Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data

Abstract

Background and aims: Nickel (Ni) hyperaccumulation is a rare form of physiological specialization shared by a small number of angiosperms growing on ultramafic soils. The evolutionary patterns of this feature among European members of tribe Alysseae (Brassicaceae) are investigated using a phylogenetic approach to assess relationships among Ni hyperaccumulators at the genus, species and below-species level.

Methods: Internal transcribed spacer (ITS) sequences were generated for multiple accessions of Alysseae. Phylogenetic trees were obtained for the genera of the tribe and Alyssum sect. Odontarrhena. All accessions and additional herbarium material were tested for Ni hyperaccumulation with the dimethylglyoxime colorimetric method.

Key results: Molecular data strongly support the poorly known hyperaccumulator endemic Leptoplax (Peltaria) emarginata as sister to hyperaccumulator species of Bornmuellera within Alysseae. This is contrary to current assumptions of affinity between L. emarginata and the non-hyperaccumulator Peltaria in Thlaspideae. The lineage Bornmuellera-Leptoplax is, in turn, sister to the two non-hyperaccumulator Mediterranean endemics Ptilotrichum rupestre and P. cyclocarpum. Low ITS sequence variation was found within the monophyletic Alyssum sect. Odontarrhena and especially in A. murale sensu lato. Nickel hyperaccumulation was not monophyletic in any of three main clades retrieved, each consisting of hyperaccumulators and non-hyperaccumulators of different geographical origin.

Conclusions: Nickel hyperaccumulation in Alysseae has a double origin, but it did not evolve in Thlaspideae. In Bornmuellera-Leptoplax it represents an early synapomorphy inherited from an ancestor shared with the calcicolous, sister clade of Mediterranean Ptilotrichum. In Alyssum sect. Odontarrhena it has multiple origins even within the three European clades recognized. Lack of geographical cohesion suggests that accumulation ability has been lost or gained over the different serpentine areas of south Europe through independent events of microevolutionary adaptation and selection. Genetic continuity and strong phenotypic plasticity in the A. murale complex call for a reduction of the number of Ni hyperaccumulator taxa formally recognized.

Fig. 1.

One of the two most-parsimonious trees of tribe Alysseae generated by ITS 5·8S sequences with branch lengths (L = 1251, CI = 0·57, RI = 0·63). The main clades discussed in the text are indicated by upper case letters (A–D). Bootstrap values >50 % are indicated at the nodes; nodes collapsing in the strict consensus are indicated by dotted lines. Grey boxes indicate clades including Ni hyperaccumulators.

Fig. 2.

Bayesian phylogram (consensus) of tribe Alysseae generated by ITS 5·8S sequences. The main clades discussed in the text are indicated by upper case letters (A–D). Posterior probabilities are indicated at the nodes. Grey boxes indicate clades including Ni hyperaccumulators.

Fig. 3.

Bayesian phylogram of Alyssum section Odontarrhena generated by ITS 5·8S sequences. The main clades discussed in text are indicated as O1–O3. Posterior probabilities are shown at the nodes; corresponding bootstrap values >50 % of MP strict consensus tree (not shown) are reported in parentheses. Ni hyperaccumulator accessions as resulting from the DMG test are in bold; species names are based on evidence of the present study (see text) and taxonomic synonyms are given in parentheses.

Fig. 4.

Chorological relationships among Bornmuellera (1), Leptoplax (2), Bornmuellera plus Leptoplax (overlapping area 3), Ptilotrichum cyclocarpum and P. rupestre (4); black spots indicate the main serpentine areas in SE Europe.

Fig. 5.

Distribution of Alyssum murale in the Balkan peninsula. White and black circles indicate, respectively, non-Ni-hyperaccumulating and Ni-hyperaccumulating populations as resulting from DMG tests; black spots indicate the main serpentine areas in SE Europe.