Motility-Independent Vertical Transmission of Bacteria in Leaf Symbiosis

Hereditary symbioses have the potential to drive transgenerational effects, yet the mechanisms responsible for transmission of heritable plant symbionts are still poorly understood. The leaf symbiosis between Dioscorea sansibarensis and the bacterium Orrella dioscoreae offers an appealing model system to study how heritable bacteria are transmitted to the next generation. Here, we demonstrate that inoculation of apical buds with a bacterial suspension is sufficient to colonize newly formed leaves and propagules, and to ensure transmission to the next plant generation. Flagellar motility is not required for movement inside the plant but is important for the colonization of new hosts. Further, tissue-specific regulation of putative symbiotic functions highlights the presence of two distinct subpopulations of bacteria in the leaf gland and at the shoot meristem. We propose that bacteria in the leaf gland dedicate resources to symbiotic functions, while dividing bacteria in the shoot tip ensure successful colonization of meristematic tissue, glands, and propagules. Compartmentalization of intrahost populations together with tissue-specific regulation may serve as a robust mechanism for the maintenance of mutualism in leaf symbiosis.