Clonal integration and heavy-metal stress: responses of plants with contrasting evolutionary backgrounds

Gruntman, Michal; Anders, Clarissa; Mohiley, Anubhav; Laaser, Tanja; Clemens, Stephan; Höreth, Stephan; Tielbӧrger, Katja

doi:10.1007/s10682-016-9840-9

Cited by 12 publications

(15 citation statements)

References 42 publications

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“…All soils from the same habitats (metalliferous or non‐metalliferous) were mixed, sieved (2 mm mesh size) and steam‐sterilized for 2.5 hr at 80°C to destroy the seed bank and remove potential pathogens in the soil. Metal concentration analyses conducted in a parallel study (Gruntman et al, ) confirmed our assumption that Cd concentration was markedly greater for metalliferous soils compared to non‐metalliferous soils (3.04 vs. 0.71 µg/g dry soil, respectively). Therefore, these soils are hereafter referred to as high‐Cd or low‐Cd soils respectively.…”

Section: Methodssupporting

confidence: 77%

“…These differences could be attributed to different mechanisms of Cd sequestration that might be employed by these ecotypes. For example, in a previous study with A. halleri from the same populations, metalliferous populations had a higher Cd tolerance compared to non‐metalliferous populations (Gruntman et al, ), suggesting that Cd sequestration in the cells might be more efficient in metalliferous populations. Similarly, Meyer et al () found that in non‐metalliferous populations of A. halleri , drastic modifications of the shoot cell wall occur due to high‐Cd toxicity, and suggested that in these populations, Cd might not be sequestered in specific compartments such as vacuoles but stored in spaces outside the plasma membrane (apoplast; Isaure et al, ; Meyer et al, ).…”

Section: Discussionmentioning

confidence: 94%

“…After 2 weeks, they were transplanted into pots with either high-Cd or low-Cd soils to obtain contrasting Cd leaf concentra- After 6 months, six to eight leaves per plant were harvested and analysed for their Cd concentration. The leaf extracts were prepared with the same methodology described in Gruntman et al (2016) and analysed with ICP-OES technique for Cd quantification (Stein et al, 2016). The same plant individuals used in this experiment were also used in the following herbivore feeding experiment, seed germination experiments and seedling growth experiments.…”

Section: Accumulation Experimentsmentioning

confidence: 99%

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The role of biotic interactions in determining metal hyperaccumulation in plants

et al. 2020

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Heavy metal hyperaccumulation (MH) is a rare trait found in plant species that inhabit metal‐contaminated soils. Two main hypotheses proposed to explain the selective advantage of MH are the elemental defence hypothesis and elemental allelopathy hypothesis. The elemental defence hypothesis suggests that MH functions as defence against herbivores while the elemental allelopathy hypothesis suggests that MH acts to inhibit the growth of neighbours. Nevertheless, these hypotheses are not likely to be mutually exclusive. Here, we present the first study to test both hypotheses simultaneously. We examined these hypotheses with the Cd hyperaccumulator, Arabidopsis halleri, which inhabits both metalliferous and non‐metalliferous soils, thus providing an opportunity to test the hypotheses of both habitats. Arabidopsis halleri plants originating from several populations in both metalliferous and non‐metalliferous soils were grown in a greenhouse in soils with or without cadmium (Cd). Their leaves were used in a feeding experiment with a specialist herbivore and in a set of leaf‐leachate experiments that tested their effect on seed germination and seedling establishment of species co‐occurring with A. halleri. Finally, a field survey in several A. halleri populations was conducted to compare herbivore load between A. halleri and neighbours from metalliferous versus non‐metalliferous soils. Results of the feeding experiment and field survey suggest that Cd accumulation in A. halleri leaves could provide it with defence against herbivores. Results of the leaf‐leachate experiments reveal that Cd accumulation has no effect on seed germination of neighbouring species but inhibits seedling establishment, particularly of plant species originating from non‐metalliferous soils. Our results suggest that both herbivores and competing neighbours may jointly select for MH in plants. Moreover, MH could provide a selective advantage particularly in non‐metalliferous soils, where neighbouring plants lack metal tolerance. These results highlight the importance of including different origins and populations of both the target species and its neighbouring plant species when studying the ecological role of MH. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Methodssupporting

confidence: 77%

Section: Discussionmentioning

confidence: 94%

Section: Accumulation Experimentsmentioning

confidence: 99%

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The role of biotic interactions in determining metal hyperaccumulation in plants

et al. 2020

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“…ramets of the same genet). As well as risk spreading, multiple rosettes may be physiologically integrated through connections between them, to cope with the spatial heterogeneity of environments (Gruntman et al 2017). We expect that clonal propagation through aerial rosettes has evolved in response to habitat disturbance or habitat productivity.…”

Section: Life Historymentioning

confidence: 99%

Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation

Honjo

Kudoh

2019

AoB PLANTS

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Local adaptation is assumed to occur when populations differ in a phenotypic trait or a set of traits, and such variation has a genetic basis. Here, we introduce Arabidopsis halleri and its life history as a perennial model system to study population differentiation and local adaptation. Studies on altitudinal adaptation have been conducted in two regions: Mt. Ibuki in Japan and the European Alps. Several studies have demonstrated altitudinal adaptation in ultraviolet-B (UV-B) tolerance, leaf water repellency against spring frost and anti-herbivore defences. Studies on population differentiation in A. halleri have also focused on metal hyperaccumulation and tolerance to heavy metal contamination. In these study systems, genome scans to identify candidate genes under selection have been applied. Lastly, we briefly discuss how RNA-Seq can broaden phenotypic space and serve as a link to underlying mechanisms. In conclusion, A. halleri provides us with opportunities to study population differentiation and local adaptation, and relate these to the genetic systems underlying target functional traits.

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“…Currently, a large number of studies have documented effects of physiological integration on performance of clonal plants both in heterogeneous and in homogeneous environments (Alpert, 1991; Hartnett & Bazzaz, 1983; de Kroon et al., 1996; Lu et al., 2020; Song et al., 2013; Stuefer et al., 1994; Wang, Muller‐Scharer, et al, 2017; Zhang et al., 2016). For instance, in heterogeneous environments, clonal integration has been reported to improve growth of ramets suffering from various environmental stresses, including shading (Alpert, 1999; Stuefer et al., 1994), drought (Alpert, 1990; van Kleunen & Stuefer, 1999; de Kroon et al., 1996), nutrient deficiency (Alpert, 1991; D'Hertefeldt et al., 2011), sand burial (Chen et al., 2010; Yu et al., 2004), wind erosion (Yu et al., 2008), herbivory (Liu et al., 2009; Rodríguez et al., 2018), trampling (Xu et al., 2012), heavy metal contamination (Gruntman et al., 2017; Roiloa & Retuerto, 2012), high salinity (Salzman & Parker, 1985; Zhang et al., 2015) and submergence (Luo et al., 2014).…”

Section: Introductionmentioning

confidence: 99%

A meta‐analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments

Wang

et al. 2020

Functional Ecology

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Clonal plants play key roles in maintaining community productivity and stability in many ecosystems. Connected individuals (ramets) of clonal plants can translocate and share, for example, photosynthates, water and nutrients, and such physiological integration may affect performance of clonal plants both in heterogeneous and homogeneous environments. However, we still lack a general understanding of whether or how physiological integration in clonal plants differs across homogeneous versus heterogeneous environments. We compiled data from 198 peer‐reviewed scientific studies conducted in 19 countries with 108 clonal plant species from 35 families, and carried out a meta‐analysis of effects of physiological integration on 16 traits related to plant growth, morphology, physiology or allocation. Our analyses evaluated these relationships in (A) heterogeneous environments where at least one resource essential for plant growth (e.g. light, soil water and mineral nutrients) or non‐resource factor (e.g. grazing, trampling and burial) is spatially non‐uniformly distributed and (B) homogeneous environments where all these factors are spatially uniformly distributed. Physiological integration increased growth of whole clones in both homogeneous and heterogeneous environments due to its highly significant contribution to growth of recipient ramets. Integration did not affect growth of donor ramets in heterogeneous environments, but decreased it in homogeneous environments. Integration affected physiological traits of donor ramets in neither homogeneous nor heterogeneous environments. It did not affect any physiological traits of recipient ramets in homogeneous environments, but increased most of them in heterogeneous environments. For donor ramets, integration increased height by 53% and internode length by 37% in heterogeneous environments, but had no effect in homogeneous environments. For recipient ramets, integration increased height by 73% in homogeneous environments and by 115% in heterogeneous environments, and increased internode length by 35% only under heterogeneous environments. In heterogeneous environments, integration increased biomass allocation to roots of donor ramets under high water/nutrient conditions and decreased it under high light. Physiological integration plays a strong role in clonal plant physiology, morphology and growth, especially for recipient ramets in heterogeneous environments. Therefore, physiological integration may have contributed to the widespread of clonal plants in nature and their dominance in many ecosystems. It may also play important roles in invasion success of alien clonal plants and in maintaining functions and stability of ecosystems where clonal plants are abundant. A free Plain Language Summary can be found within the Supporting Information of this article.

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Clonal integration and heavy-metal stress: responses of plants with contrasting evolutionary backgrounds

Cited by 12 publications

References 42 publications

The role of biotic interactions in determining metal hyperaccumulation in plants

The role of biotic interactions in determining metal hyperaccumulation in plants

Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation

A meta‐analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments

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