root system architecture are symbolised by diverse representation of the root morphology. The high (VWO-tolerant plants) (1) or low (VWO-susceptible plants) (2) content of lignin is shown by blue lines (or their absence) over the lignocellulose structure (drawn as a green cylinder). The faster (VWO-tolerant plants) (3) and slower/absent (VWO-susceptible plants) (4) expression of defence genes, in presence of the pathogen, is represented by DNA helices (marked with a red X in the case of slow/null expression). The high content in secoiridoids in VWO-tolerant plants (5) is represented by the chemical formula of oleuropein. The different taxonomical composition of the VWO-tolerant and VWO-susceptible associated microbial communities is shown in green and red, respectively. In the bottom part, a schematic, simplified representation of the main effects of V. dahliae inoculation in root endosphere and rhizosphere microbial networks is shown. Red edges represent negative interactions between modules (solid circles) and the red circle represents the module that includes the pathogen. Based on Cardoni et al. (2022) and Fernández-González et al. (2020a), and partially generated with BioRender.com.