The crane fly glycosylated triketide δ-lactone cornicinine elicits akinete differentiation of the cyanobiont in aquatic <i>Azolla</i> fern symbioses

E Güngör, J Savary, K Adema, LW Dijkhuizen, J Keilwagen, A Himmelbach, M Mascher, N Koppers, A Bräutigam, C Van Hove, O Riant, S Nierzwicki-Bauer, H Schluepmann

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The restriction of plant-symbiont dinitrogen fixation by an insect semiochemical had not been previously described. Here we report on a glycosylated triketide δ-lactone from Nephrotoma cornicina crane flies, cornicinine, that causes chlorosis in the floating-fern symbioses from the genus Azolla. Only the glycosylated trans-A form of chemically synthesized cornicinine was active: 500 nM cornicinine in the growth medium turned all cyanobacterial filaments from Nostoc azollae inside the host leaf-cavities into akinetes typically secreting CTB-bacteriocins. Cornicinine further inhibited akinete germination in Azolla sporelings, precluding re-establishment of the symbiosis during sexual reproduction. It did not impact development of the plant Arabidopsis thaliana or several free-living cyanobacteria from the genera Anabaena or Nostoc but affected the fern host without cyanobiont. Fern-host mRNA sequencing from isolated leaf cavities confirmed high NH4-assimilation and proanthocyanidin biosynthesis in this trichome-rich tissue. After cornicinine treatment, it revealed activation of Cullin-RING ubiquitin-ligase-pathways, known to mediate metabolite signaling and plant elicitation consistent with the chlorosis phenotype, and increased JA-oxidase, sulfate transport and exosome formation. The work begins to uncover molecular mechanisms of cyanobiont differentiation in a seed-free plant symbiosis important for wetland ecology or circular crop-production today, that once caused massive CO2 draw-down during the Eocene geological past.
Original languageEnglish
Pages (from-to)2675-2692
Number of pages18
JournalPlant Cell and Environment
Volume47
Issue number7
Early online date10 Apr 2024
DOIs
Publication statusE-pub ahead of print - 10 Apr 2024

Keywords

  • 2-oxoglutarate-dependent dioxygenase evolution
  • Azolla symbioses
  • N -fixation
  • Nephrotoma cornicina
  • Nostoc azollae
  • cyanobacteria cell differentiation
  • glycosylated triketide δ-lactone
  • jasmonic acid oxidase
  • plant elicitation

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