Plant specialized metabolites modulate root microbiomes

Abstract

Plants are surrounded by myriad microbes during their growth, death, and importantly, evolution (Zhang et al., 2018). It is well known that the interaction between plantassociated microbes and their hosts greatly impacts host development and health (Verbon and Liberman, 2016; Berendsen et al., 2012). One of the strategies employed by plants to defend themselves against pathogens and adapt to adverse conditions is to selectively recruit specific host-associated microbial communities possessing beneficial functions. Thus far, numerous attempts have been made to elucidate the ways by which plants regulate host-associated microbiota. Plant immune signaling (Lebeis et al., 2015) and phosphate starvation responses (Castrillo et al., 2017) have been identified to be involved in this process. In particular, plant specialized metabolites (PSMs), including root-derived organic molecules made from ~20% of the photosynthesized carbon, have clearly been shown to affect the establishment of plant microbiota. However, our knowledge as to how these PSMs modulate or control plant microbiomes is still very limited. Two recent publications by Huang et al. (Huang et al., 2019) and Chen et al. (Chen et al., 2019) reported that terpenoids, a major component of the root-specialized metabolites, contribute substantially to the assembly of Arabidopsis-specific root microbiota by selectively regulating the growth of root bacteria from different taxa (Figure 1). In these two articles, through a series of genetic and biochemical assays, Dr. Anne Osbourn from the John Innes Centre, Dr. Yang Bai and Dr. Guodong Wang from the Chinese Academy of Sciences, and their colleagues clarified the biosynthetic pathways for three triterpenes (thalianin, thalianol-derived medium-chain saturated triterpene fatty acid esters [TFAEs], and arabidin) and characterized two sesterterpene biosynthesis gene clusters in Arabidopsis. The triterpene biosynthetic network identified by Huang and colleagues, originating from evolutionarily divergent biosynthetic gene clusters, is capable of synthesizing more than 50 root metabolites. Furthermore, Chen and colleagues discovered that a single amino acid is enough to determine the substrate specificity of sesterterpene synthases (sesterTPSs). These results have substantially expanded our understanding of the in planta biosynthesis of terpenoids, the largest and most diverse plant natural product group, which may play a role in the control of root-associated microbial communities by hosts. To address the question of whether or not the terpenoid compounds produced by plants can influence root microbiota, Huang, Chen, and colleagues investigated the impacts of triterpene and sesterterpene biosynthesis on Arabidopsis root microbiome assembly. They compared the root microbiota of the field-grown Arabidopsis terpenoid pathway mutants with those of the wild type using deep 16S ribosome RNA gene sequencing, and found that the compositions of the root-associated bacterial communities of these mutants were significantly different from those of the wild-type plants. Moreover, similar root microbiota modulation patterns were exhibited by distinct mutants. These findings clearly showed that terpenoid biosynthesis profoundly af-