Plant-driven assembly of disease-suppressive microbiomes

In agriculture, crop yields are challenged by pathogenic microorganisms that cause disease. As a result, global food production heavily relies on chemical pesticides to prevent crop losses. However, plants host complex and diverse microbial communities, that in addition to pathogens also comprise commensal and beneficial microbes. Plant-associated microbiomes are crucial for sustaining plant health. Plants govern the composition of these microbiomes, thereby extending their adaptability to environmental stresses. Upon pathogen attack, plants can recruit beneficial microbes and assemble a disease-suppressive microbiome that combats the pathogen. The current knowledge on the plant-driven assembly of disease-suppressive microbiomes was extensively reviewed in Chapter 1. A notable example is provided by Arabidopsis thaliana (Arabidopsis) plants infected aboveground by the foliar obligate biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) that initiate the selective assembly of beneficial microbes. As result, a disease-suppressive soilborne legacy (SBL) is created that protects a next plant population grown in the same soil against Hpa. In this dissertation, we investigated the microbiota that form the disease-suppressive SBL, the plant-driven processes by which they are assembled upon infection, and how they are transmitted to a next generation of plants grown in the disease-suppressive soil. First, we found that foliar Hpa infection alters the metabolic profile exuded from plant roots, affecting microbiome composition (Chapter 2). The production of coumarins by diseased plants was shown to be required for the creation of the disease-suppressive SBL. In Chapter 3, we found that Hpa infection impacts the microbiome on the aboveground plant parts in particular. Leaves of Hpa-infected plants are selectively enriched for highly specific and abundant Hpa-associated microbiota (HAM) that thrive in the infected environment but suppress Hpa. We showed that HAM are assembled by the diseased plants and that their buildup is causal to the creation of the disease-suppressive SBL (Chapters 3 & 4). Finally, we found that although transmitted via soil, HAM are primarily assembled and predominantly accumulate on aboveground plant parts of successive plant population grown in the disease-suppressive SBL soil (Chapter 4). Thus, downy mildew disease-suppressive soils transmit a protective microbiome to the leaves of a next generation of plants. Our findings highlight a crucial link between belowground and aboveground plant-driven microbiome assembly processes and underscore the phyllosphere as a key hub for the accumulation of soilborne disease-suppressive microbiomes. In Chapter 5, these findings are discussed in a broader perspective by exploring the processes that may govern HAM assembly and functioning and linking these between aboveground and belowground microbial habitats. We propose that disease-associated microbiomes are selected as crucial moderators of plant-pathogen interactions. Developing crop protection strategies that harness their plant-beneficial potential could pave the way for a more sustainable form of agriculture.