Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

Abstract

Background Hyperaccumulator plants are unusual plants that accumulate particular metals or metalloids, such as nickel, zinc, cadmium and arsenic, in their living tissues to concentrations that are hundreds to thousands of times greater than what is normal for most plants. The hyperaccumulation phenomenon is rare (exhibited by less than 0.2% of all angiosperms), with most of the ~500 hyperaccumulator species known globally for nickel. Scope This review highlights the contemporary understanding of nickel hyperaccumulation processes, which include root uptake and sequestration, xylem loading and transport, leaf compartmentation and phloem translocation processes. Conclusions Hyperaccumulator plants have evolved highly efficient physiological mechanisms for taking up nickel in their roots followed by rapid translocation and sequestration into the aerial shoots. The uptake of nickel is mainly involved with low affinity transport systems, presumably from the ZIP family. The presence of high concentrations of histidine prevents nickel sequestration in roots. Nickel is efficiently loaded into the xylem, where it mainly presents as Ni 2+. The leaf is the main storage organ, which sequestrates nickel in nonactive sites, e.g. vacuoles and apoplast. Recent studies show that phloem translocates high levels of nickel, which has a strong impact on nickel accumulation in young growing tissues. Nickel hyperaccumulator plants: Discovery and application Nickel (Ni) is the latest element to be considered essential for higher plants (Brown et al. 1987; Marschner 1995; Gerendas et al. 1999), due to its key role in urease, an enzyme that is widely distributed in higher plants (Hogan et al. 1983). The presence of urease prevents the accumulation of urea, which is generated during metabolic processes and is toxic to plants when presents in high concentrations. Apart from its function in urease activation, other physiological functions of Ni are poorly understood in higher plants (Gerendas et al. 1999). Although Ni is an essential micronutrient, its physiological requirement is extremely low. It is shown that 0.1 mg kg −1 or lower is sufficient for seed germination and plant growth (Brown et al. 1987; Gerendas et al. 1999). Hence, Ni deficiency in naturally-grown plants rarely occurs, and the only known case is for the pecan (Wood et al. 2004). Plants usually contain low concentrations of Ni, normally ranging from 0.01-5 mg kg −1 (Welch 1981). In contrast to the low Ni accumulation in normal plants, there is a group of plant species (hyperaccumulators) that can accumulate exceptional concentrations of Ni (>1000 mg kg −1 dry weight) in their living shoots without symptoms of toxicity (Brooks et al. 1977). Amazingly, up to 60.2 and 66.7 g kg −1 foliar Ni concentrations in the Ni hyperaccumulator Phyllanthus × pallidus from Cuba and Alyssum cassium from Turkey have been recorded (Reeves et al. 1996; Reeves and Adıgüzel 2008); while 25% Ni is found in the latex of the New Caledonian tree Pycnandra acuminata, and 16.9% Ni in the phloem sap exu...

Morais Ultramafic Complex: A Survey towards Nickel Phytomining

“…Leaves and flowers from site 2 present no significant differences between them in terms of Ni accumulation, with 7723 and 7264 mg kg −1 , respectively. These results are expected, since other studies show that the leaves are the main storage organ where the majority of Ni is accumulated [38]. Groeber et al reported that flowers of hyperaccumulator plants can accumulate Ni concentrations as high as that in leaves, which is in agreement with this study [39].…”

Phytoremediation of Soil Contaminated with Lithium Ion Battery Active Materials—A Proof-of-Concept Study

“…All leaf samples showed increased Ni, Co, and Mn concentrations after 26 days of accumulation (>20%). Hence, leaves are likely the main storage organ for Ni, Co, and Mn hyperaccumulation [21]. Overall, a distinct trend for accumulation in plant tissues, especially for higher concentrations (18/27, green), and a reduced contamination of soils were observed (7/9, red).…”

“…Images of the leaves at contamination levels 1 and 2 for Ni, Co, and Mn after the accumulation phase are shown in the supporting information ( Figure S4). The Ni uptake mechanism was studied intensively in recent years and the translocation can be described by multiple complexation and decomplexation steps (chelating agents like histidine, glutamine, and carboxylic acids) during the Ni 2+ transport from the roots via the xylem to the leaf [21]. In the leaf, Ni is generally complexed by citric acid and sequestered in leaf vacuoles via transporters from the zinc transporter protein (ZIP) family [21].…”

“…The hypertolerance toward toxic metals can be explained by (I) detoxification by complexation, (II) metal sequestration in cellular compartments, and (III) metal sequestration via exocellular deposition [19]. The capability of hyperaccumulation for Ni 2+ , Co 2+ , and Mn 2+ ions was described for different species, and the application of plants for the detoxification of soils has been demonstrated (phytoremediation) [19][20][21][22][23][24]. This low-cost and green technology constitutes a valuable niche compared to expensive conventional soil remediation approaches.…”

The behavior of nickel isotopes at the biogeochemical interface between ultramafic soils and Ni accumulator species

“…Studies carried out over the past 40 years have focused on Ni (hyper)accumulators (e.g. Jaffré et al, 1976;Lee et al, 1977;Brooks et al, 1979;Reeves et al, 1983) to better understand the Ni accumulation phenomenon resulting from the stimulated uptake of Ni by the roots and an efficient transfer of Ni to the leaves through efficient xylem transport and phloem distribution (Centofanti et al, 2013;Tang et al, 2016;Deng et al, 2018), and to evaluate their phytomining and phytoremediation potential (e.g. Minguzzi and Vergnano, 1948;Reeves et al, 1996Reeves et al, , 1999Puschenreiter et al, 2005;Centofanti et al, 2012;van der Ent et al, 2015).…”