Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts

Tatyana Grayfer,Jacob L Gorenflos López,Karl Gademann,Leo Eberl,Chien-Chi Hsiao,Simon Sieber,Aurélien Bailly,Antri Georgiou

doi:10.1038/s41598-021-01867-2

Abstract

After a century of investigations, the function of the obligate betaproteobacterial endosymbionts accommodated in leaf nodules of tropical Rubiaceae remained enigmatic. We report that the α-d-glucose analogue (+)-streptol, systemically supplied by mature Ca.Burkholderia kirkii nodules to their Psychotria hosts, exhibits potent and selective root growth inhibiting activity. We provide compelling evidence that (+)-streptol specifically affects meristematic root cells transitioning to anisotropic elongation by disrupting cell wall organization in a mechanism of action that is distinct from canonical cellulose biosynthesis inhibitors. We observed no inhibitory or cytotoxic effects on organisms other than seed plants, further suggesting (+)-streptol as a bona fide allelochemical. We propose that the suppression of growth of plant competitors is a major driver of the formation and maintenance of the Psychotria–Burkholderia association. In addition to potential agricultural applications as a herbicidal agent, (+)-streptol might also prove useful to dissect plant cell and organ growth processes.

Highlights

The leaves of discrete genera of Rubiaceae and Primulaceae host Burkholderia symbionts in their mesophyll and form stoma-derived structures, termed nodules, in a limited number of species[1,2,3]
Leachates obtained by bathing intact P. kirkii leaves in water contained sufficient inhibitory activity to prevent lettuce root establishment, but did not completely block germination, as embryo roots protruded from the seed coat and hypocotyls developed in treated and untreated seedlings (Supplementary Fig. 1c)
The ongoing adaptive role of the symbiosis is challenged by the recent placement of two non-nodulated Psychotria species within the nodulated clade[69] and the pseudogenization of cyclitol biosynthetic genes in several symbionts[10], indicating that cyclitol production is not the only contribution to the obligate character of the symbiotic association

Summary

Introduction

The leaves of discrete genera of Rubiaceae and Primulaceae host Burkholderia symbionts in their mesophyll and form stoma-derived structures, termed nodules, in a limited number of species[1,2,3]. PKIR01 orthologous genes are found in other Psychotria leaf nodule s ymbionts[10] Their conservation underlines their importance for the symbiosis. The plasmid pKIR01 encodes enzymes with significant homology to genes involved in the biosynthesis of C7 cyclitol-containing secondary metabolites in Actinobacteria[11]. Bioactivities of such compounds include glycosidase inhibition (acarbose), and antitumoral (pericosine A), antifungal (validamycin A), and insecticidal (validoxylamine A) p roperties[13,14]. The exclusive distribution and conservation of the cyclitol biosynthetic genes in leaf-nodule Burkholderia, supported by the presence of the compounds in host p lants[10], argues for positive selection of these traits and suggests a defensive symbiosis. This is the first report of a natural antagonist that targets root growth of seed plants

Methods

Results

Conclusion