Born to rewild: Reconnecting beneficial plant-microbiome alliances for resilient future crops

Plant domestication has profoundly shaped human history by transforming wild plants into crops capable of sustaining growing populations. Selection for yield, storage, and edibility restructured plant genomes through domestication sweeps, polyploidy, and genetic bottlenecks, collectively known as the domestication syndrome. At the same time, relocating crops from their native habitats to human-managed environments disrupted long-standing coevolutionary relationships among plants, soils, and their associated microbiota (Chapter 1). This thesis investigates how domestication and modern agriculture altered plant–microbiome interactions in potato (Solanum tuberosum) (Chapter 2), how restoring native microbes enhances plant health (Chapter 3), and how the soil microbiome modulates heterosis in modern breeding systems (Chapter 4). Together, these findings contribute to the emerging concept of plant microbiome rewilding and its relevance for sustainable agriculture. Chapter 2 examines habitat domestication in the potato center of origin in South America. A latitudinal survey across 14 paired native and agricultural sites in the Ecuadorian Andes revealed that conversion of native vegetation into cropland homogenized both soil chemistry and microbiome composition. Native soils exhibited strong gradients in chemical properties, reflecting distinct microbial assemblages. Agricultural practices erased these gradients, producing chemically uniform soils that are disconnected from their natural variability. Diverse, site-specific microbial communities were replaced by functionally convergent assemblages dominated by disturbance-adapted taxa such as Firmicutes and Actinobacteria. These results demonstrate that habitat domestication simplifies soil microbiomes and erases functional diversity. Chapter 3 investigates whether microbial taxa lost during domestication retain functional importance and whether their reintroduction can restore plant protection. Using soils from the Andean transect, potato plants grown in native soils showed lower severity of late blight caused by Phytophthora infestans compared with those grown in agricultural soils. Soil heat treatments and live-soil transplants confirmed that disease suppression was microbially mediated. A 14-member synthetic bacterial community derived from native-enriched taxa restored protection in heat-treated native and agricultural soils, whereas a community derived from agricultural taxa did not. These findings provide mechanistic support for microbiome rewilding, demonstrating that ancestral microbial consortia can recover lost ecological functions, likely through induced systemic resistance. Chapter 4 integrates microbial ecology with plant genetics to assess how the soil microbiome influences heterosis in true potato seed systems. Six inbred lines and four hybrids were grown in live and sterilized soils. Hybrids displayed greater biomass in live soils, whereas inbreds showed reduced growth and elevated stress responses. A Genotype × Environment × Microbiome model indicated that the microbiome explained more variation in shoot biomass than genotype alone. Although hybrids and inbreds shared largely overlapping rhizosphere communities, inbreds appeared to mount exaggerated immune responses, while hybrids maintained balanced defense signaling. These findings expand the genetic framework of heterosis to include microbial interactions, suggesting that hybrid vigor partly reflects improved host–microbiome homeostasis. Together, this thesis links domestication, ecology, microbial function, and plant breeding within a unified framework. By conceptualizing crops as holobionts, whose fitness depends on both plant and microbial genomes, microbiome rewilding emerges as a strategy to reconnect domesticated crops with beneficial ancestral partners and enhance resilience in sustainable agriculture.