The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation

Abstract

Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is known about the influence of specialized exudates from crop plants. The aims of this work were to understand whether sorgoleone, a unique lipophilic secondary benzoquinone exuded only from the root hairs of sorghum, influences belowground microbial community structure in the field, to assess the effect of purified sorgoleone on the cultured bacteria from field soils, and to determine whether sorgoleone inhibits nitrification under field conditions. Studies were conducted comparing wild-type sorghum and lines with genetically reduced sorgoleone exudation. In the soil near roots and rhizosphere, sorgoleone influenced microbial community structure as measured by β-diversity and network analysis. Under greenhouse conditions, the soil nitrogen content was an important factor in determining the impacts of sorgoleone. Sorgoleone delayed the formation of the bacterial and archaeal networks early in plant development and only inhibited nitrification at specific sampling times under field conditions. Sorgoleone was also shown to both inhibit and promote cultured bacterial isolate growth in laboratory tests. These findings provide new insights into the role of secondary metabolites in shaping the composition and function of the sorghum root-associated bacterial microbiomes. Understanding how root exudates modify soil microbiomes may potentially unlock an important tool for enhancing crop sustainability and yield in our changing environment. IMPORTANCE Plant roots exude a complex mixture of metabolites into the rhizosphere. Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities in agricultural and natural ecosystems. Previous work on plant root exudates and their influence on soil microbes has mainly been restricted to model plant species. Plant are a diverse group of organisms and produce a wide array of different secondary metabolites. Therefore, it is important to go beyond studies of model plants to fully understand the diverse repertoire of root exudates in crop plant species that feed human populations. Extending studies to a wider array of root exudates will provide a more comprehensive understanding of how the roots of important food crops interact with highly diverse soil microbial communities. This will provide information that could lead to tailoring root exudates for the development of more beneficial plant-soil microbe interactions that will benefit agroecosystem productivity.

Biological and synthetic approaches to inhibiting nitrification in non-tilled Mediterranean soils

“…1a) and in several other studies [41,42]. Nevertheless, previous work with DMP-based nitrification inhibitors and with sorgoleone has shown that there are some shifts in non-target bacterial abundance, even when the total bacterial abundance is not altered, with SNIs associated with decreases in bacterial diversity [43] and BNIs associated with changes in bacterial networks (BNIs) [44]. These studies are still preliminary, so further work should expand these analyses to determine exactly what effects are exerted by these compounds on the soil microbiota.…”

Applications of the indole-alkaloid gramine modulate the assembly of individual members of the barley rhizosphere microbiota

“…A prediction of this observation is that, within the Poaceae family, different classes of secondary metabolites may have evolved to fine-tune microbiota composition. Congruently, sorghum produces a species-specific allelopathic compound designated sorgoleone (Czarnota et al, 2001;Dayan et al, 2010) capable of selectively modulating bacterial microbiota composition as demonstrated by experiments conducted using RNA-interference lines impaired in sorgoleone biosynthesis grown under soil conditions (Wang et al, 2021). Likewise, oat plants impaired in the production of avenacin, a triterpenoid defensive compound active against fungal pathogens (Papadopoulou et al, 1999), recruit a taxonomically distinct rhizosphere microbiota compared to cognate wild type plants .…”

Natural variation in root exudation of GABA and DIMBOA impacts the maize root endosphere and rhizosphere microbiomes

“…The rhizosphere is the area around plant roots influenced by root secretion [2]. Root exudates are the main compounds secreted in the rhizosphere and includes a diversity of carbon-containing primary and secondary metabolites such as amino acids, sugars, organic acids and hormones [3], which serve as energy and carbon sources for the heterotrophic soil microbiota [4,5]. In turn, soil microbial activity release nutrients for plant growth through organic matter decomposition, nitrogen (N) fixation, metal chelation, phytohormones production and also support plant health by alleviating abiotic stresses and suppressing pathogens [6][7][8][9].…”