Photosynthesizing while hyperaccumulating nickel: Insights from the genus Odontarrhena (Brassicaceae).

Nickel-induced changes in photosynthetic activity were investigated in three Ni-hyperaccumulating Odontarrhena species with increasing Ni tolerance and accumulation capacity, O. muralis, O. moravensis, and O. chalcidica. Plantlets were grown in hydroponics at increasing NiSO4 concentrations (0, 0.25, and 1 mM) for one week, and the effects of Ni on growth, metal accumulation, photosynthesis, and nitrogen (N) allocation to components of the photosynthetic apparatus were analysed. Nickel treatments in O. chalcidica, and O. moravensis to a lesser extent, increased not only the photochemical efficiency of photosystem II (PSII) and the CO2 assimilation rate, but also CO2 diffusion from the atmosphere to the carboxylation sites. These two species displayed a specific increase and/or rearrangement of the photosynthetic pigments and a higher leaf N allocation to the photosynthetic components in the presence of the metal. Odontarrhena muralis displayed a decrease in photosynthetic performance at the lowest Ni concentration due to a combination of both stomatal and non-stomatal limitations. Our data represent the first complete investigation of the effects of Ni on the photosynthetic machinery in Ni hyperaccumulating plants. Our findings clearly indicate a stimulatory, hormetic-like, effect of the metal on both biophysics and biochemistry of photosynthesis in the species with the highest hyperaccumulation capacity.

Population Genetics of Odontarrhena (Brassicaceae) from Albania: The Effects of Anthropic Habitat Disturbance, Soil, and Altitude on a Ni-Hyperaccumulator Plant Group from a Major Serpentine Hotspot.

Albanian taxa and populations of the genus Odontarrhena are most promising candidates for research on metal tolerance and Ni-agromining, but their genetic structure remains unknown. We investigated phylogenetic relationships and genetic differentiation in relation to distribution and ploidy of the taxa, anthropic site disturbance, elevation, soil type, and trace metals at each population site. After performing DNA sequencing of selected accessions, we applied DNA-fingerprinting to analyze the genetic structure of 32 populations from ultramafic and non-ultramafic outcrops across Albania. Low sequence divergence resulted in poorly resolved phylograms, but supported affinity between the two diploid serpentine endemics O. moravensis and O. rigida. Analysis of molecular variance (AMOVA) revealed significant population differentiation, but no isolation by distance. Among-population variation was higher in polyploids than in diploids, in which genetic distances were lower. Genetic admixing at population and individual level occurred especially in the polyploids O. chalcidica, O. decipiens, and O. smolikana. Admixing increased with site disturbance. Outlier loci were higher in serpentine populations but decreased along altitude with lower drought and heat stress. Genetic variability gained by gene flow and hybridization at contact zones with "resident" species of primary ultramafic habitats promoted expansion of the tetraploid O. chalcidica across anthropogenic sites.

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

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. 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.