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

Odontarrhena serpyllifolia (Desf.) Jord. & Fourr. (=Alyssum serpyllifolium Desf.) occurs in the Iberian Peninsula and adjacent areas on a variety of soils including both limestone and serpentine (ultramafic) substrates. Populations endemic to serpentine are known to hyperaccumulate nickel, and on account of this remarkable phenotype have, at times, been proposed for recognition as taxonomically distinct subspecies or even species. It remains unclear, however, to what extent variation in nickel hyperaccumulation within this taxon merely reflects differences in the substrate, or whether the different populations show local adaptation to their particular habitats. To help clarify the physiological basis of variation in nickel hyperaccumulation among these populations, 3 serpentine accessions and 3 limestone accessions were cultivated hydroponically under common-garden conditions incorporating a range of Ni concentrations, along with 2 closely related non-accumulator species, Clypeola jonthlaspi L. and Alyssum montanum L. As a group, serpentine accessions of O. serpyllifolia were able to tolerate Ni concentrations approximately 10-fold higher than limestone accessions, but a continuous spectrum of Ni tolerance was observed among populations, with the least tolerant serpentine accession not being significantly different from the most tolerant limestone accession. Serpentine accessions maintained relatively constant tissue concentrations of Ca, Mg, K, and Fe across the whole range of Ni exposures, whereas in the limestone accessions, these elements fluctuated widely in response to Ni toxicity. Hyperaccumulation of Ni, defined here as foliar Ni concentrations exceeding 1g kg-1 of dry biomass in plants not showing significant growth reduction, occurred in all accessions of O. serpyllifolia, but the higher Ni tolerance of serpentine accessions allowed them to hyperaccumulate more strongly. Of the reference species, C. jonthlaspi responded similarly to the limestone accessions of O. serpyllifolia, whereas A. montanum displayed by far the lowest degree of Ni tolerance and exhibited low foliar Ni concentrations, which only exceeded 1 g kg-1 in plants showing severe Ni toxicity. The continuous spectrum of physiological responses among these accessions does not lend support to segregation of the serpentine populations of O. serpyllifolia as distinct species. However, the pronounced differences in degrees of Ni tolerance, hyperaccumulation, and elemental homeostasis observed among these accessions under common-garden conditions argues for the existence of population-level adaptation to their local substrates.

Phylogenetic and geographic distribution of nickel hyperaccumulation in neotropical Psychotria.

PREMISE: Hyperaccumulation of heavy metals in plants has never been documented from Central America or Mexico. Psychotria grandis, P. costivenia, and P. glomerata (Rubiaceae) have been reported to hyperaccumulate nickel in the Greater Antilles, but they also occur widely across the neotropics. The goals of this research were to investigate the geographic distribution of hyperaccumulation in these species and explore the phylogenetic distribution of hyperaccumulation in this clade by testing related species. METHODS: Portable x-ray fluorescence (XRF) spectroscopy was used to analyze 565 specimens representing eight species of Psychotria from the Missouri Botanical Garden herbarium. RESULTS: Nickel hyperaccumulation was found in specimens of Psychotria costivenia ranging from Mexico to Costa Rica and in specimens of P. grandis from Guatemala to Ecuador and Venezuela. Among related species, nickel hyperaccumulation is reported for the first time in P. lorenciana and P. papantlensis, but no evidence of hyperaccumulation was found in P. clivorum, P. flava, or P. pleuropoda. Previous reports of hyperaccumulation in P. glomerata appear to be erroneous, resulting from taxonomic synonymy and specimen misidentification. CONCLUSIONS: Hyperaccumulation of nickel by Psychotria is now known to occur widely from southern Mexico through Central America to northwestern South America, including some areas not known to have ultramafic soils. Novel aspects of this research include the successful prediction of new hyperaccumulator species based on molecular phylogeny, use of XRF technology to nondestructively obtain elemental data from herbarium specimens, and documentation of previously unknown areas of ultramafic or nickel-rich soil based on such data.

X-Ray Fluorescence Ionomics of Herbarium Collections.

Global herbaria are the greatest repositories of information on the plant kingdom. Discoveries of trace element hyperaccumulator plants have historically required time-consuming destructive chemical analysis of fragments from herbarium specimens, which severely constrains the collection of large datasets. Recent advances in handheld X-Ray Fluorescence spectroscopy (XRF) systems have enabled non-destructive analysis of plant samples and here we propose a new method, which we term "Herbarium XRF Ionomics", to extract elemental data from herbarium specimens. We present two case studies from major tropical herbaria where Herbarium XRF Ionomics has led to the discovery of new hyperaccumulator plants and provided valuable insights into phylogenetic patterns of trace element hyperaccumulation. Herbarium XRF Ionomics is a new value proposition for continued funding and retention of herbarium specimens globally.

Facultative hyperaccumulation of heavy metals and metalloids.

Approximately 500 species of plants are known to hyperaccumulate heavy metals and metalloids. The majority are obligate metallophytes, species that are restricted to metalliferous soils. However, a smaller but increasing list of plants are "facultative hyperaccumulators" that hyperaccumulate heavy metals when occurring on metalliferous soils, yet also occur commonly on normal, non-metalliferous soils. This paper reviews the biology of facultative hyperaccumulators and the opportunities they provide for ecological and evolutionary research. The existence of facultative hyperaccumulator populations across a wide edaphic range allows intraspecific comparisons of tolerance and uptake physiology. This approach has been used to study zinc and cadmium hyperaccumulation by Noccaea (Thlaspi) caerulescens and Arabidopsis halleri, and it will be instructive to make similar comparisons on species that are distributed even more abundantly on normal soil. Over 90% of known hyperaccumulators occur on serpentine (ultramafic) soil and accumulate nickel, yet there have paradoxically been few experimental studies of facultative nickel hyperaccumulation. Several hypotheses suggested to explain the evolution of hyperaccumulation seem unlikely when most populations of a species occur on normal soil, where plants cannot hyperaccumulate due to low metal availability. In such species, it may be that hyperaccumulation is an ancestral phylogenetic trait or an anomalous manifestation of physiological mechanisms evolved on normal soils, and may or may not have direct adaptive benefits.

Quantitative genetics of zinc hyperaccumulation in Thlaspi caerulescens.

We examined variation within and between populations of Thlaspi caerulescens J. & C. Presl (Brassicaceae). a plant species known to hyperaccumulate zinc to foliar concentrations exceeding 3 % (d.wt basis). Seeds were collected as sib families from two populations in Derbyshire, UK along with leaf samples from the parent plants. Offspring were grown hydroponically from seed, in culture solution containing 10 mg 1 -1 Zn. Significant differences in zinc concentration and plant size were Found between populations and among sib families within populations. Heritability analysis based on resemblance among sibs revealed significant heritable variation within one population, but not the other. The characters of zinc accumulation and plant size were not correlated. Parent-offspring recession did not prove useful for estimation of heritability, because of heterogeneity in metal availability to parents growing in the field. The results are relevant to attempts to exploit metal hyperaccumulation as a technology for remediation of contaminated soil, and to our understanding of the evolutionary origins of the phenomenon of hyperaccumulation.

Variation in Cnidoscolus texanus in relation to herbivory.

Twelve Oklahoma populations of Cnidoscolus texanus were investigated for morphological variation between and within populations, and between site classes with contrasting histories of use by domesticated livestock. Characters scored were numbers of stinging hairs on petioles and midribs, and depth of leaf lobing. Leaf lobing was not significantly variable within or among populations or grazing categories. Stinging hair numbers showed significant differences within and among populations. Petiole stinging hairs were more numberous in heavily grazed sites, suggesting population differentiation in response to the selective pressures of herbivory.