In their natural environment plants are part of a rich ecosystem including numerous and diverse microorganisms in the soil. It has been long recognized that some of these microbes, such as mycorrhizal fungi or nitrogen fixing symbiotic bacteria, play important roles in plant performance by improving mineral nutrition. However, the full range of microbes associated with plants and their potential to replace synthetic agricultural inputs has only recently started to be uncovered. In the last few years a great progress has been made in the knowledge on composition of rhizospheric microbiomes and their dynamics. There is clear evidence that plants shape microbiome structures, most probably by root exudates, and also that bacteria have developed various adaptations to thrive in the rhizospheric niche. The mechanisms of these interactions and the processes driving the alterations in microbiomes are however largely unknown. In this review we focus on the interaction of plants and root associated bacteria enhancing plant mineral nutrition, summarizing the current knowledge in several research fields that can converge to improve our understanding of the molecular mechanisms underpinning this phenomenon.

One of the major questions in contemporary plant science involves determining the functional mechanisms that plants use to shape their microbiome. Plants produce a plethora of chemically diverse secondary metabolites, many of which exert bioactive effects on microorganisms. Several recent publications have unequivocally shown that plant secondary metabolites affect microbiome composition and function. These studies have pinpointed that the microbiome can be influenced by a diverse set of molecules, including: coumarins, glucosinolates, benzoxazinoids, camalexin, and triterpenes. In this review, we summarize the role of secondary metabolites in shaping the plant microbiome, highlighting recent literature. A body of knowledge is now emerging that links specific plant metabolites with distinct microbial responses, mediated via defined biochemical mechanisms. There is significant potential to boost agricultural sustainability via the targeted enhancement of beneficial microbial traits, and here we argue that the newly discovered links between root chemistry and microbiome composition could provide a new set of tools for rationally manipulating the plant microbiome.

Significance: To address mechanisms by which plants control their associated microorganisms, we designed a screen using a bacterial activity in soil. A detailed analysis of a candidate gene from the screen, CYP71A27 , identified an additional root-specific component of synthesis of camalexin, a natural product involved in plant defense against pathogens. Loss of function of CYP71A27 affected not only the microbiota in soil but also interactions with single plant growth-promoting bacteria. The loss of the promoting effect in the mutants could be complemented chemically by adding camalexin to the bacteria. Thus, our study identified an additional role for camalexin in facilitating interaction with microbes in the rhizosphere and an additional gene for its synthesis.