The association between Dioscorea sansibarensis and Orrella dioscoreae as a model for hereditary leaf symbiosis

PLoS One. 2024 Apr 22;19(4):e0302377. doi: 10.1371/journal.pone.0302377. eCollection 2024.

Abstract

Hereditary, or vertically-transmitted, symbioses affect a large number of animal species and some plants. The precise mechanisms underlying transmission of functions of these associations are often difficult to describe, due to the difficulty in separating the symbiotic partners. This is especially the case for plant-bacteria hereditary symbioses, which lack experimentally tractable model systems. Here, we demonstrate the potential of the leaf symbiosis between the wild yam Dioscorea sansibarensis and the bacterium Orrella dioscoreae (O. dioscoreae) as a model system for hereditary symbiosis. O. dioscoreae is easy to grow and genetically manipulate, which is unusual for hereditary symbionts. These properties allowed us to design an effective antimicrobial treatment to rid plants of bacteria and generate whole aposymbiotic plants, which can later be re-inoculated with bacterial cultures. Aposymbiotic plants did not differ morphologically from symbiotic plants and the leaf forerunner tip containing the symbiotic glands formed normally even in the absence of bacteria, but microscopic differences between symbiotic and aposymbiotic glands highlight the influence of bacteria on the development of trichomes and secretion of mucilage. This is to our knowledge the first leaf symbiosis where both host and symbiont can be grown separately and where the symbiont can be genetically altered and reintroduced to the host.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dioscorea* / genetics
  • Dioscorea* / microbiology
  • Plant Leaves* / microbiology
  • Symbiosis*

Grants and funding

This work was supported by the UGent Special Research Fund under grant BOFSTA2017002001 to AC. AC also acknowledges support from the French National Research Agency under grant agreement ANR-19-TERC-0004-01 and from the French Laboratory of Excellence project "TULIP" (ANR-10-LABX-41; ANR-11-IDEX-0002-02). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.