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 plastids and bacteria from wild-collected samples, we show phylogenetic patterns consistent with a dominant vertical mode of transmission of the symbionts. Unique so far among leaf nodule symbioses, the bacteria can be cultured and are amenable to comparative transcriptomics, revealing a potential role in complementing the host’s arsenal of secondary metabolites. We propose a recent establishment of a vertical mode of transmission in this symbiosis which, together with a large effective population size explains the cultivability and apparent 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 candidate mechanisms enabling a permanent association in the phyllosphere.
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Acknowledgements
We wish to thank Dr. Olivier Leroux (Ghent University) for his help with microscopy. This work was supported by the Flemish Fonds Wetenschappelijk Onderzoek under grant G017717N and the Special Research fund of Ghent University under grant BOF17/STA/024. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the Oxford Genomics Centre at the Wellcome Centre for Human Genetics (funded by Wellcome Trust grant reference 203141/Z/16/Z) for the generation and initial processing of the sequencing data. Finally, We thank three anonymous reviewers for constructive comments which substantially improved the manuscript.
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A.C. designed the research, F.D.M. performed the molecular biology experiments, including isolation of DNA and RNA, and phenotyping experiments. B.D. performed the genome assemblies and annotation, metagenome mining and phylogenetic analyses. T.A. provided microscopy images and microbiological data. R.R., M.T.R., and V.J. identified and collected field samples. F.D.M, B.D., and A.C. analyzed and interpreted the data; F.D.M, B.D., T.A., and A.C. wrote the manuscript.
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De Meyer, F., Danneels, B., Acar, T. et al. Adaptations and evolution of a heritable leaf nodule symbiosis between Dioscorea sansibarensis and Orrella dioscoreae. ISME J 13, 1831–1844 (2019). https://doi.org/10.1038/s41396-019-0398-8
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DOI: https://doi.org/10.1038/s41396-019-0398-8
