Bumblebees sense rootstock-mediated nutrition and fertilization regime in tomato

Aims Since producing more with less is required for increasing agricultural sustainability and reducing its environmental impact, breeding varieties with increased yield stability under reduced fertilizer application is an important goal, particularly in high valued horticultural crops such as tomato ( Solanum lycopersicum L.). However, because of the difficulties to conciliate yield and fertilizer use efficiency through breeding, the graft-compatible genetic biodiversity existing in horticultural species offers the possibility to directly approach this objective in high-yielding elite varieties through improving nutrient capture and promoting ecosystem services such as insect pollination. We hypothesized that rootstocks affect pollinator foraging decisions through the nutritional status that impacts yield. Methods Fifteen genetically diverse experimental rootstocks were grafted to a scion tomato variety and cultivated under optimal and reduced (25% of optimal) P and NPK fertilization in the presence of managed bumblebee pollinators ( Bombus terrestris ). Results Up to twofold yield variability between rootstocks was associated with leaf nutrition and photosynthesis of the scion. Interestingly, fertilization regime and the rootstock genotype influenced the pollinator foraging decisions since bumblebees showed feeding preference for plants cultivated under low P, and for the most yielding and nutritious graft combinations under reduced but not under optimal fertilization. Bumblebees can sense plant nutritional status through source-sink relations, as supported by the consistent relationship between pollinator preferences and leaf carbon concentration. Conclusions This study opens new perspectives for using pollinators as “phenotypers” to select the most resilient plants under suboptimal conditions and/or genotypes that synergistically increase crop productivity by promoting the ecosystem service provided by the insects.