Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode

No study of a single nickel (Ni) hyperaccumulator species has investigated the impact of hyperaccumulation on herbivores representing a variety of feeding modes. Streptanthus polygaloides plants were grown on high- or low-Ni soils and a series of no-choice and choice feeding experiments was conducted using eight arthropod herbivores. Herbivores used were two leaf-chewing folivores (the grasshopper Melanoplus femurrubrum and the lepidopteran Evergestis rimosalis), a dipteran rhizovore (the cabbage maggot Delia radicum), a xylem-feeder (the spittlebug Philaenus spumarius), two phloem-feeders (the aphid, Lipaphis erysimi and the spidermite Trialeurodes vaporariorum) and two cell-disruptors (the bug Lygus lineolaris and the whitefly Tetranychus urticae). Hyperaccumulated Ni significantly decreased survival of the leaf-chewers and rhizovore, and significantly reduced population growth of the whitefly cell-disruptor. However, vascular tissue-feeding insects were unaffected by hyperaccumulated Ni, as was the bug cell-disruptor. We conclude that Ni can defend against tissue-chewing herbivores but is ineffective against vascular tissue-feeding herbivores. The effects of Ni on cell-disruptors varies, as a result of either variation of insect Ni sensitivity or the location of Ni in S. polygaloides cells and tissues.     

Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Plutella xylostella (Lepidoptera: Plutellidae)

We determined the effectiveness of Ni as an elemental defence of Streptanthus polygaloides (Brassicaceae) against a crucifer specialist folivore, diamondback moth (DBM), Plutella xylostella. An oviposition experiment used arrays of S. polygaloides grown on Ni-amended (high-Ni) soil interspersed with plants grown on unamended (low-Ni) soil and eggs were allowed to hatch and larvae fed freely among plants in the arrays. We also explored oviposition preference by allowing moths to oviposit on foil sheets coated with high- or low-Ni plant extract. This was followed by an experiment using low-Ni plant extract to which varying amounts of Ni had been added and an experiment using sheets coated with sinigrin (allyl glucosinolate) as an oviposition stimulant. Diamondback moths laid 2.5-fold more eggs on low-Ni plants than on high-Ni plants and larval feeding was greater on low-Ni plants. High-Ni plants grew twice as tall, produced more leaves, and produced almost 3.5-fold more flowers. Low-Ni plants contained more allyl glucosinolate than high-Ni plants and moths preferred to oviposit on foil sheets dipped in low-Ni plant extract. Moths showed no preference when Ni concentration of low-Ni extract was varied and overwhelmingly preferred sinigrin coated sheets. We conclude that Ni hyperaccumulation is an effective elemental defence against this herbivore, increasing plant fitness through a combination of toxicity to DBM larvae and decreased oviposition by adults.     

Metal Tolerance and Accumulation Ability of the Ni Hyperaccumulator Streptanthus polygaloides Gray (Brassicaceae)

High concentrations of metals occur in some plant species (termed hyperaccumulators), such as the Ni hyperaccumulator Streptanthus polygaloides. We determined the tolerance of S. polygaloides to, and its accumulation abilities for, six metals (Ni, Zn, Cu, Co, Mn, and Pb). Potting mix concentrations used for all metals ranged from 0 to 1200 μg/g dry weight. For Ni, a treatment of 1600 μg/g was included. For Mn, treatments of 1600, 2000, and 2500 μg/g also were used, and for Pb these concentrations plus 3500 μg/g were included. Germination, plant number per pot, and size at days 30 and 39, number of plants at the end of the experiment (day 49), flower production, and metal concentration in the aboveground biomass were documented. Lead and Ni showed no consistent effects on plant performance, but yielded increased tissue metal concentrations. Streptanthus polygaloides was more sensitive to Co, Cu, and Zn, as ≥ 400 mg/g significantly suppressed plant growth, survival, and flower production. Tissue metal concentrations also were increased to maxima of 1500 μg Co/g, 120 μg Cu/g, and 6000 μg Zn/g. Manganese affected S. polygaloides less markedly, as ≥ 800 mg/kg decreased growth, survival, and flower production. Maximum tissue Mn concentration was 2900 μg/g. We concluded that S. polygaloides would be an appropriate phytoextractor for soils contaminated with Ni or low levels of Co but would not be useful for Cu, Zn, Mn, and Pb.     

Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae)

Plants use chemical defences to reduce damage from herbivores and the effectiveness of these defences can be altered by biotic and abiotic factors, such as herbivory and soil resource availability. Streptanthus polygaloides , a nickel (Ni) hyperaccumulator, possesses both Ni-based defences and organic defences (glucosinolates), but the extent to which these defences interact and respond to environmental conditions is unknown. S. polygaloides plants were grown on high-Ni and low-Ni soil and concentrations of Ni and glucosinolates were compared with those of the congeneric non-hyperaccumulator, S. insignus spp. insignus , grown under the same conditions. Ni contents were highest (4000 μg g⁻¹ dry tissue) in S. polygaloides plants grown on high-Ni soil. Glucosinolate content was significantly higher in S. insignus than in S. polygaloides suggesting that plants defended by Ni produce a lower concentration of organic defences. In a separate experiment, high-Ni S. polygaloides plants were exposed to simulated herbivory or live folivores to determine the inducibility of Ni-based and organic defences. Contents of Ni were not affected by either herbivory treatment, whereas glucosinolate concentrations were >30% higher in damaged plants. We concluded that the Ni-based defence of S. polygaloides is not induced by herbivory.     

Localization of Nickel in Tissues of Streptanthus polygaloides Gray (Cruciferae) and Endemic Nickel Hyperaccumulators from California

The genus Streptanthus Nutt. is one of the most important indicators of ultramafic floras in western North America. This genus contains taxa that are endemic or tolerant of ultramafic soils. Streptanthus polygaloides is an annual nickel hyperaccumulator strictly confined to ultramafic soils throughout the Californian Sierra Nevada foothills. Nickel concentration in S. polygaloides populations was evaluated by elemental microanalysis using inductively coupled plasma mass spectrometry (ICP-MS). Representative samples of S. polygaloides roots, stems, leaves, flowers, and fruits were studied by scanning electron microscopy (SEM) coupled to an energy-dispersive X-ray probe (SEM-EDX). Results show Ni accumulation values between 0.09 and 1.18 %, and a distribution pattern similar to that observed in other Ni hyperaccumulator taxa, with the leaf epidermis accumulating the largest concentrations.     

Antibodies against the Calcium-Binding Protein: Calsequestrin from Streptanthus tortuosus (Brassicaceae)

Plant microsomes contain a protein clearly related to a calcium-binding protein, calsequestrin, originally found in the sarcoplasmic reticulum of muscle cells, responsible for the rapid release and uptake of Ca²⁺ within the cells. The location and role of calsequestrin in plant cells is unknown. To generate monoclonal antibodies specific to plant calsequestrin, mice were immunized with a microsomal fraction from cultured cells of Streptanthus tortuosus (Brassicaceae). Two clones cross-reacted with one protein band with a molecular weight equal to that of calsequestrin (57 kilodaltons) by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunoblotting. This band is able to bind ⁴⁵Ca²⁺ and can be recognized by a polyclonal antibody against the canine cardiac muscle calsequestrin. Rabbit skeletal muscle calsequestrin cross-reacted with the plant monoclonal antibodies. The plant monoclonal antibodies generated here are specific to calsequestrin protein.     

Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait

Adaptations to particular stresses may occur only in populations experiencing those stresses or may be widespread within a species. Nickel hyperaccumulation is viewed as an adaptation to high-Ni (serpentine) soils, but few studies have determined if hyperaccumulation ability is restricted to populations from high-Ni soils or if it is a constitutive trait found in populations on both high- and low-Ni soils. We compared mineral element concentrations of Thlaspi montanum var. montanum plants grown on normal and high-Ni greenhouse soils to address this question. Seed sources were from four populations (two serpentine, two non-serpentine) in Oregon and northern California, USA. Plants from all populations were able to hyperaccumulate Ni, showing Ni hyperaccumulation to be a constitutive trait in this species. Populations differed in their ability to extract some elements (e.g., Ca, Mg, P) from greenhouse soils. We noted a negative correlation between tissue concentrations of Ni and Zn. We suggest that the ability to hyperaccumulate Ni has adaptive value to populations growing on non- serpentine soil. This adaptive value may be a consequence of metal-based plant defense against herbivores/pathogens, metal- based interference against neighboring plant species, or an efficient nutrient scavenging system. We suggest that the Ni hyperaccumulation ability of T. montanum var. montanum may be an inadvertent consequence of an efficient nutrient (possibly Zn or Ca) uptake system.     

The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator

Background: The flora of serpentine/ultramafic soils provides an excellent model system for the study of natural selection in plant populations. Streptanthus polygaloides is a nickel hyperaccumulator that is endemic to serpentine soils in the Sierra Nevada of California, and has four floral morphs (yellow, purple, yellow-to-purple and undulate).

Aims: We investigate three hypotheses: (1) the purple morph occurs in colder, wetter climates than the yellow morph; (2) tissue–soil ionic relationships differ among morphs; and (3) morphs occur on soils with differing elemental concentrations.

Methods: We queried herbarium records to investigate patterns of occurrence among the yellow and purple floral morphs, and analysed soil and tissue samples from wild populations of all four morphs.

Results: The purple morph inhabited serpentine outcrops with colder temperatures and greater precipitation levels than the yellow morph. Concentrations of elements in leaf tissue and rhizosphere soil differed little among populations of the morphs, but showed substantial within-site variation.

Conclusions: Our results suggest that a climatic gradient may be responsible for divergence in floral colour among populations of S. polygaloides. Because of the large within-site variation in soil and tissue elemental concentrations, plants appear to have a varied physiological response to edaphic factors, regardless of morph membership.     

Nickel and zinc hyperaccumulation by Alyssum murale and Thlaspi caerulescens (Brassicaceae) do not enhance survival and whole-plant growth under drought stress

Nickel and Zn hyperaccumulation by Alyssum murale and Thlaspi caerulescens bear substantial energetic costs and should confer benefits to the plant. This research determined whether metal hyperaccumulation can increase osmotic adjustment and resistance to water stress (drought). Alyssum murale and Thlaspi caerulescens treated with low or high concentrations of Ni or Zn were exposed to moderate (?0·4 MPa) and severe (?1·0 MPa) water stresses using aqueous polyethylene glycol. In the absence of metals both water deficits inhibited shoot growth. Nickel and Zn hyperaccumulation did not ameliorate growth inhibition by either level of water stress. The water stress did not induce major changes in shoot metal concentrations of these constitutive hyperaccumulators. Moreover, metal hyperaccumulation had minimal effects on the osmolality of leaf‐sap extracts, relative water content of the shoots, or rate of evapotranspiration. It is concluded that Ni or Zn hyperaccumulation does not augment whole‐plant capacity for drought resistance in A. murale and T. caerulescens.     

Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae)

Plant and Soil - This study evaluated the effect of phloem translocation on Ni accumulation in the hyperaccumulator Noccaea caerulescens. The first experiment assessed the metal and organic...     

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

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.     

Streptanthus bracteatus (Brassicaceae), a rare annual woodland forb, thrives in less cover: evidence of a vanished habitat?

One of the challenges of understanding habitat requirements of endangered species is that the remaining populations may not be in optimal habitat, requiring experimentation to determine optimal habitat and to guide management. A better knowledge of its habitat requirements is important for the conservation of Streptanthus bracteatus, a rare annual of central Texas woodlands. The habitat requirements of a rare, declining species like S. bracteatus can also provide insights into anthropogenic habitat degradation and into previous disturbance regimes. We conducted a garden experiment and a transplant experiment to determine the effect of different light environments on the growth and reproduction of S. bracteatus. Higher levels of light improved S. bracteatus performance, especially fecundity. The optimum level of combined canopy and understory cover at the height of a S. bracteatus plant (??0.5?m above ground) was less than 50?%. The remaining populations of S. bracteatus are in sub-optimal habitat because it is not open enough. The results are consistent with the hypothesis that this species was a ??fire-follower.?? The results also support the hypotheses that central Texas woodlands were once more open and that fire played an ecological role in these woodlands, an example of the ecological requirements of a rare species revealing past community structure and dynamics.     

The ebb and flow of antimicrobial skin peptides defends northern leopard frogs (Rana pipiens) against chytridiomycosis

Many amphibian species are threatened with extinction by the emerging infectious disease, chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis. This unprecedented global crisis threatens to reduce the biodiversity of the entire amphibian class. The fungus invades the skin and impairs the uptake and retention of essential ions leading to cardiac arrest. Antimicrobial peptides (AMPs) secreted into the mucus of some amphibians are thought to be an important defense against chytridiomycosis. However, little is known about the quantities of AMPs secreted under natural conditions, whether they are sufficient to protect against this pathogen, and how they interact with commensal microbes. To understand how defensive peptides and skin microbes may interact, it is essential to know the precise quantities of AMPs present under natural conditions. Using matrix‐assisted laser desorption time‐of‐flight mass spectrometry and growth inhibition assays, we show that northern leopard frogs (Rana pipiens) at rest constitutively release low amounts of AMPs that inhibit B. dendrobatidis in vitro, and AMP defenses are elevated following a simulated predator attack. Using a synthetic peptide analogue of brevinin‐1Pb as an external control, we quantified the amounts of four previously described AMPs (brevinin 1Pa, brevinin‐1Pb, brevinin‐1Pd, and ranatuerin‐2P) at several time points after secretion. Once secreted onto the skin, the peptides are most active for 15 min, and small quantities persist for at least 2 h. Taken together, our data suggest that small amounts of AMPs are rapidly available and quite stable on the skin of R. pipiens. They are effective inhibitors of B. dendrobatidis at these low constitutive concentrations but degrade within 2 h, protecting the integrity of the skin and commensal bacteria.     

Egg-mimics of Streptanthus (Cruciferae) deter oviposition by Pieris sisymbrii (Lepidoptera: Pieridae)

Summary Streptanthus breweri, a serpentine-soil annual mustard, produces pigmented callosities on its upper leaves which are thought to mimic the eggs of the Pierid butterfly Pieris sisymbrii. P. sisymbrii is one of several inflorescence-infructescence-feeding Pierids which assess egg load visually on individual host plants prior to ovipositing. Removal of the egg-mimics from S. breweri plants in situ significantly increases the probability of an oviposition relative to similar, intact plants.     

Evolutionary processes in the genusCapsella (Brassicaceae)

Capsella comprises diploid (C. grandiflora andC. rubella) and tetraploid taxa. It is argued that the tetraploidC. bursa-pastoris is of intraspecific origin despite disomic inheritance and fixed heterozygosity. It is of considerable age as evidenced by the fossil record and molecular data. Gene duplication by polyploidization and a mixed mating system provided the genetic flexibility for greatest colonizing success. Pronounced variation patterns at a micro- and macrogeographic scale are observed inC. bursa-pastoris for many characters including life history traits, leaf morphology and allozymes. This variation pattern can be explained by several components comprising phylogenetic age, random processes, ecotypic variation and colonization history. The adaptive strategy ofC. bursa-pastoris cannot be assigned to either ecotypic differentiation or phenotypic plasticity alone. It depends on the trait under study.Dedicated to emer. Univ.-Prof. DrFriedrich Ehrendorfer on the occasion of his 70th birthday     

A study of Draba cacuminum (Brassicaceae)

A morphological analysis of the Scandinavian mountain endemic Draba cacuminum Elis. Ekman is presented, based on Scandinavian herbarium collections and a population sample from the Finse area, S Norway. It is compared with supposedly close relatives, especially D. norvegica Gunnerus, and is found to be a distinct species with infraspecies variation at two levels. The populations of southern and northern Scandinavia have been separated as subspecies, ssp. cacuminum and ssp. angusticarpa Elven ssp. nov., respectively, and there is also variation within the southern subspecies. A lectotype has been chosen for D. cacuminum , a revised distribution map is presented, and the ecology and phytogeography of the species is discussed. It seems to be a weak competitor, and its present very discontinuous area is assumed to be a remnant of one continuous or more probably two areas (in S Norway and N Scandinavia) in the late Weichselian.     

Erysimum canum undE. hayekii (Brassicaceae)

Erysimum canum (Pill. & Mitterp).Polatschek transferred fromCheiranthus orSyrenia into the genusErysimum; it has 2n=14 chromosomes and a very small distribution range (parts of CSSR, Hungary, Yugoslavia). —Erysimum hayekii (Jav. & Rech. f.)Polatschek, is risen to specific rank; it has 2n=14 chromosomes (first count) and eastern Aegean distribution (Cyclades, Sporades). Typifications were made for both species.     

Leaf waxes in Coincya Rouy (Brassicaceae)

A total of 55 populations belonging to the genus Coincya Rouy (Brassicaceae) from the Iberian Peninsula were examined for their leaf wax composition. The total wax content and the relative proportions of the five main lipid fractions, hydrocarbons, esters, ketones, free alcohols and free sterols were determined. It was observed that there was a positive correlation between chemical composition and environmental adaptation, and also with certain morphological characterS. Changes relate to low temperatures or to high relative humidity, and there is a positive correlation between chemical composition and leaf glaucosity.