The role of biotic interactions in determining metal hyperaccumulation in plants

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Dokumentart: PhDThesis
Date: 2020-02-04
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Biologie
Advisor: Gruntman, Michal (Dr.)
Day of Oral Examination: 2019-07-23
DDC Classifikation: 570 - Life sciences; biology
580 - Plants (Botany)
Keywords: Schwermetall , Pflanzenökologie
Other Keywords:
heavy metal
plant ecology
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Heavy metal hyperaccumulation is a rare trait found in few plant species that inhabit metal contaminated soils. Two non-mutually exclusive hypotheses were proposed to explain the adaptive value of metal hyperaccumulation in plants: the elemental defense hypothesis suggests that metal hyperaccumulation functions as defense against herbivores, while the elemental allelopathy hypothesis suggests that metal hyperaccumulation acts to inhibit the growth of neighbors. In my doctoral research, I studied the role of these two biotic interactions, herbivory and competition, in selecting for metal hyperaccumulation and in its induction. My thesis comprises of the three experimental chapters that aimed to study these questions in the model hyperaccumulating species Arabidopsis halleri. The first study of my thesis (chapter 2) was the first study to compare the predictions of both the elemental defense and elemental allelopathy hypotheses. These predictions were compared between populations from both metalliferous and non-metalliferous soils of A. halleri. A. halleri plants were grown in soils with metals (such as, cadmium (Cd) and zinc (Zn)) or without metal and their leaves were used to examine the elemental defense hypothesis in a feeding experiment with a specialist herbivore. Leaves from the same plants were then used to examine the elemental allelopathy hypothesis in a set of leaf-leachate experiments that tested their effect on seed germination and seedling establishment of species co-occurring with A. halleri. The feeding experiment and field-survey results suggest that Cd accumulation in A. halleri leaves could provide it with defense against herbivores. Moreover, results of the leaf-leachate experiments reveal that Cd accumulation had no effects on seed germination of neighboring species but inhibited seedling establishment, particularly of neighboring plant species originating from non-metalliferous soils. These results suggest, for the first time, that both the need for herbivore defense and neighbor inhibition could jointly select for metal hyperaccumulation in plants. Moreover, they offer first evidence that metal hyperaccumulation could provide a selective advantage particularly in non-metalliferous soils, where neighboring plants probably lack metal tolerance. The second and third studies of my thesis (chapters 3, 4) aimed to explore the unstudied hypothesis that herbivory and competition might induce the uptake and foraging for heavy metals in A. halleri. Plants can exhibit foraging behaviors in response to resource heterogeneity and demand. However, biotic stressors might also affect these foraging decisions, such as herbivory and competition, which could alter the demand for particular resources, for example those required for herbivore resistance and competitive offense i.e. allelopathy. To study this hypothesis, I first examined the effect of simulated herbivory on clonal foraging and metal uptake in A. halleri (chapter 3). In this experiment, two connected ramets were grown in either a high-metal or a low-metal pot. Herbivory was simulated using jasmonic acid and pierced holes with water as a control. Secondly, I examined the effect of simulated competition on root foraging and uptake of heavy metals in A. halleri (chapter 4). In this experiment, A. halleri plants originating from both metalliferous and non-metalliferous soils were grown in a “split-root” setup with one root in a high-metal pot and the other in a low-metal one. The plants were then assigned to either simulated light competition or control no-competition treatments, using vertical green or clear plastic filters, respectively. The results of the first experiment (chapter 3) revealed that herbivory can induce both metal hyperaccumulation and sharing among ramets, particularly in ramets originating from populations of non-metalliferous soils. This result therefore suggests, for the first time, that clonal foraging for metal in plants can be induced by herbivory. In contrast, in the second experiment (chapter 4) simulated competition did not induce greater root allocation into the high-metal pots, regardless of A. halleri’s origin. However, simulated light competition did result in enhanced metal uptake by A. halleri, particularly in the less metal-tolerant plants originating from non-metalliferous soils. This result therefore suggests, for the first time, that metal uptake in plants can be induced by competition. Together, the results of both experiments open a novel facet in the study of decision-making in plants, implying that their foraging and nutrient uptake decisions can be a complex process in which not only resource distribution is evaluated but also its relative demand and alteration by environmental stressors. Interestingly, this induced uptake was displayed only for Cd and not Zn, in the case of herbivory, while for competition this induced uptake was displayed for Zn and not Cd, demonstrating separate uptake pathways and preferential resource selection, which is influenced by these biotic stressors. These results therefore highlight a new research avenue of prey selection in plants.

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