Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex

Abstract

Metal hyperaccumulation is an uncommon but highly distinctive adaptation found in certain plants that can grow on metalliferous soils. Here we review what is known about evolution of metal hyperaccumulation in plants and describe a population-genetic analysis of the Alyssum serpyllifolium (Brassicaceae) species complex that includes populations of nickelhyperaccumulating as well as non-accumulating plants growing on serpentine (S) and non-serpentine (NS) soils, respectively. To test whether the S and NS populations belong to the same or separate closely related species, we analysed genetic variation within and between four S and four NS populations from across the Iberian peninsula. Based on microsatellites, genetic variation was similar in S and NS populations (average H o = 0.48). The populations were significantly differentiated from each other (overall F ST = 0.23), and the degree of differentiation between S and NS populations was similar to that within these two groups. However, high S versus NS differentiation was observed in DNA polymorphism of two genes putatively involved in adaptation to serpentine environments, IREG1 and NRAMP4, whereas no such differentiation was found in a gene (ASIL1) not expected to play a specific role in ecological adaptation in A. serpyllifolium. These results indicate that S and NS populations belong to the same species and that nickel hyperaccumulation in A. serpyllifolium appears to represent a case of adaptation to growth on serpentine soils. Further functional and evolutionary genetic work in this system has the potential to significantly advance our understanding of the evolution of metal hyperaccumulation in plants.

Comparative RNA‐seq analysis of nickel hyperaccumulating and non‐accumulating populations of Senecio coronatus (Asteraceae)

“…Three genes required for the maintenance of epigenetic silencing of gene expression, MOM1, STRS1 and ICU2 (Hyun et al, 2013;Khan et al, 2014;Han et al, 2016), as well as several chromatin remodellers and a histone deacetylase, also showed elevated expression levels in the hyperaccumulators (Table S6); this finding is line with the recent suggestion that chromatin compaction may increase genome stability in hyperaccumulators (Gull ı et al, 2018). (Merlot et al, 2014;Sobczyk et al, 2017). RNA-Seq provides the means by which to analyse gene expression in these species, but the choice of plant system is critical to extraction of the most biologically meaningful information (Halimaa et al, 2014a).…”

“…While most hyperaccumulator plants accumulate Ni, we understand relatively little about the molecular basis of this trait (Merlot et al ., ; Sobczyk et al ., ). RNA‐Seq provides the means by which to analyse gene expression in these species, but the choice of plant system is critical to extraction of the most biologically meaningful information (Halimaa et al ., ).…”

“…Genes annotated as IRT1 and IREG2 showed increased expression in N. caerulescens roots from serpentine versus non‐serpentine populations (Halimaa et al ., ), and a vacuolar‐targeted IREG ( PgIREG1 ) is expressed at higher levels in the hyperaccumulator P. gabriellae versus the non‐accumulator Psychotria semperflorens (Merlot et al ., ). Furthermore, strong genetic differentiation that is consistent with diversifying selection has been reported between serpentine and non‐serpentine populations of Alyssum serpyllifolium at an IREG locus (Sobczyk et al ., ). The expression pattern of these genes in Ni hyperaccumulators differs markedly from that in Arabidopsis in which it is largely restricted to the root epidermis and was barely detectable under Fe‐replete conditions (Colangelo and Guerinot, ; Schaaf et al ., ).…”

“…RNA-Seq provides the means by which to analyse gene expression in these species, but the choice of plant system is critical to extraction of the most biologically meaningful information (Halimaa et al, 2014a). Expression profiling of a plant species that exhibits variation in Ni accumulation will minimise any variation due to evolutionary divergence or adaptation to other environmental factors, and is therefore an attractive strategy by which to identify the patterns of gene expression that underpin the Ni hyperaccumulation phenotype (Sobczyk et al, 2017).…”

Parallel ecological filtering of ultramafic soils in three distant island floras

“…Ca, Mg, K) and transition metals (e.g. Fe, Ni) are linked to adaptation to serpentine (Arnold et al, 2016;Bradshaw, 2005;Sobczyk, Smith, Pollard, & Filatov, 2017;Turner, Bourne, Von Wettberg, Hu, & Nuzhdin, 2010). Among these candidate genes, transporters of the Ferroportin/IREG family were shown to transport Ni in Brassicaceae and some other plant families (Halimaa et al, 2014;Meier et al, 2018;Merlot et al, 2014;Morrissey et al, 2009;Schaaf et al, 2006), and could therefore constitute a link between adaptation to ultramafic soils and Ni hyperaccumulation.…”