Plant domestication reshapes rhizosphere microbiome-mediated adaptation to nitrogen stress

Nitrogen (N) is a major limiting nutrient for plant growth in both natural and agricultural ecosystems. While plants have evolved diverse physiological strategies to cope with N stress, mounting evidence indicates that effective N stress adaptation often depends on interactions with the rhizosphere microbiome. However, crop domestication has largely occurred under high-input conditions, potentially weakening plant traits that facilitate microbiome-assisted adaptation. How domestication has reshaped microbiome-mediated N stress responses therefore remains poorly understood.
Using wild tomato (Solanum pennellii) and domesticated tomato (Solanum lycopersicum cv. Moneyberg) as a comparative system, this thesis demonstrates that wild tomato exhibits superior tolerance to severe N limitation. This advantage is linked to a stronger capacity to restructure the rhizosphere microbiome, particularly through the recruitment of functionally distinct Priestia megaterium lineages that enhance host N stress tolerance by modulating microbial community composition. Beyond N starvation, P. megaterium strains also alleviate ammonium toxicity. Using Arabidopsis thaliana, we show that wild-tomato-derived P. megaterium promotes growth under ammonium nutrition by enhancing redox homeostasis via upregulation of host ascorbate peroxidase activity. Furthermore, these beneficial strains mitigate N deficiency-associated biotic stress by suppressing tomato-potato cyst nematode hatching through modulation of root exudate composition and repression of solanoeclepin A biosynthesis.
Together, this work demonstrates that domestication has reshaped microbiome-mediated N stress adaptation and reveals P. megaterium as a multifunctional rhizobacterium integrating nutrient, redox, and biotic stress responses. These findings highlight the rhizosphere microbiome as a critical, yet underappreciated, component of plant adaptive evolution and a promising target for sustainable crop improvement.