Arbuscular mycorrhizal fungi‐indicative blumenol‐C‐glucosides predict lipid accumulations and fitness in plants grown without competitors

Abstract

Summary Hydroxy‐ and carboxyblumenol C‐glucosides specifically accumulate in roots and leaves of plants harboring arbuscular mycorrhizal fungi (AMF). To explore blumenol function in AMF relationships, we silenced an early key‐gene in blumenol biosynthesis, CCD1 (carotenoid cleavage dioxygenase 1), in the ecological model plant, Nicotiana attenuata, and analyzed whole‐plant performance in comparison with control and CCaMK‐silenced plants, unable to form AMF associations. Root blumenol accumulations reflected a plant's Darwinian fitness, as estimated by capsule production, and were positively correlated with AMF‐specific lipid accumulations in roots, with relationships that changed as plants matured when grown without competitors. When grown with wild‐type competitors, transformed plants with decreased photosynthetic capacity or increased carbon flux to roots had blumenol accumulations that predicted plant fitness and genotype trends in AMF‐specific lipids, but had similar levels of AMF‐specific lipids between competing plants, likely reflecting AMF‐networks. We propose that when grown in isolation, blumenol accumulations reflect AMF‐specific lipid allocations and plant fitness. When grown with competitors, blumenol accumulations predict fitness outcomes, but not the more complicated AMF‐specific lipid accumulations. RNA‐seq analysis provided candidates for the final biosynthetic steps of these AMF‐indicative blumenol C‐glucosides; abrogation of these steps will provide valuable tools for understanding blumenol function in this context‐dependent mutualism.