Evolutionary history can shape belowground ecological interactions in eucalypts
Creators: name: Senior, JK
Publisher: name: University Of Tasmania
Year: 2023

description: The influence of plant-microbial interactions on the structure and dynamics of native vegetation is gaining increasing attention. Plants may alter (i.e., 'condition') soil microbial communities with subsequent consequences for their performance via plant-soil feedbacks. Such feedbacks often vary in direction and magnitude among species and have been linked to the successional state, diversity and structure of temperate and tropical ecosystems. The drivers of variable conditioning and feedbacks are not clear, but recent studies suggest that plant evolutionary history may be a predictor of belowground ecological interactions. This thesis investigates whether plant evolutionary history can indeed explain plant-soil feedbacks using Tasmanian eucalypt species representing the subgenera, Eucalyptus and Symphyomyrtus, as well as the underlying genetic mechanisms. In chapter 2, seedlings of a species from each subgenus, E. globulus and E. obliqua, were examined for responses to native soil inoculum that were consistent with plant-soil feedback, and whether feedbacks could be modified by wild fire. Soils were collected from beneath mature E. globulus or E. obliqua trees within native forest stands that had or had not been burnt by a recent wildfire and were subsequently used to inoculate seedlings of both species in a glasshouse experiment. Eucalyptus globulus displayed responses consistent with a positive plant-soil feedback, where seedlings performed better when inoculated with E. globulus as opposed to E. obliqua soils. However, this effect was only present when seedlings were inoculated with soils collected from unburnt as opposed to burnt stands, suggesting that fire removed the positive effect of E. globulus inoculum. These findings indicated that eucalypt species, and possibly subgenera, may differ in plant-soil feedbacks and these feedbacks can be influenced by external factors. Chapter 3 tests whether feedbacks are a consequence of soil conditioning and whether there is a phylogenetic signal to these feedbacks. Seedlings of 14 Tasmanian eucalypt species from both subgenera were inoculated with soils conditioned by each of these species in a common garden. Conditioning and feedback effects were detected and shown to exhibit a significant phylogenetic signal. For each focal species, feedback was calculated as the slope of the linear regression of its relative response to each conditioned soil against its phylogenetic distance from the soil conditioning species. Species from subgenus Eucalyptus performed better when inoculated with soils conditioned by more distant relatives (i.e., negative plant-soil feedback), while species from subgenus Symphyomyrtus either showed neutral or small positive responses. These results argued that plant evolutionary history can shape soil conditioning and plant-soil feedbacks. In chapter 4, DNA was extracted from the same conditioned soils and sequenced to determine whether the eucalypt subgenera differentially conditioned soil microbes and whether conditioning was associated with phylogenetic signal in plant-soil feedbacks. Fungal community composition was found to differ between soils conditioned by each subgenus, indicating phylogenetic signal in the conditioning of fungal communities. Further, soils sampled from subgenus Eucalyptus species more frequently contained fungal taxa that exhibit pathogenic relationships with eucalypts. These taxa were associated with negative feedbacks to conditioned soils, presenting potential candidate organisms driving the negative responses of subgenus Eucalyptus to its own soils. Chapter 5 examines species differences in root chemistry as a potential mechanism for conditioning of the soil microbial community, and ultimately, phylogenetic signal in plant-soil feedbacks. The concentrations of total phenolics, condensed tannins, carbohydrates, terpenes and formylated phloroglucinol compounds in the roots significantly varied among 24 Tasmanian eucalypt species studied from both subgenera. There was significant phylogenetic signal to this variation, with subgenus Eucalyptus roots containing higher concentrations of only total phenolics, while subgenus Symphyomyrtus roots contained higher concentrations of all other groups of compounds, especially, terpenes and formylated phloroglucinol compounds. Integration of these results with those from chapters 3 and 4, showed statistically significant relationships of root compounds with microbial taxa that were associated with feedbacks as well as the feedbacks themselves. These findings suggested that susceptibility of subgenus Eucalyptus species to soil pathogens and thus, negative feedbacks, may ultimately be related to root chemical traits. This thesis contributes significantly to the field of plant-soil interactions. It provides further support for the use of evolutionary history as a predictor of plant ecological interactions. While plant-soil feedbacks have been associated with microbial conditioning and recent work has suggested that soil conditioning can display a phylogenetic signal, this thesis provides the first evidence of a phylogenetic signal in both microbial conditioning and feedback responses. Thus, closely related species can condition similar microbial communities and respond to conditioned communities similarly, highlighting a putative mechanism driving phylogenetic structure to plant communities. This work encourages the continued investigation of phylogenetic structure in plant-soil interactions and holds the potential to increase our understanding of the mechanisms structuring plant communities and vegetation dynamics.