Belowground Microbiota and the Health of Tree Crops

Abstract

Trees are crucial for sustaining life on our planet. Forests and land devoted to tree crops do not only supply essential edible products to humans and animals, but also additional goods such as paper or wood. They also prevent soil erosion, support microbial, animal, and plant biodiversity, play key roles in nutrient and water cycling processes, and mitigate the effects of climate change acting as carbon dioxide sinks. Hence, the health of forests and tree cropping systems is of particular significance. In particular, soil/rhizosphere/root-associated microbial communities (known as microbiota) are decisive to sustain the fitness, development, and productivity of trees. These benefits rely on processes aiming to enhance nutrient assimilation efficiency (plant growth promotion) and/or to protect against a number of (a)biotic constraints. Moreover, specific members of the microbial communities associated with perennial tree crops interact with soil invertebrate food webs, underpinning many density regulation mechanisms. This review discusses belowground microbiota interactions influencing the growth of tree crops. The study of tree-(micro)organism interactions taking place at the belowground level is crucial to understand how they contribute to processes like carbon sequestration, regulation of ecosystem functioning, and nutrient cycling. A comprehensive understanding of the relationship between roots and their associate microbiota can also facilitate the design of novel sustainable approaches for the benefit of these relevant agro-ecosystems. Here, we summarize the methodological approaches to unravel the composition and function of belowground microbiota, the factors influencing their interaction with tree crops, their benefits and harms, with a focus on representative examples of Biological Control Agents (BCA) used against relevant biotic constraints of tree crops. Finally, we add some concluding remarks and suggest future perspectives concerning the microbiota-assisted management strategies to sustain tree crops.

Keywords: belowground microbiota; biological control agents; endophytes; mycorrhiza; phytoparasitic nematodes; plant-growth-promoting microorganisms; soil-borne pathogens; tree crops.

Figure 1

Total world surface (triangles) and yield/hectar (solid squares) of main tree crops (citrus, fresh and tropical, pome and stone fruits) (source FAOSTAT: http://fenix.fao.org/faostat/beta/en/).

Figure 2

A simplified food web describing main soil components and their relationships. The nodes are classified by roles as: primary root (dark green), beneficial soil components, organisms or promoters, including soil factors (blue), decomposers (brown), pathogens (orange) and biocontrol agents or antagonists (pale green). Arrows show negative effects (A), such as predation, parasitism, pathogenicity or (B) positive links, such as growth promotion, symbiosis or alimentary provision. Indirect factors such as those related to abundance, competition or other density-dependent effects are not included. Node labels and sizes are proportional to their connection level (number of edges). Analysis produced with Gephi (Bastian et al., 2009).

Figure 3

Summary of the benefits that belowground microbiota (or some of their components) may confer to tree crops.

Figure 4

Chlamydospores of the nematode parasitic and root endophytic hyphomycete Pochonia chlamydosporia showing their persistent cellular structure (A). Hyphae emerging from killed root-knot nematode eggs, in vitro (B). The aquatic fungus Catenaria anguillulae (C) is one of the most common parasites of nematodes (in the picture inside Xiphinema sp.) killing its hosts in a few hours. However, in spite of its ubiquity and polyphagy, and due to the zoospores dependence on water for host attachment, a persistent regulation of phytoparasitic nematodes is seldom observed.

Figure 5

A strategy to manage biotic constraints affecting tree crops (i.e., pathogens, pests, invasive species) based on the identification, characterisation and harnessing of soil/root microbiota [based on a conceptual framework by Kowalski et al. (2015)].