Inability to accumulate Ni in a genus of hyperaccumulators: the paradox of Odontarrhena sibirica (Brassicaceae)

Abstract

Main conclusion Odontarrhena is a highly diverse genus of Ni-hyperaccumulators. Here, we demonstrate substantial inability to accumulate Ni in the facultative serpentinophyte O. sibirica, which seems a unique case among the numerous species of the genus that grow on ultramafic soils. Abstract Odontarrhena is the most diverse genus of Ni-accumulating plants in W Eurasia, with most taxa growing obligatorily or facultatively on ultramafic soils. A notable exception may be O. sibirica, a facultative serpentinophyte from the E Mediterranean and W Asia in which accumulation ability is still enigmatic. We addressed this issue using observational and experimental methods. Atomic Absorption Analysis of 33 herbarium specimens and plant and soil samples from seven ultramafic and non-ultramafic sites in Greece revealed shoot Ni values always much lower than 1000 µg g−1, non-significant differences between plants from the two soil types and no relationship with soil pH. Only two Turkish specimens from waste mines had shoot Ni concentration > 1000 µg g−1. The reasons for this deviating result remain obscure, but may be associated with inherent peculiarities of the local populations. When cultivated together with congeneric Ni-accumulating species on the same natural ultramafic soil, only O. sibirica was unable to accumulate the metal. Although plant growth was stimulated in hydroponics at relatively low NiSO4 levels (50–150 µM), as typical for hyperaccumulators, Ni-accumulation occurred only at higher concentrations which had a toxic effect. This peculiar combination of Ni-response traits could be the result of a partial evolutionary loss of ability with respect to all other Ni-accumulating congeneric species. For this, O. sibirica could represent a unique model system for further studies on the evolutionary dynamics, physiological mechanisms and genetic control of metal accumulation and homeostasis.

Trichome Biomineralization and Soil Chemistry in Brassicaceae from Mediterranean Ultramafic and Calcareous Soils

“…Adaptations may involve either tolerance or avoidance, such as metal exclusion at the root level, compartmentalization in various plant organs and toxicity tolerance [22]. Some species are able to accumulate over 100 to 1000 times as much metal in their shoots and leaves as their non-hyperaccumulating relatives without displaying toxicity symptoms [22,[28][29][30]. Minimum hyperaccumulation thresholds in plants are defined at 10000, 1000, 300 μg g −1 of leaf dry weight for Mn, Ni and Co, respectively [29].…”

Diversity of Ni growth response and accumulation in Central-Eastern Mediterranean Odontarrhena (Brassicaceae) populations on and off serpentine sites

“…Such Ni-hyperaccumulators are often obligate endemics of Ni-rich serpentine outcrops, while more rarely they grow either on or off these substrates with, respectively, hyperaccumulating and nonaccumulating populations (Wójcik et al, 2017). So far, the only known exception is O. sibirica, the serpentine populations of which are apparently the only ones in the genus incapable of metal hyperaccumulation (Bettarini et al, 2020). Odontarrhena taxa and populations have been studied as indicators in prospecting for metals (Brooks, 1983), as model systems to investigate the mechanisms of metal-hyperaccumulation (Verbruggen et al, 2009;Deng et al, 2018) and, more recently, as resources for practical applications of metal phytoextraction and agromining (van der Ent et al, 2015;Kidd et al, 2018).…”

“…In addition, such studies were based on populations of a single species or, in other cases, on one population of two or three distantly related species, sometimes of doubtful taxonomic identification (Cecchi et al, 2018). A recent investigation on O. sibirica provided a more detailed analysis of the Ni-induced stimulation of growth at low metal concentrations (Bettarini et al, 2020). In such study, the metal response in terms of root and shoot growth was found to fit the Brain-Cousens hormetic model (Brain and Cousens, 1989) in serpentine populations of both O. sibirica and O. chalcidica.…”

Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of Odontarrhena serpyllifolia (Brassicaceae: Alysseae) from the Iberian Peninsula

“…As thus construed, the genus Odontarrhena includes 40-50 species of Ni hyperaccumulators [28,[32][33][34][35]. The majority are obligate metallophytes [36,37], but eight or more species are facultative hyperaccumulators [11]. Odontarrhena serpyllifolia (Desf.)…”

“…As explained above, the experimental design included non-metallophyte reference species; however, because almost all Odontarrhena spp. are capable of hyperaccumulation [37], it was necessary to use species from other closely related genera in the tribe Alysseae. Two such species were employed, neither of which has been reported to be commonly associated with serpentine or other ultramafic soil [34,42,43,46].…”