Edaphic factors and rhizobia influence the distribution of legumes (Fabaceae) in the Core Cape Subregion of South Africa

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2018

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University of Cape Town

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Fabaceae is the second most speciose plant family in the Core Cape Subregion (CCR) of South Africa, a Mediterranean type ecosystem, with mostly nutrient-poor soils. A majority of the legumes occurring in this region belong to the predominantly nitrogen-fixing subfamily Papilionoideae and they employ a variety of strategies for nutrient acquisition. However, legumes are neither uniformly nor randomly distributed in the CCR landscape. Instead, distinct legume species assemblages tend to occupy particular habitats within the landscape. The drivers of this distribution pattern are yet to be determined. In this thesis, it was hypothesized that edaphic factors (soil chemical and physical characteristics) and the distribution of rhizobia have influenced legume distributions in the CCR landscape. The influence of edaphic factors on the distribution of legume species assemblages in the Cape Peninsula (a microcosm of the CCR) is the subject of the second chapter of the thesis. It was hypothesized that the composition of legume species assemblages is correlated with soil physical and chemical properties and that the interaction of Phosphorus (P) and the three cations that often bind P, i.e. Aluminium, Calcium and Iron, making it unavailable to plants, drive legume species assemblages in the landscape. Soils from 27 legume sites, spanning all major soil types of the Cape Peninsula, were analysed for 31 chemical and physical properties. Surveys of legume species present at each site were conducted to generate a presence/absence matrix. Canonical correspondence analysis was used to test for a correlation between legume species composition and edaphic factors. The strength of the association between legume species composition and site groupings based on edaphic properties was assessed using indicator species analysis. A significant correlation between edaphic factors and species composition was found and the key edaphic parameters driving the relationship were clay content, iron (Fe), potassium (K), sulphur (S) and zinc (Zn). Indicator species, characteristic of the various edaphic habitats were also identified. These findings indicate that distinct edaphic habitats are occupied by discrete legume species assemblages, implying a significant influence of edaphic factors on the legume distributions. Chapter three of the thesis sought to determine if the ecological parameters; altitude, pH and soil type influence the distribution of the two main rhizobial genera (Burkholderia and Mesorhizobium) that nodulate various legumes of the CCR, and to determine the diversity and phylogenetic position of rhizobia that associate with the narrowly distributed and rare Indigofera superba in the CCR. The first objective was pursued through molecular characterisation of rhizobial strains isolated from nodules of legume species collected in the field across the Cape Peninsula. DNA sequences for 16S rRNA, recA and nodA were combined with data from a previous study that sampled broadly within the CCR and phylogenetic analyses were conducted. Tests for phylogenetic signals for the three ecological parameters were conducted, using the D statistic for soil type and Pagel’s λ for altitude and pH. These analyses were used to test the hypothesis that closely related species occupy similar habitats with respect to each of the three ecological parameters. For the study of rhizobial symbionts of Indigofera superba, field nodules were sampled from multiple populations across its distribution range and a phylogeny of its symbionts was reconstructed in a matrix that included symbionts of diverse legumes from different habitats within the CCR. The results showed that Burkholderia is restricted to acidic habitats, while Mesorhizobium occurs in both acidic and alkaline habitats. Additionally, both rhizobial genera showed significant phylogenetic clustering for pH and most soil types. However, none of the genera showed a phylogenetic structure with respect to altitude. These findings indicate that pH and soil type influence the distribution of rhizobia in the CCR. Implications of these findings for the distribution of legumes in the landscape are discussed. For the narrowly distributed I. superba, the results showed that it associates with diverse strains within the genus Burkholderia and such strains are not phylogenetically distinct from strains isolated from localities outside its distribution range. These findings lead to the hypothesis that I. superba does not exhibit rhizobia specificity at the intrageneric level. Testing of this hypothesis through analysis of its nodulation capability on soils from outside its distribution range is recommended. The fourth chapter of the thesis determined the extent of horizontal gene transfer among rhizobial genera in the Core Cape Subregion (CCR) of South Africa and reconstructed the ancestral symbionts of the legumes. Phylogenies of two chromosomal genes (16S rRNA and recA) and one nodulation gene (nodA) of rhizobia, isolated from diverse legumes in the CCR, were reconstructed using Bayesian and Maximum Likelihood techniques. A cophylogenetic analysis was used to test for congruence between the chromosomal and the nodA phylogenies. Five genera of rhizobia (Bradyrhizobium, Burkholderia, Ensifer, Mesorhizobium and Rhizobium) were studied. A phylogeny of the legumes was reconstructed from matK and rbcL DNA sequences and it was used to reconstruct their ancestral rhizobia, using Bayesian methods. The chromosomal phylogeny of the rhizobia was mostly incongruent with that of nodA, indicating potential horizontal inheritance of the latter. The nodA genes of Burkholderia, Mesorhizobium and Rhizobium had different evolutionary histories from their counterparts in other parts of the globe. Burkholderia was reconstructed as the ancestral symbionts of the CCR legumes. Evidence of co-diversification between the legumes and their symbionts was observed and this highlights a potential role of the legume-rhizobia interaction to the high diversity of legumes in the CCR. Finally, the availability of compatible rhizobia and their competitive ability are discussed as possible drivers for the lack of shared legumes between the CCR’s Fynbos biome and the Kwongan of Australia. Overall, the study shows that edaphic factors and biotic interactions (rhizobia) have significant influence on the distribution of legumes in the Cape Peninsula and the larger Core Cape Subregion of southern Africa. These findings are consistent with the theory that edaphic factors and biotic interactions have a strong influence on species distributions at local and site spatial scales.
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