Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)

Abstract

Plants deploy both primary and species-specific, specialized metabolites to communicate with other organisms and adapt to environmental challenges, including interactions with soil-dwelling microbial communities. However, the role of specialized metabolites in modulating plant-microbiome interactions often remains elusive. In this study, we report that maize (Zea mays) diterpenoid metabolites with known antifungal bioactivities also influence rhizosphere bacterial communities. Metabolite profiling showed that dolabralexins, antibiotic diterpenoids that are highly abundant in roots of some maize varieties, can be exuded from the roots. Comparative 16S rRNA gene sequencing determined the bacterial community composition of the maize mutant Zman2 (anther ear 2), which is deficient in dolabralexins and closely related bioactive kauralexin diterpenoids. The Zman2 rhizosphere microbiome differed significantly from the wild-type sibling with the most significant changes observed for Alphaproteobacteria of the order Sphingomonadales. Metabolomics analyses support that these differences are attributed to the diterpenoid deficiency of the Zman2 mutant, rather than other large-scale metabolome alterations. Together, these findings support physiological functions of maize diterpenoids beyond known chemical defenses, including the assembly of the rhizosphere microbiome.

Triterpenoid and Steroidal Saponins Differentially Influence Soil Bacterial Genera

“…In the last decade, multiple studies have revealed that PSMs are involved in the formation of the rhizosphere and root microbiome [ 10 , 11 ]. PSM-deficient mutants of certain plant species, such as thale cress ( Arabidopsis thaliana ) and maize ( Zea mays ), show that di-, sester-, tri-terpenoids, coumarins, and benzoxazinoids modulate the root-associated microbiome [ 12 , 13 , 14 , 15 , 16 , 17 , 18 ]. The treatment of soils with authentic compounds has also helped to reveal the roles of PSMs such as flavonoids (daidzein and quercetin), alkaloids (nicotine and gramine), benzoxazinoid, and opine (santhopine) in modulating the soil microbiome [ 19 , 20 , 21 , 22 ].…”

Comparative transcriptomics and metabolomics reveal specialized metabolite drought stress responses in switchgrass (Panicum virgatumL.)

“…For example, maize studies demonstrated the accumulation of specialized kauralexin and dolabralexin diterpenoids in response to oxidative, drought and salinity stress (Christensen et al 2018; Mafu et al 2018), and diterpenoid-deficient maize mutants show decreased resilience to abiotic stress (Vaughan et al 2015b). Additionally, antioxidative functions in relation to drought stress have been shown for select diterpenoids (Munné-Bosch and Alegre 2003), and diterpenoid roles in the root microbiome assembly have been suggested based on changes in the microbiome composition in the kauralexin- and dolabralexin-deficient maize an2 mutant (Murphy et al 2021).…”

Functions and biosynthesis of plant signaling metabolites mediating plant–microbe interactions

“…Dolabralexins (6,7,8) could not only inhibit Fusarium verticillioides and Fusarium graminearum 37 but also modulate rhizosphere microbiota with a pronounced change in Alphaproteobacteria abundance. 39 Similar to kauralexins (4, 5) and dolabralexins (6,7,8) found in maize, rice produces phytoalexins momilactones (9, 10), phytocassanes (11,12), and oryzalexins (13,14) for chemical defense purpose. 40 Amongst these, momilactones (9, 10) are the most intensively studied ones in terms of both biosynthesis and bioactivity.…”