Plant adaptation to metal polluted environments—Physiological, morphological, and evolutionary insights from Biscutella laevigata

Babst-Kostecka, Alicja; Waldmann, Patrik; Frérot, Hélène; Vollenweider, Pierre

doi:10.1016/j.envexpbot.2016.03.001

Cited by 38 publications

(21 citation statements)

References 70 publications

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“…If this is indeed the case, the overestimation of F ST would not change the conclusions from our Q ST – F ST comparison. Diversifying selection has already been suggested to play a role in the evolution of metal tolerance among M and NM populations in A. halleri (Meyer et al., ), Noccaea caerulescens (Jiménez‐Ambriz et al., ) and B. laevigata (Babst‐Kostecka et al., ) during adaptation to soil metal concentrations. Similarly, the significant difference among M and NM populations that we observed for Zn hyperaccumulation suggests that diversifying selection is due to opposite evolutionary trends in metal‐polluted and unpolluted habitats.…”

Section: Discussionmentioning

confidence: 98%

“…Yet, the demographic history of populations may also play a role (i.e., populations from specific phylogeographic units may show particular patterns; Gonneau et al, 2017). Thus, analyses of natural intraspecific variation in pseudometallophytes provide excellent opportunities to study the evolutionary dynamics of adaptive traits in plant species that occur in contrasted environments (Babst- Kostecka, Waldmann, Frérot, & Vollenweider, 2016;Linhart & Grant, 1996).…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: The case of zinc hyperaccumulation in Arabidopsis halleri

et al. 2018

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Metal hyperaccumulation in plants is an ecological trait whose biological significance remains debated, in particular because the selective pressures that govern its evolutionary dynamics are complex. One of the possible causes of quantitative variation in hyperaccumulation may be local adaptation to metalliferous soils. Here, we explored the population genetic structure of Arabidopsis halleri at fourteen metalliferous and nonmetalliferous sampling sites in southern Poland. The results were integrated with a quantitative assessment of variation in zinc hyperaccumulation to trace local adaptation. We identified a clear hierarchical structure with two distinct genetic groups at the upper level of clustering. Interestingly, these groups corresponded to different geographic subregions, rather than to ecological types (i.e., metallicolous vs. nonmetallicolous). Also, approximate Bayesian computation analyses suggested that the current distribution of A. halleri in southern Poland could be relictual as a result of habitat fragmentation caused by climatic shifts during the Holocene, rather than due to recent colonization of industrially polluted sites. In addition, we find evidence that some nonmetallicolous lowland populations may have actually derived from metallicolous populations. Meanwhile, the distribution of quantitative variation in zinc hyperaccumulation did separate metallicolous and nonmetallicolous accessions, indicating more recent adaptive evolution and diversifying selection between metalliferous and nonmetalliferous habitats. This suggests that zinc hyperaccumulation evolves both ways-towards higher levels at nonmetalliferous sites and lower levels at metalliferous sites. Our results open a new perspective on possible evolutionary relationships between A. halleri edaphic types that may inspire future genetic studies of quantitative variation in metal hyperaccumulation.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: The case of zinc hyperaccumulation in Arabidopsis halleri

et al. 2018

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“…The latter category includes a number of species that accumulate nickel from ultramafic soils as well as some widespread species that display ‘inadvertent uptake’ when growing on polluted soils (Pollard et al ., ). Examples are Biscutella laevigata with > 1% thallium (Babst‐Kostecka et al ., ), Pteris vittata with up to 2.3% arsenic (Ma et al ., ), and Phytolacca americana which can accumulate > 1% manganese (Xue et al ., ). A few species appear to show extreme variations in metal uptake, even when confined to metalliferous soils; this behaviour may be a reflection of widely varying metal availability caused by variations in pH or other soil properties, as for Pimelea leptospermoides in Australia (Reeves et al ., ).…”

Section: Hyperaccumulator Plants and The Need For A Databasementioning

confidence: 99%

A global database for plants that hyperaccumulate metal and metalloid trace elements

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“…Metalliferous (M) habitats exert a strong selection pressure on plant communities from high and potentially toxic concentrations of some trace metal elements (TMEs) in soils ( Thlaspi caerulescens 4 , Biscutella laevigata 5 ). Such high concentrations of TMEs can occur naturally, for example in rare serpentine soils 6 , or can result from anthropogenic activities (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Phenotypic studies on adaptation to calamine or serpentine soils using species that thrive on both M and NM soils, so called pseudometallophytes, have revealed considerable intraspecific variation in metal tolerance and hyperaccumulation 5 , 9 , 20 . At the species level, this large quantitative variation is commonly associated with different edaphic origins of populations.…”

Section: Introductionmentioning

confidence: 99%

Transmembrane transport and stress response genes play an important role in adaptation of Arabidopsis halleri to metalliferous soils

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Babst-Kostecka

Fischer

et al. 2018

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When plants adapt to local environments, strong signatures of selection are expected in the genome, particularly in high-stress environments such as trace metal element enriched (metalliferous) soils. Using Arabidopsis halleri, a model species for metal homeostasis and adaptation to extreme environments, we identifid genes, gene variants, and pathways that are associated with soil properties and may thus contribute to adaptation to high concentrations of trace metal elements. We analysed whole-genome Pool-seq data from two metallicolous (from metalliferous soils) and two non-metallicolous populations (in total 119 individuals) and associated allele frequencies of the identified single-nucleotide polymorphisms (SNPs) with soil variables measured on site. Additionally, we accounted for polygenic adaptation by searching for gene pathways showing enrichment of signatures of selection. Out of >2.5 million SNPs, we identified 57 SNPs in 19 genes that were significantly associated with soil variables and are members of three enriched pathways. At least three of these candidate genes and pathways are involved in transmembrane transport and/or associated with responses to various stresses such as oxidative stress. We conclude that both allocation and detoxification processes play a crucial role in A. halleri for coping with these unfavourable conditions.

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Plant adaptation to metal polluted environments—Physiological, morphological, and evolutionary insights from Biscutella laevigata

Cited by 38 publications

References 70 publications

Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: The case of zinc hyperaccumulation in Arabidopsis halleri

Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: The case of zinc hyperaccumulation in Arabidopsis halleri

A global database for plants that hyperaccumulate metal and metalloid trace elements

Transmembrane transport and stress response genes play an important role in adaptation of Arabidopsis halleri to metalliferous soils

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