Molecular Phylogenies of Plants and Frankia Support Multiple Origins of Actinorhizal Symbioses

doi:10.1006/mpev.1999.0692

Molecular Phylogenetics and Evolution

Volume 13, Issue 3, December 1999, Pages 493-503

https://doi.org/10.1006/mpev.1999.0692 Get rights and content

Abstract

Molecular phylogenetic trees were reconstructed from nucleotide sequences of nifH and 16S rDNA for Frankia and of rbcL for actinorhizal plants. Comparison of Frankia phylogenetic trees reconstructed using nifH and 16S rDNA sequences indicated that subgroupings of both trees correspond with each other in terms of plant origins of Frankia strains. The results suggested that 16S rDNAs can be utilized for coevolution analysis of actinorhizal symbioses. Frankia and plant phylogenetic trees reconstructed using 16S rDNA and rbcL sequences were compared. The comparison by tree matching and likelihood ratio tests indicated that although branching orders of both trees do not strictly correspond with each other, subgroupings of Frankia and their host plants correspond with each other in terms of symbiotic partnership. Estimated divergence times among Frankia and plant clades indicated that Frankia clades diverged more recently than plant clades. Taken together, actinorhizal symbioses originated more than three times after the four plant clades diverged.

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The first hypothesis has been almost universally dismissed, whereas the latter is widely accepted on the basis of two main arguments [14–24]. First, it comprises scenarios that require fewer evolutionary events and that are supported by phylogenetic ancestral state reconstruction studies [14–16,20,22]. Second, there is considerable variation among nodulating lineages in the type of microsymbiont, nodule ontogeny, and physiology [25–28].
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This group is likely to be the most ancient branching in Frankia’s evolutionary history and could have diverged 263–285 Myr bp, long before actinorhizal plants appearance in the fossil records [25] dated between 70 Myr [115] and 100 Myr [127]. The broad host range – encompassing four phylogenetically distant families [57,116] – of Cluster 2 strains could be a remnant of a symbiotic ancestor common to present-day lineages [117]. On the opposite, Clusters 1 and 3 comprise the most recently evolved groups of strains.
Diazotrophic Actinobacteria of the genus Frankia represent a challenge to classical bacterial taxonomy as they include many unculturable strains. As a consequence, we still have a poor understanding of their diversity, evolution and biogeography. In this study, a Multi-Locus Sequence Analysis (MLSA) using atpD, dnaA, ftsZ, pgk, and rpoB loci was done on a large set of cultured and uncultured strains, compared to 16S rRNA and correlated to Average Nucleotide Identity (ANI) from available Frankia genomes. MLSA provided a robust resolution of Frankia genus phylogeny and clarified the status of unresolved species and complex of species.
The robustness of single-gene topologies and their congruence with the MLSA tree were tested. Lateral Gene Transfers (LGT) were few and scattered, suggesting they had no impact on the concatenate topology. The pgk marker – providing the longest sequence, highest mean genetic divergence and least occurrence of LGT – was used to survey an unequalled number of Alnus-infective Frankia — mainly uncultured strains from a broad range of host-species and geographic origins. This marker allowed reliable Single-Locus Strain Typing (SLST) below the species level, revealed an undiscovered taxonomical diversity, and highlighted the effect of cultivation, sporulation phenotype and host plant species on symbiont richness, diversity and phylogeny.
Typing of nitrogen-fixing Frankia strains by matrix-assisted laser desorption ionization-time-of-flight (MALDI-TOF) mass spectrometry
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Citation Excerpt :
The first sub-group represents strains of the Alnus host infection group, including Casuarina-infective strains, the second sub-group represents yet uncultured endophytes in nodules of Dryas, Coriaria, and Datisca species, the third sub-group represents strains of the Elaeagnus host infection group and the last sub-group represents atypical, non-nitrogen-fixing strains [53]. While atypical, non-nitrogen fixing isolates are generally neglected in phylogenetic studies on the genus Frankia, the first three subgroups, also referred to as clusters 1–3 [12], have widely been confirmed by additional sequence analyses of 16S rRNA gene fragments [11,13,14] or of recA [40], glnA, glnII [12,16] or nifH gene fragments [15,33,45,61], suggesting genotypic classification reflecting physiological differences, i.e., phenotypic traits within the genus Frankia. The differentiation into these three DNA-sequence type groups is further confirmed by DNA–DNA relatedness of pure cultures that differentiate Frankia strains from different host infection groups.
Matrix-assisted laser desorption ionization-time-of-flight (MALDI-TOF) mass spectrometry (MS) was evaluated as a technique to characterize strains of the nitrogen-fixing actinomycete Frankia. MALDI-TOF MS reliably distinguished 37 isolates within the genus Frankia and assigned them to their respective host infection groups, i.e., the Alnus/Casuarina and the Elaeagnus host infection groups. The assignment of individual strains to sub-groups within the respective host infection groups was consistent with classification based on comparative sequence analysis of nifH gene fragments, confirming the usefulness of MALDI-TOF MS as a rapid and reliable tool for the characterization of Frankia strains.
Diversity of frankiae in root nodules of Morella pensylvanica grown in soils from five continents
2009, Systematic and Applied Microbiology
Bioassays with Morella pensylvanica as capture plant and comparative sequence analyses of nifH gene fragments of Frankia populations in nodules formed were used to investigate the diversity of Frankia in soils over a broad geographic range, i.e., from sites in five continents (Africa, Europe, Asia, North America, and South America). Phylogenetic analyses of 522-bp nifH gene fragments of 100 uncultured frankiae from root nodules of M. pensylvanica and of 58 Frankia strains resulted in a clear differentiation between frankiae of the Elaeagnus and the Alnus host infection groups, with sequences from each group found in all soils and the assignment of all sequences to four and five clusters within these groups, respectively. All clusters were formed or dominated by frankiae obtained from one or two soils with single sequences occasionally present from frankiae of other soils. Variation within a cluster was generally low for sequences representing frankiae in nodules induced by the same soil, but large between sequences of frankiae originating from different soils. Three clusters, one within the Elaeagnus and two within the Alnus host infection groups, were represented entirely by uncultured frankiae with no sequences from cultured relatives available. These results demonstrate large differences in nodule-forming frankiae in five soils from a broad geographic range, but low diversity of nodule-forming Frankia populations within any of these soils.
Plant Symbioses with Frankia and Cyanobacteria
2007, Biology of the Nitrogen Cycle
In addition to rhizobia, two other groups of prokaryotes enter N₂-fixing symbioses with plants. This chapter discusses plant symbioses with Frankia and Cyanobacteria. Actinorhizal nodules are formed in symbioses between the members of the actinomycetous eubacterial genus Frankia and the roots of more than 200 dicotyledonous plant species belonging to 24 genera from eight plant families. In planta, the shape, septation, and subcellular localization of Frankia vesicles are determined by the host plant, which therefore, can direct bacterial differentiation. Frankia can also form multilocular sporangia. The members of the Fabales are colonized intracellularly, whereas the members of the other plant groups are colonized intercellularly. Cyanobacterial symbioses covers the general distribution of cyanobacterial symbioses, the plant organs, the cyanobionts, evolutionary aspects, the colonization units— -hormogonia, signals, the colonization process, and adaptations and exchange of metabolites. A recent study implies that the organ colonized in Gunnera (stem glands) only develops under combined N deprivation. The largest variation in cyanobionts is found in lichens, ranging in morphology from unicellular to more complex filamentous forms. The vital role of hormogonia in the colonization process has also been demonstrated in reconstitution experiments. The importance of hormogonia in symbiosis is also manifested in their chemotactic behavior. The colonization of plants by cyanobacteria has been intensively studied in the Gunnera symbiosis. The host's control of cyanbiont proliferation is supported by the observation that the relative proportion of cyanobacterial biomass compared to plant biomass in symbiotic organs always remains relatively small.
Genetic diversity among Elaeagnus compatible Frankia strains and sympatric-related nitrogen-fixing actinobacteria revealed by nifH sequence analysis
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Elaeagnus compatible Frankia isolates from Tunisian soil have been previously clustered with Frankia, colonizing Elaeagnaceae and Rhamnaceae in two different phylogenetic subgroups, while strain BMG5.6 was described as a new lineage closely related to Frankia and Micromonospora genera. In this study we further assess the diversity of captured Frankia and the relationship with BMG5.6-like actinobacteria, by using nifH gene sequences. Using PCR-RFLP screening on DNA extracted from lobe nodules, additional microsymbionts sharing BMG5.6 features have been detected proving a widespread occurrence of these actinobacteria in Elaeagnus root nodules. Neighbour-Joining trees of Frankia nifH sequences were consistent with previously published 16S rRNA and GlnII phylogenetic trees. Although four main clades could be discerned, actinobacterial strain BMG5.6 was clustered with Frankia strains isolated from Elaeagnus. The present study underscored the emanation of new diazotrophic taxon isolated from actinorhizal nodules occupying intermediate taxonomic position between Frankia and Micromonospora. Moreover, its aberrant position in nifH phylogeny should open network investigations on the natural history of nitrogen-fixing gene among actinobacteria.

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Regular ArticleMolecular Phylogenies of Plants and Frankia Support Multiple Origins of Actinorhizal Symbioses

Abstract

Cladistics

Trends Ecol. Evol.

Functional constraints and rbcL evidence for land plant phylogeny

Ann. Mo. Bot. Gard.

Relationships among pure cultured strains of Frankia based on host-specificity

Physiol. Plant.

Amplification of 16S rRNA genes from Frankia strains in root nodules of Ceanothus griseus, Coriaria arborea, Coriaria plumosa, Discaria toumatou, and Purshia tridentata

Appl. Environ. Microbiol.

The genetics of actinorhizal Betulaceae

Phylogenies from molecular sequences: Inference and reliability

Annu. Rev. Genet.

Cospeciation in host–parasite assemblages: Comparative analysis of rates of evolution and timing of cospeciation

Syst. Zool.

Disparate rates of molecular evolution in cospeciating hosts and parasites

Science

Molecular phylogenies and host–parasite cospeciation: Gophers and lice as a model system

Phil. Trans. R. Soc. Lond. B

The probabilities of rooted tree-shapes generated by random bifurcation

Adv. Appl. Prob.

Statistical tests of host–parasite cospeciation

Evolution

Phylogenetic methods come of age: Testing hypotheses in an evolutionary context

Science

Molecular phylogeny of the genus Ceanothus using ndhF and rbcL sequences

Theor. Appl. Genet.

A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences

J. Mol. Evol.

Advances in the taxonomy of Frankia: Recognition of species alni and eleagni and novel subspecies pommerii and vandijkii

Fundamentals of Molecular Evolution

Molecular phylogeny of the actinorhizal Hamamelidae and relationship with host promiscuity towards Frankia

Mol. Ecol.

A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts

Proc. R. Soc. Lond. B Biol. Sci.

Regular Article
Molecular Phylogenies of Plants and Frankia Support Multiple Origins of Actinorhizal Symbioses