Comparative transcriptomics between Solanum lycopersicum and S. pennellii sheds light into adaptation to arbuscular mycorrhizal symbiosis and combined stress resilience

The root-associated microbiota can protect plants against biotic and abiotic stresses. A role in plant resilience to nutrients limitation and drought, major issues for crop productivity in modern agriculture, has been attributed to arbuscular mycorrhizal (AM) fungi that establish a mutualistic symbiosis with most land plants. Among Mediterranean crops, tomato (Solanum lycopersicum) will be one of the most disadvantaged, and innovative solutions, from genotypes selection to growing practices, are required. In this work we characterized, under controlled conditions, susceptibility and responsiveness to the AM fungus Funneliformis mosseae in the tomato ‘M82’ cultivar and the drought-tolerant wild species Solanum pennellii, which is largely exploited in tomato breeding. S. pennellii showed a reduced colonization, although arbuscule morphology was normal, and a negative growth response upon AM inoculation, differently from tomato. To elucidate the molecular mechanisms underpinning this phenotype an RNA-seq was performed considering both species and combined water/nutrient stress conditions. Among 20,162 orthologs identified, 1,822 genes were modulated by AM symbiosis across species and conditions. Under well-watered conditions, the number of AM-responsive genes was lower in S. pennellii compared to tomato, but under combined-stress numbers were similar. A different expression pattern was observed in symbiotic signaling pathway genes since the up-regulation detected in tomato under well-watered conditions was not observed in S. pennellii. Also genes involved in synthesis and metabolism of strigolactones, important signaling molecules during early AM interaction, showed a lower expression in S. pennellii. However, no difference was found in the expression of genes related to nutrient exchanges, in line with the occurrence in S. pennellii roots of few, but well-developed, arbuscules. This work will enlarge our knowledge on plant adaptation to the AM symbiosis and on the effect of the symbiosis on plant responses to water and nutrients limiting conditions, possibly highlighting relevant alleles involved in plant resilience.