Missing symbionts–emerging pathogens? Microbiome management for sustainable agriculture

Plant diversification and co-evolution shaped the plant microbiome and vice versa. This resulted in a specific composition of the plant microbiome and a strong connection with the host in terms of functional interplay. Symbionts are part of the microbiota, and important for the plant’s germination and growth, nutrition, as well as stress protection. However, human activities in the Anthropocene are linked to a significant shift of diversity, evenness and specificity of the plant microbiota. In addition, and very importantly, many plant symbionts are missing or no longer functional. It will require targeted microbiome management to support and reintroduce them. In future agriculture, we should aim at replacing harmful chemicals in the field, as well as post-harvest, by using precision microbiome engineering. This is because the plant microbiome is connected across systems and crucial for human and planetary health. This commentary aims to inspire holistic studies for the development of solutions for sustainable agriculture in framework of the One Health and the Planetary Health concepts.
1 Plants are holobionts and consist of the plant and its co-evolved microbiota

All plants are holobionts; they form a structural and functional unit with microorganisms (Vandenkoornhuyse et al. 2015). Plant-associated microorganisms comprise bacteria, archaea, fungi, algae and protists, the so-called plant microbiota (Berg et al. 2020). On surfaces and within plant tissues they are the plant microbiome, which can be differentiated into the phyllosphere (above ground), rhizosphere (below ground) and endosphere (inside tissues) microbiome. Plant microbiomes are diversified in each of these habitats and adapt to the specific conditions that require functional engagement (Cordovez et al. 2019). Moreover, they are specific for each plant species/genotype and each stage of development (Berg and Smalla 2009).This specificity is a result of plant-microbe coevolution (Delaux and Schornack 2021). Since plants colonized land, they have evolved a range of symbiotic associations with microorganisms that include protection mechanisms (Delaux and Schornack 2021). These symbiotic associations were likely required by plants to grow under harsh, nutrient-poor, and difficult conditions and involved symbiotic plant-microbe interactions resulting in survival and cooperation (Fig. 1).