Effect of strigolactones on recruitment of the rice root-associated microbiome

Abstract

Strigolactones are endogenous plant hormones regulating plant development and are exuded into the rhizosphere when plants experience nutrient deficiency. There, they promote the mutualistic association of plants with arbuscular mycorrhizal fungi that help the plant with the uptake of nutrients from the soil. This shows that plants actively establish-through the exudation of strigolactones-mutualistic interactions with microbes to overcome inadequate nutrition. The signaling function of strigolactones could possibly extend to other microbial partners, but the effect of strigolactones on the global root and rhizosphere microbiome remains poorly understood. Therefore, we analyzed the bacterial and fungal microbial communities of 16 rice genotypes differing in their root strigolactone exudation. Using multivariate analyses, distinctive differences in the microbiome composition were uncovered depending on strigolactone exudation. Moreover, the results of regression modeling showed that structural differences in the exuded strigolactones affected different sets of microbes. In particular, orobanchol was linked to the relative abundance of Burkholderia-Caballeronia-Paraburkholderia and Acidobacteria that potentially solubilize phosphate, while 4-deoxyorobanchol was associated with the genera Dyella and Umbelopsis. With this research, we provide new insight into the role of strigolactones in the interplay between plants and microbes in the rhizosphere.

Keywords: bacterial communities; fungal communities; rhizosphere; rice; strigolactones.

Figure 1.

Strigolactone concentration in the roots of rice plants grown on forest soil. SLs—orobanchol (A), 4-deoxyorobanchol (4DO) (B) and methoxy-5-deoxystrigol isomer 1 (Me5DS1) (C)—were analyzed using liquid chromatography–mass spectrometry. Each dot represents a single sample and letters indicate significant differences of means between samples (corrected P < 0.05 for multiple testing, Dunn's test). (D) PCA of SLs. Each dot represents a sample point and the arrows represent the loadings of the SLs. n.d, not detected; GWD, Gangweondo; Bina, Binagimbing; Sonk, Sonkanoir; Bhas, Bhasmanik; SC, Shuang-Chiang.

Figure 2.

Diversity and composition of the rice rhizosphere and roots bacterial (A, CandE) and fungal (B, D and F) communities. (A and B) Shannon index. Each dot represents a sample point. Different letters indicate significant differences between samples (corrected P < 0.05 for multiple testing, Dunn's test). (C and D) Principal coordinate ordination based on Bray–Curtis distance. Each dot represents a sample point. (E and F) Microbial composition at phylum level. Ag, agricultural soil; Fo, forest soil; BK, bulk soil; RS, rhizosphere; RT, root.

Figure 3.

Glomeromycota in the rhizosphere and roots of rice grown on two natural soils. (A) Relative abundance of Glomeromycota. Each dot represents a sample point. Different letters indicate significant differences between samples (corrected P < 0.05 for multiple testing, Dunn's test). (B) Composition of orders belonging to the Glomeromycota. Significant correlation between the plant total fresh biomass and the relative abundance of Glomeromycota orders in (C) the rhizosphere and (D and E) the roots. All correlation studies were performed using linear regression modeling (red line) as indicated by the P-value with a validation by permutation test. Each dot represents a sample point. Ag, agricultural soil; Fo, forest soil; BK, bulk soil; RS, rhizosphere; RT, root.

Figure 4.

Principal coordinate ordination based on Bray–Curtis distance constrained by the level of orobanchol in rice grown on forest soil. (AandB) Bacterial community. (CandD) Fungal community. (A and C) Rhizosphere. (B and D) Roots. Arrows present ASVs having high species score extracted from first axis of CAP1. The models were validated using an ANOVA-like permutation test (1000 permutations) as indicated by the P-value. Each dot represents individual sample points and colors represent amount of orobanchol.

Figure 5.

Correlation between the level of SLs and the relative abundance of ASVs/genera in the rhizosphere and roots of rice grown on forest soil. Venn diagram of bacterial and fungal ASVs positively (red label) and negatively (blue label) correlated with the level of SLs (A) in the rhizosphere and (B) in the roots. Family and genus belonging to AMF (Archaeosporales and Acaulospora) and bacterial genera (BCP and Granulicella) positively correlated with the level of orobanchol (C) in the rhizosphere and (D) in the roots. All correlation studies were performed using negative binomial generalized linear modeling (red line) as indicated by the P-value with a validation by permutation test (1000). Each dot represents a sample point. 4DO, 4-deoxyorobanchol; MeO5DS, methoxy-5-deoxystrigol isomer 1; BCP, Burkholderia–Caballeronia–Paraburkholderia.