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

Abstract

Most metal hyperaccumulating plants accumulate nickel, yet the molecular basis of Ni hyperaccumulation is not well understood. We chose Senecio coronatus to investigate this phenomenon as this species displays marked variation in shoot Ni content across ultramafic outcrops in the Barberton Greenstone Belt (South Africa), thus allowing an intraspecific comparative approach to be employed. No correlation between soil and shoot Ni contents was observed, suggesting that this variation has a genetic rather than environmental basis. This was confirmed by our observation that the accumulation phenotype of plants from two hyperaccumulator and two non-accumulator populations was maintained when the plants were grown on a soil mix from these four sites for 12 months. We analysed the genetic variation among 12 serpentine populations of S. coronatus, and used RNA-seq for de novo transcriptome assembly and analysis of gene expression in hyperaccumulator versus non-accumulator populations. Genetic analysis revealed the presence of hyperaccumulators in two well supported evolutionary lineages, indicating that Ni hyperaccumulation may have evolved more than once in this species. RNA-Seq analysis indicated that putative homologues of transporters associated with root iron uptake in plants are expressed at elevated levels in roots and shoots of hyperaccumulating populations of S. coronatus from both evolutionary lineages. We hypothesise that Ni hyperaccumulation in S. coronatus may have evolved through recruitment of these transporters, which play a role in the iron-deficiency response in other plant species.

Parallel ecological filtering of ultramafic soils in three distant island floras

“…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. The latter qualifies plants that accumulate particular metals in their leaves to levels that may be hundreds or thousands of times greater than is normal for most plants (Reeves et al, 2018).…”

Constitutively enhanced genome integrity maintenance and direct stress mitigation characterize transcriptome of extreme stress-adaptedArabidopsis halleri

“…The biological functions of the identified loci and sequence variants on serpentine soils remain to be addressed. Recent comparative transcriptomics studies identified sets of genes with different overlapping orthologues in A. thaliana as more highly expressed in Ni hyperaccumulators on serpentine soil than in closely related nonaccumulator plants on other soils (de la Torre et al 2018;Meier et al 2018; van der Pas and Ingle 2019). Several DNA integrity maintenance genes were found to be more highly expressed in serpentine than in non-serpentine accessions of Senecio coronatus, but no quantitative enrichment was reported (Meier et al 2018).…”

“…Recent comparative transcriptomics studies identified sets of genes with different overlapping orthologues in A. thaliana as more highly expressed in Ni hyperaccumulators on serpentine soil than in closely related nonaccumulator plants on other soils (de la Torre et al 2018;Meier et al 2018; van der Pas and Ingle 2019). Several DNA integrity maintenance genes were found to be more highly expressed in serpentine than in non-serpentine accessions of Senecio coronatus, but no quantitative enrichment was reported (Meier et al 2018). It must be noted that the plants compared contrast not only in their edaphic habitat, but also in the metal hyperaccumulation trait, different from A. halleri populations Noss and Pais of this study.…”

Towards an Understanding of the Molecular Basis of Nickel Hyperaccumulation in Plants

“…Substantial intraspecific variation in Ni content can result from environmental factors, as is the case for Pimelea leptospermoides where shoot Ni contents ranging from 13 to 2873 mg kg −1 DW have been attributed to variation in total soil Ni content and pH [23]. However, in S. coronatus, this phenotypic variation has a genetic basis; plants from hyperaccumulator and non-accumulator populations have different root ultra-structures, and the accumulation phenotype of a given population persists when the plants are grown on a common soil substrate [24,25].…”

“…Subsequently, two comparative RNA-Seq studies have been reported. Meier et al [24] performed a comparative RNA-Seq analysis of Ni hyperaccumulating and non-accumulating serpentine populations of S. coronatus to identify candidate genes that may underpin the Ni hyperaccumulation phenotype. A large-scale RNA-Seq study comparing seven pairs of related Ni hyperaccumulating and non-accumulating species across five families (Brassicaceae, Rubiaceae, Cunoniaceae, Salicaceae and Euphorbiaceae) from Cuba, New Caledonia and France has recently been reported [32].…”