Bacterial leaf symbiosis in Ardisia (Myrsinoideae, Primulaceae): molecular evidence for host specificity

Lemaire, Benny; Smets, Erik; Dessein, Steven

doi:10.1016/j.resmic.2011.04.003

Cited by 30 publications

(28 citation statements)

References 25 publications

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“…The genus Ardisia is recovered as monophyletic group (BI 100%) and sister to the Myrsine - Rapanea clade (BI 97%). The interspecific relationships in Ardisia received weak support, but the monophyly of leaf nodulating species was strongly supported (BI 100%) as described previously [16], [36]. The divergence time estimations with credibility intervals obtained for the asterids, lamiids, campanulids, Ericales, Cornales, Ardisia and the origin of leaf nodulation in Ardisia are listed in Table 1.…”

Section: Resultssupporting

confidence: 66%

Bacterial Leaf Symbiosis in Angiosperms: Host Specificity without Co-Speciation

et al. 2011

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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.

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Section: Resultssupporting

confidence: 66%

Bacterial Leaf Symbiosis in Angiosperms: Host Specificity without Co-Speciation

et al. 2011

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“…To reveal the identity of these symbionts, Lemaire et al (2011b) used a molecular phylogenetic approach to investigate nodulated species of Ardisia and concluded that the symbionts belonged to Burkholderia. It is notable that Burkholderia was also suggested to be the leaf-nodule symbiont of Rubiaceae (Van Oevelen et al 2002Lemaire et al 2011cLemaire et al , 2011d, the other angiosperm family in which vertically transmitted bacterial symbionts occur (Lersten and Horner 1976;Miller 1990).…”

Section: Previous Isolation and Identification Attemptsmentioning

confidence: 99%

“…It is notable that Burkholderia was also suggested to be the leaf-nodule symbiont of Rubiaceae (Van Oevelen et al 2002Lemaire et al 2011cLemaire et al , 2011d, the other angiosperm family in which vertically transmitted bacterial symbionts occur (Lersten and Horner 1976;Miller 1990). Lemaire et al (2011b) further indicated that the nodulated taxa of Ardisia formed a monophyletic group and that the symbionts not only exhibited host specificity but also had a phylogeny mirroring that of the hosts. However, the Ardisia samples were all collected from cultivated plants in botanic gardens, and the origins of the plants of two nodulated taxa (A. crenata and A. mamillata) were unknown .…”

Section: Previous Isolation and Identification Attemptsmentioning

confidence: 99%

“…In addition, Ardisia is one of the largest genera in Myrsinaceae (Stå hl and Anderberg 2004), estimated to have over 400 species (Chen and Pipoly 1996), and at least 70 species have been assigned to Crispardisia, the subgenus characterized by leaf nodules, based on Mez (1902) and published literature on regional floras (Sleumer 1988;Stone 1989;Chen and Pipoly 1996;Larsen and Hu 1996;Hu and Vidal 2004). Because only three nodulated taxa and eight other Ardisia species were included in Lemaire et al (2011b), the evidence for the monophyly of the nodulated taxa is not strong enough. 94 …”

Section: Previous Isolation and Identification Attemptsmentioning

confidence: 99%

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Phylogenetic and Cophylogenetic Analyses of the Leaf-Nodule Symbiosis inArdisiaSubgenusCrispardisia(Myrsinaceae): Evidence from Nuclear and Chloroplast Markers and BacterialrrnOperons

2014

International Journal of Plant Sciences

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Editor: Elizabeth A. KelloggPremise of research. Leaf-nodule symbiosis represents an intriguing relationship between angiosperms and bacteria. In leaf-nodulated Ardisia (subgenus Crispardisia), it has been hypothesized that the bacterial symbionts, which are also observed in reproductive organs, are transmitted to the next generation in a vertical and closed manner. We tested this hypothesis by using molecular approaches to locate the symbionts within hosts and to conduct host-symbiont cophylogenetic analyses.Methodology. Universal primers were used to amplify bacterial rrn operon from field-collected Crispardisia for identification of symbionts and design of symbiont-specific primers for PCR detection. The relationships of symbionts from 11 Crispardisia taxa with 60 validly named species in the same genus were analyzed. The monophyly of the hosts was also explored by constructing a phylogeny of Ardisia based on nuclear ribosomal internal transcribed spacer (nrITS) and three chloroplast markers from 36 taxa belonging to nine subgenera. Host-symbiont cophylogenetic analyses were conducted using TreeMap and ParaFit.Pivotal results. Ribosomal RNA operons amplified from the rod-shaped Gram-negative symbionts of Crispardisia suggested they form a clade within Burkholderia. The host taxa were also resolved as a monophyletic group in the phylogenetic analyses based on nrITS, trnL-trnF, atpB-rbcL, and psbA-trnH. PCR detection confirmed the speculation based on electron microscope observation that the same symbiotic bacteria occur in both vegetative and reproductive organs. The similarity of rrn operon sequences of symbionts from hosts collected from different localities and the overall Crispardisia-Burkholderia cophylogenetic pattern suggest that the symbionts have been confined to the host's life cycle since the formation of such an intimate association.Conclusions. Overall, this study supports the hypothesis that Ardisia leaf-nodule symbionts are vertically transmitted and should be recognized as an integral part of Crispardisia.

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“…All attempts to cultivate the bacterial partner failed, suggesting that the endosymbionts are absolutely dependent on the host for growth and survival (9,16,24). Recent studies using culture-independent PCR methods revealed the identity of the endophytes of all leaf-nodulated plants as Burkholderia (10)(11)(12)24). More interestingly, it was also demonstrated that high host specificity occurs as a result of vertical symbiont transfer and that frequent host switches are observed, rejecting a long-term cospeciation (13).…”

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Endosymbiont Transmission Mode in Bacterial Leaf Nodulation as Revealed by a Population Genetic Study of Psychotria leptophylla

Lemaire

Janssens

Smets

et al. 2012

Appl Environ Microbiol

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Leaf-nodulated plants are colonized by vertically inherited bacterial endosymbionts, which maintain symbioses throughout host generations. The permanent character of the interaction implies phylogenetic congruence between the host and the endosymbiont. However, the present population genetic study of Psychotria leptophylla provides evidence for a mixed symbiont transmission involving both vertical inheritance and horizontal transfers from the environment.

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Bacterial leaf symbiosis in Ardisia (Myrsinoideae, Primulaceae): molecular evidence for host specificity

Cited by 30 publications

References 25 publications

Bacterial Leaf Symbiosis in Angiosperms: Host Specificity without Co-Speciation

Bacterial Leaf Symbiosis in Angiosperms: Host Specificity without Co-Speciation

Phylogenetic and Cophylogenetic Analyses of the Leaf-Nodule Symbiosis inArdisiaSubgenusCrispardisia(Myrsinaceae): Evidence from Nuclear and Chloroplast Markers and BacterialrrnOperons

Endosymbiont Transmission Mode in Bacterial Leaf Nodulation as Revealed by a Population Genetic Study of Psychotria leptophylla

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