Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts

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.

Symbiotic organs: the nexus of host–microbe evolution

“…Chemical defense systems can also extend to protecting the host from predators and competitors. In leaf nodules of Bwanashupa shrubs (Psychotria kirkii), bacterial symbionts (Candidatus Burkholderia kirkii) provide the host with chemicals toxic to arthropods or that impede root elongation in competitors, preventing seed plants from growing near the host [42]. Although the symbiont has experienced significant genomic erosion associated with vertical transmission, it maintains two gene clusters not found in free-living Burkholderia, which are involved in the synthesis of these chemicals [43].…”

Cyclitol secondary metabolism is a central feature ofBurkholderialeaf symbionts

“…Ca . B. kirkii is likely involved in the synthesis of two cyclitol metabolites: kirkamide, a C 7 N aminocyclitol with insecticidal properties, and streptol glucoside, a derivative of valienol with broad allelopathic activities (Sieber et al , 2015; Georgiou et al , 2021). Similar gene clusters containing putative EEVS were also detected in the genomes of other Psychotria and a Pavetta leaf symbionts (Pinto-Carbó et al , 2016), further highlighting the importance of cyclitol compounds in these leaf symbioses.…”

Allylic Carbocyclic Inhibitors Covalently Bind Glycoside Hydrolases

“…1,16,17 Streptol/valienol 18,19 and kirkamide 20,21 (Figure 1A) are C 7 cyclitol natural products that have been identified 22,23 in an obligatory symbiosis system composed of the plant Psychotria kirkii and the bacterium Candidatus Burkholderia kirkii. These natural products have been shown to act as allelochemicals inhibiting plant (competitor) growth, 19,23,24 as insecticides, 20 and grazer deterrents. 18 An interesting compound is represented by streptol glucoside, which was isolated from the same bacteria/plant symbiosis.…”

“…(A) Streptol (Valienol) and kirkamide are allelopathic agents produced by plant-symbiotic bacteria for defense purposes. Streptol glucoside features a potential leaving group in the 4-position. − (B) Can the allylic C–O bond in streptol glucoside be cleaved? (C) Well-established mechanism for enzymatic carbohydrate hydrolysis at the anomeric position.…”

“…Streptol glucoside features a potential leaving group in the 4-position. 18 − 24 (B) Can the allylic C–O bond in streptol glucoside be cleaved? (C) Well-established mechanism for enzymatic carbohydrate hydrolysis at the anomeric position.…”