Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants

Abstract

Microorganisms and their hosts communicate with each other through an array of signals. The plant hormone auxin (indole-3-acetic acid; IAA) is central in many aspects of plant development. Cyclodipeptides and their derivative diketopiperazines (DKPs) constitute a large class of small molecules synthesized by microorganisms with diverse and noteworthy activities. Here, we present genetic, chemical, and plant-growth data showing that in Pseudomonas aeruginosa, the LasI quorum-sensing (QS) system controls the production of three DKPs-namely, cyclo(L-Pro-L-Val), cyclo(L-Pro-L-Phe), and cyclo(L-Pro-L-Tyr)-that are involved in plant growth promotion by this bacterium. Analysis of all three bacterial DKPs in Arabidopsis thaliana seedlings provided detailed information indicative of an auxin-like activity, based on their efficacy at modulating root architecture, activation of auxin-regulated gene expression, and response of auxin-signaling mutants tir1, tir1 afb2 afb3, arf7, arf19, and arf7arf19. The observation that QS-regulated bacterial production of DKPs modulates auxin signaling and plant growth promotion establishes an important function for DKPs mediating prokaryote/eukaryote transkingdom signaling.

Inhibition of biofilm in Bacillus amyloliquefaciens Q-426 by diketopiperazines

“…It was suggested that L-cyclo(Pro-Phe) and L-cyclo(Pro-Leu) produced by A. faecalis played a probable role in spongebacterial interaction (Li et al 2008). The observation that QS-regulated bacterial production of DKPs modulates auxin signaling and plant growth promotion established an important function for DKPs mediating prokaryote/ eukaryote transkingdom signaling (Ortiz-Castro et al 2011). The roles of DKPs played in QS offered an alternative approach to activate or antagonize the QS-mediated biological activities, such as biofilm formation.…”

Gut and Root Microbiota Commonalities

“…In plants, root genes induced by rhizospheric bacteria are involved in oxidative and defense responses, in plant secondary metabolism, or in signaling (140). Plants may detect bacterial cyclopeptides through auxin sensing pathways (147). In a more specialized symbiosis, a cascade of signaling processes occurs inside root cells in the presence of rhizobia or Nod factors (148).…”

Endophytic Streptomyces in the traditional medicinal plant Arnica montana L.: secondary metabolites and biological activity

“…Especially cyclo-prolyl-phenylalanyl is discussed recently to act as a signalling mimic of the plant hormone auxin (Ortiz-Castro et al 2011;Venturi and Fuqua 2013).…”

“…Cyclo-isoleucyl-prolyl and cyclo-prolyl-valyl were not present in the NIST11 database. Identification was done by comparison with published fragmentation patterns (Bitzer 2005;Wang et al 2010;Ortiz-Castro et al 2011). Only extract 3 contained all mentioned molecules and the respective strain was therefore chosen for genome sequencing.…”