Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?

Plants that accumulate metal and metalloid trace elements to extraordinarily high concentrations in their living biomass have inspired much research worldwide during the last decades. Hyperaccumulators have been recorded and experimentally confirmed for elements such as nickel, zinc, cadmium, manganese, arsenic and selenium. However, to date, hyperaccumulation of lead, copper, cobalt, chromium and thallium remain largely unconfirmed. Recent uses of the term in relation to rare-earth elements require critical evaluation. Since the mid-1970s the term ‘hyperaccumulator’ has been used millions of times by thousands of people, with varying degrees of precision, aptness and understanding that have not always corresponded with the views of the originators of the terminology and of the present authors. There is therefore a need to clarify the circumstances in which the term ‘hyperaccumulator’ is appropriate and to set out the conditions that should be met when the terms are used. We outline here the main considerations for establishing metal or metalloid hyperaccumulation status of plants, (re)define some of the terminology and note potential pitfalls. Unambiguous communication will require the international scientific community to adopt standard terminology and methods for confirming the reliability of analytical data in relation to metal and metalloid hyperaccumulators.

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Hyperaccumulators of metal and metalloid trace elements: Facts and fiction

During the history of life on Earth, tectonic and climatic change repeatedly generated large territories that were virtually devoid of life and exhibited harsh environmental conditions. The ability of a few specialist pioneer plants to colonize such hostile environments was thus of paramount ecological importance for the continuous maintenance of primary production over time. Yet, we know very little about how extreme traits evolve and function in plants. Recent breakthroughs have given first insights into the molecular basis underlying the complex extreme model trait of metal hyperaccumulation and associated metal hypertolerance. This review gives an introduction into the hyperaccumulator research field and its history; provides an overview of hyperaccumulator germplasm; describes the state of the art of our understanding of the physiological, molecular, and genetic basis underlying metal hyperaccumulation and its evolution; and highlights future research needs and opportunities.

Metal Hyperaccumulation in Plants

Arsenic (As) is an element that is nonessential for and toxic to plants. Arsenic contamination in the environment occurs in many regions, and, depending on environmental factors, its accumulation in food crops may pose a health risk to humans.Recent progress in understanding the mechanisms of As uptake and metabolism in plants is reviewed here. Arsenate is taken up by phosphate transporters. A number of the aquaporin nodulin26-like intrinsic proteins (NIPs) are able to transport arsenite,the predominant form of As in reducing environments. In rice (Oryza sativa), arsenite uptake shares the highly efficient silicon (Si) pathway of entry to root cells and efflux towards the xylem. In root cells arsenate is rapidly reduced to arsenite, which is effluxed to the external medium, complexed by thiol peptides or translocated to shoots. One type of arsenate reductase has been identified, but its in planta functions remain to be investigated. Some fern species in the Pteridaceae family are able to hyperaccumulate As in above-ground tissues. Hyperaccumulation appears to involve enhanced arsenate uptake, decreased arsenite-thiol complexation and arsenite efflux to the external medium, greatly enhanced xylem translocation of arsenite, and vacuolar sequestration of arsenite in fronds. Current knowledge gaps and future research directions are also identified.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.2008.02716.x

Arsenic uptake and metabolism in plants.

Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils.

Mine tailings can have a specific assemblage of plant species due to their unique physicochemical properties, and this process can be important in developing ecological theory and restoration practice. Physicochemical properties and natural colonization of plants on five lead/zinc (Pb/Zn) mine tailings in southern China were investigated. The tailings studied included Fankou and Lechang in Guangdong Province, and Huangshaping, Shuikoushan, and Taolin in Hunan Province. Physicochemical properties of the tailings varied greatly both among and within tailings ponds, but in general, all contained high concentrations of heavy metals (Pb, Zn, Cu, and Cd) and low concentrations of N, P, and organic matter. Toxic levels of heavy metals and deficiency of major nutrients appeared to be the major constraints for colonization of plants on these Pb/Zn tailings and were reflected in the metal concentration of the plant tissues. The natural colonization of plants on these tailings was limited, with only some small patches distributed mainly on the edge of tailing ponds and even fewer patches on the center of the ponds. In total 54 plant species belonging to 51 genera and 24 families were recorded on the five tailings ponds, of which the 13 species belonging to Gramineae were major components of the tailings’ flora. Species establishing on the tailings at the initial colonization phase greatly depended on their seed-dispersal capacity. Further establishment and growth were then dependent on at least one of the three ecological strategies: (1) microsite (avoidance) strategy: plant establishment on tailings depended on dispersing onto microsites of relatively favorable edaphic conditions; (2) tolerance strategy: plant establishment was a result of evolving metal-tolerant ecotypes or constitutional metal tolerance; and (3) rhizome strategy: plant establishment on tailings depended on clonal growth by rhizomatous extension.

Natural Colonization of Plants on Five Lead/Zinc Mine Tailings in Southern China

Uptake and accumulation of arsenic by 11 Pteris taxa from southern China.

The goal of the present study was to assess a soil seed bank as an input seed source for revegetating lead/ zinc (Pb/Zn) mine tailings. The seed bank source was abandoned farmland, whose top 10-cm layer of topsoil contained 6,850 ± 377 seeds/m 2 from 41 species. The seeds in the soil were principally distributed in the upper 0-2 cm, which held 75.8% of total seeds and 92.7% of species composition. The top 2-cm layer of topsoil may be sufficient to serve the purpose of providing a seed source for revegetation on derelict lands, including mined lands. Four different thicknesses of topsoil (1, 2, 4, and 8 cm, redistributed from the total 0-10-cm layer from the farmland) were field-tested on the Pb/Zn mine tailings. There was no significant difference in seedling density among the 4 thickness treatments. Many seeds in the treatments with more than 1-cm of topsoil were unable to emerge from the deeper layer. Seedlings in plots with topsoil of 1-, 2-and 4-cm failed to establish within 1 year due to the extremely high acidity (pH 2.39 to 2.76). A shallow layer of topsoil cannot neutralize the sulfuric acid generated from oxidation of pyrites in the tailings. For establishment of seedlings on metalliferous lands, an insulating layer such as subsoil, building rubble, or domestic refuse is necessary before covering with valuable topsoil. The woody legume Leucaena leucocephala grown on the tailings with a topsoil cover of 8-cm was the most dominant species. Lead was accumulated in root, branch, stem bark, and xylem, which accounted for more than 80% of the total metal concentration in the plant. This portion of Pb will reside in the plant for a long period, while the smaller portion of Pb in the leaf (about 15%) could be returned to the environment as litter during growth. Woody plants may have an advantage in metal-phyto-remediation over herbaceous plants.

Soil seed bank as an input of seed source in revegetation of lead/zinc mine tailings

Lime and pig manure as ameliorants for revegetating lead/zinc mine tailings: a greenhouse study

The present project aims to investigate the possible contamination of teas with the trace metals: Al, Cu and Zn. Tea bushes sampled from two tea plantations in the northern part of Guangdong Province accumulated higher concentrations of Cu and Zn in young leaves, and of Al in old leaves. The analysis of the three metals in tea produced in different provinces indicated higher Al levels in those obtained from Guangdong and Yunnan Provinces, which may be due to the lower soil pH in these areas. Green tea had the lowest Al concentration among the four types of tea studied, as only the bud and two young leaves are used, whereas older leaves are used for other types of tea (black, Oolong and Puerh tea). The transfer of Al, Cu and Zn from soil to different parts of tea bushes was low in general, except for Zn at Lechang tea plantation which next to a Pb/Zn mine, where a higher transfer was observed from young leaves to tea products, indicating possible metal contamination during tea processing. However, low concentrations of Cu and Zn (less than 0.07 mg Cu L-1 and 0.17 mg Zn L-1), and moderate amounts of Al (2.1-2.5 mg L-1) were obtained in the tea liquor (1% hot water extracts).

C. Y. Lan

Papers

Natural Colonization of Plants on Five Lead/Zinc Mine Tailings in Southern China

Uptake and accumulation of arsenic by 11 Pteris taxa from southern China.

Soil seed bank as an input of seed source in revegetation of lead/zinc mine tailings

Lime and pig manure as ameliorants for revegetating lead/zinc mine tailings: a greenhouse study

Trace metal contents (Al, Cu and Zn) of tea: tea and soil from two tea plantations, and tea products from different provinces of China