Early steps in the evolution of vertical transmission revealed by a plant-bacterium symbiosis

Abstract

Various plant species establish intimate symbioses with bacteria within their aerial organs. The bacteria are contained within nodules or glands often present in distinctive patterns on the leaves in what is commonly referred to as leaf nodule symbiosis. We describe here a highly specific symbiosis between a wild yam species from Madagascar, Dioscorea sansibarensis and bacteria of the species Orrella dioscoreae. Using whole genome sequencing of plastid and bacteria from wild-collected samples, we show phylogenetic patterns consistent with a vertical transmission of the symbionts. Unique among leaf nodule symbioses, the bacteria can be cultured and are amenable to comparative transcriptomics and phenotypic characterization, revealing a potential role in complementing the hosts arsenal of secondary metabolites. We propose a very recent acquisition of the vertical mode of transmission in this symbiosis which, together with a large effective populations size explain the cultivability and remarkable lack of genome reductive evolution in O. dioscoreae. We leverage these unique features to reveal pathways and functions under positive selection in these specialized endophytes, highlighting the mechanisms enabling a permanent association in the phyllosphere.