Priming of rhizobial nodulation signaling in the mycosphere accelerates nodulation of legume hosts

Abstract

The simultaneous symbiosis of leguminous plants with two root mutualists, endophytic fungi and rhizobia is common in nature, yet how two mutualists interact and co-exist before infecting plants and the concomitant effects on nodulation are less understood.Using a combination of metabolic analysis, fungal deletion mutants and comparative transcriptomics, we demonstrated that Bradyrhizobium and a facultatively biotrophic fungus, Phomopsis liquidambaris, interacted to stimulate fungal flavonoid production, and thereby primed Bradyrhizobial nodulation signaling, enhancing Bradyrhizobial responses to root exudates and leading to early nodulation of peanut (Arachis hypogaea), and such effects were compromised when disturbing fungal flavonoid biosynthesis.Stress sensitivity assays and reactive oxygen species (ROS) determination revealed that flavonoid production acted as a strategy to alleviate hyphal oxidative stress during P. liquidambaris-Bradyrhizobial interactions. By investigating the interactions between P. liquidambaris and a collection of 38 rhizobacteria, from distinct bacterial genera, we additionally showed that the flavonoid-ROS module contributed to the maintenance of fungal and bacterial co-existence, and fungal niche colonization under soil conditions.Our results demonstrate for the first time that rhizobial nodulation signaling can be primed by fungi before symbiosis with host plants and highlight the importance of flavonoid in tripartite interactions between legumes, beneficial fungi and rhizobia.

Engineered Phomopsis liquidambaris with Fhb1 and Fhb7 Enhances Resistance to Fusarium graminearum in Wheat

“…P. liquidambaris as an endophyte and a carrier offered potential for plant growth, production, and biotic or abiotic stress as a natural biocontrol agent in our previous research, which is friendly to the environment of rice and peanut. 29,40 The inherent nature of endophytes to colonize in plants provides a novel approach as a delivery system between plants and microorganisms for various beneficial traits. 52 In fact, horizontal gene transfer is very common within bacteria, fungi, and virus but might be more complex in plants.…”

“…27,28 This organism grows rapidly in soil and forms a network of mycelia that help Bradyrhizobium quickly reach the root. 29 P. liquidambaris secretes flavonoid substances as a signal to improve the expression of nodulation-related genes in rhizobia and promote the advances of peanut nodulation. 29 Genetic manipulation via the CRISPR-Cas9 system and the refactor of the pathway by a DNA assembly in P. liquidambaris were performed.…”

“…29 P. liquidambaris secretes flavonoid substances as a signal to improve the expression of nodulation-related genes in rhizobia and promote the advances of peanut nodulation. 29 Genetic manipulation via the CRISPR-Cas9 system and the refactor of the pathway by a DNA assembly in P. liquidambaris were performed. 14,30−32 These studies laid a foundation for the study of interaction between P. liquidambaris and plants.…”

“…The fungus Phomopsis liquidambaris was isolated from Bischofia polycarpa, which could colonize rice and peanuts and promote the growth of host plants, decrease the peanut continuous cropping barrier, and enhance disease resistance for plants by increasing the lignin content, callose, and antioxidant enzyme activity and activating the salicylic acid-dependent pathway to alleviate the damage of Fusarium oxysporum to peanut under stress. − P. liquidambaris could alter the root exudate when it colonizes in peanut root by secreting organic acids and amino acids to promote rhizobium chemotaxis, growth, and biofilm formation. , This organism grows rapidly in soil and forms a network of mycelia that help Bradyrhizobium quickly reach the root P.…”

“…P. liquidambaris secretes flavonoid substances as a signal to improve the expression of nodulation-related genes in rhizobia and promote the advances of peanut nodulation . Genetic manipulation via the CRISPR-Cas9 system and the refactor of the pathway by a DNA assembly in P.…”