Early-onset Dynamics of Arbuscular Mycorrhizal Symbiosis Reprogram Metabolic and Physiological Responses in Tomato Roots

Abstract Arbuscular mycorrhizal fungi (AMF) are widely utilized in agriculture to enhance plant fitness. However, the processes underlying symbiosis establishment remain poorly understood. This study investigates the dynamics of mycorrhization in tomato plants ( Solanum lycopersicum L.) over one month in environmentally controlled condition, integrating metabolomics analysis of roots and root exudates with phenotypic traits, including morphological (RGB imaging) and physiological (fluorescent imaging) analyses to study the onset of symbiotic relationships when AMF were applied at either seeding or post-germination. The results revealed that AMF reduced root system growth at one-month post-germination but enhanced photosynthetic efficiency (Fv/Fm), suggesting a “metabolic cost” induced by the fungal association. Notably, the shoot/root ratio significantly increased by 102% in seed-treated and 45% in post-germination inoculated plants. Interestingly, AMF decreased tomato performance during the early stages of development compared to their untreated counterparts. Shoot biomass decreased by 30% and 25% under seed priming and fungal inoculation, respectively. The development of the root system was also adversely affected, with an average reduction in biomass of 35% and in length of 31%. Metabolomics results indicate that AMF slows initial plant growth to facilitate the establishment of symbiosis, pushing resources towards secondary metabolism and exudation of recruiting compounds. Application methods influenced early-stage physiological responses, with post-germination inoculated plants exhibiting higher “metabolic cost” than seed-primed counterparts. Mycorrhization in tomato was fully established approximately 27 days after AMF treatment.