Abstract
Bacterial leaf symbiosis is a unique and intimate interaction between bacteria and flowering plants, in which endosymbionts are organized in specialized leaf structures. Previously, bacterial leaf symbiosis has been described as a cyclic and obligate interaction in which the endosymbionts are vertically transmitted between plant generations and lack autonomous growth. Theoretically this allows for co-speciation between leaf nodulated plants and their endosymbionts. We sequenced the nodulated Burkholderia endosymbionts of 54 plant species from known leaf nodulated angiosperm genera, i.e. Ardisia, Pavetta, Psychotria and Sericanthe. Phylogenetic reconstruction of bacterial leaf symbionts and closely related free-living bacteria indicates the occurrence of multiple horizontal transfers of bacteria from the environment to leaf nodulated plant species. This rejects the hypothesis of a long co-speciation process between the bacterial endosymbionts and their host plants. Our results indicate a recent evolutionary process towards a stable and host specific interaction confirming the proposed maternal transmission mode of the endosymbionts through the seeds. Divergence estimates provide evidence for a relatively recent origin of bacterial leaf symbiosis, dating back to the Miocene (5–23 Mya). This geological epoch was characterized by cool and arid conditions, which may have triggered the origin of bacterial leaf symbiosis.
Highlights
A remarkable diversity of prokaryote-eukaryote symbioses has been described across many taxa and the degree of interaction can vary from loose and temporary associations to highly specific and permanent assemblages [1]
Endosymbiont phylogeny From endosymbionts of 14 nodulated Pavetta species, 35 nodulated Psychotria species, 2 nodulated Sericanthe species and 3 nodulated Ardisia species, 16S rRNA, recA and gyrB sequence data were obtained and subjected to molecular phylogenetic analyses together with sequences of non-nodulating Burkholderia representatives
The nodulated Psychotria endosymbionts form a monophyletic group (100% BPP/46% BS) with exception of the Psychotria kirkii endosymbionts. The latter are placed in two different phylogenetic positions: the endosymbionts of seven Psychotria kirkii specimens are related with the Pavetta endosymbionts (100% BPP/97% BS), while two Psychotria kirkii endosymbionts are sister to the endosymbionts of Sericanthe petitii (100% BPP/ 100% BS)
Summary
A remarkable diversity of prokaryote-eukaryote symbioses has been described across many taxa and the degree of interaction can vary from loose and temporary associations to highly specific and permanent assemblages [1]. Specific microbial endosymbioses have evolved independently many times in insects [2,3], sponges [4], nematodes [5] and deep-sea clams [6]. These interactions are considered as obligate because neither the host nor the endosymbiont can survive outside the symbiotic interaction. Mutualistic interactions with obligate and vertically inherited symbionts have not been reported so far, except for the Nostoc-Azolla association [10,11,12] and the bacterial leaf symbiosis [13]. The latter association received little attention but is certainly the most intimate association known between bacteria and higher plants with leaf nodules or galls as a visible morphological aspect of the symbiosis [13]
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