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Environmental geochemistry of the abandoned Mamut Copper Mine (Sabah) Malaysia

van der Ent A, Edraki M

Environ Geochem Health, 2018 Feb;40(1):189-207.
PMID: 27848090 DOI: 10.1007/s10653-016-9892-3

The Mamut Copper Mine (MCM) located in Sabah (Malaysia) on Borneo Island was the only Cu-Au mine that operated in the country. During its operation (1975-1999), the mine produced 2.47 Mt of concentrate containing approximately 600,000 t of Cu, 45 t of Au and 294 t of Ag, and generated about 250 Mt of overburden and waste rocks and over 150 Mt of tailings, which were deposited at the 397 ha Lohan tailings storage facility, 15.8 km from the mine and 980 m lower in altitude. The MCM site presents challenges for environmental rehabilitation due to the presence of large volumes of sulphidic minerals wastes, the very high rainfall and the large volume of polluted mine pit water. This indicates that rehabilitation and treatment is costly, as for example, exceedingly large quantities of lime are needed for neutralisation of the acidic mine pit discharge. The MCM site has several unusual geochemical features on account of the concomitant occurrence of acid-forming sulphide porphyry rocks and alkaline serpentinite minerals, and unique biological features because of the very high plant diversity in its immediate surroundings. The site hence provides a valuable opportunity for researching natural acid neutralisation processes and mine rehabilitation in tropical areas. Today, the MCM site is surrounded by protected nature reserves (Kinabalu Park, a World Heritage Site, and Bukit Hampuan, a Class I Forest Reserve), and the environmental legacy prevents de-gazetting and inclusion in these protected area in the foreseeable future. This article presents a preliminary geochemical investigation of waste rocks, sediments, secondary precipitates, surface water chemistry and foliar elemental uptake in ferns, and discusses these results in light of their environmental significance for rehabilitation.
Multi-element concentrations in plant parts and fluids of Malaysian nickel hyperaccumulator plants and some economic and ecological considerations

van der Ent A, Mulligan D

J Chem Ecol, 2015 Apr;41(4):396-408.
PMID: 25921447 DOI: 10.1007/s10886-015-0573-y

Information about multi-elemental concentrations in different plant parts of tropical Ni hyperaccumulator species has the potential to provide insight into their unusual metabolism relative to a range of essential and non-essential elements, but this information is scant in the literature. As Ni hyperaccumulation, and possibly co-accumulation of other toxic elements, has been hypothesized to provide herbivore (insect) protection, there is a need to quantify a range of these elements in plant tissues and transport fluids to at least verify the possibility of this explanation. In this study, multiple elements were analyzed in a range of different plant parts and transport fluids from Ni hyperaccumulator species collected from Sabah (Malaysia). The results show preferential accumulation of Ni in leaves over woody parts, but the highest concentrations were found in the phloem tissue (up to 7.9 % in Rinorea bengalensis) and phloem sap (up to 16.9 % in Phyllanthus balgooyi), visible by a bright green coloration in the field fresh material. The amount of Ni contained in one mature R. bengalensis tree was calculated at 4.77 kg. The high Ni concentration in the flowers of Phyllanthus securinegoides could affect insect floral visitors and pollination. High concentrations of Ni in the seeds of this species also could supply the seedling with Ni and aid in herbivory protection during the first stages of development. Foliar Ca and Ni in P. cf. securinegoides and R. bengalensis are positively correlated. Low accumulation of Ca is desirable for phytomining but concentrations of Ca are high in most Ni hyperaccumulators examined, and this could have consequences for the economic viability of Ni extraction from bio ore if these species were to be used as 'metal crops'.
Fulltext Range extension of Christisonia scortechinii from mainland Southeast Asia into Borneo, and notes on the distinction between Aeginetia and Christisonia (Orobanchaceae)

van der Ent A, Wong KM

Bot Stud, 2015 Dec;56(1):28.
PMID: 28510837 DOI: 10.1186/s40529-015-0109-3

BACKGROUND: Christisonia is a little-documented and poorly studied root-parasitic genus in the Orobanchaceae occurring in India, China, Indochina and part of the Malesian region. Recent collection of a Christisonia taxon in Kinabalu Park in Sabah, Borneo, taxonomically identical to earlier Sabah collections that have hitherto not been recorded in the literature, led to an assessment of the taxonomic identity of the species against Christisonia scortechinii, C. siamensis, C. sinensis and related species.
RESULTS: Some taxa in China, Indochina, the Malay Peninsula, and the Philippines are morphologically identical to the Borneo taxon except in the number of calyx lobes, but differ by several distinctive characters from other well-distinguished species in the region. Studies of dried herbarium specimens, augmented by photographic images of different stages of fresh flowering material and a scrutiny of available descriptions confirmed that the calyx has two primary lobes in the bud that may separate into 3-5 portions, giving a variable number of apparent lobes in specimen material collected at different localities. This new scrutiny of the calyx also permitted an improved description of the calyx differences that separate Christisonia and the closely related Aeginetia, which have not been clearly elucidated in the past.
CONCLUSIONS: Christisonia scortechinii Prain (Orobanchaceae), the only species that was described as having an initially spathaceous calyx among species of this root-parasitic genus, is newly recorded for Borneo (including Kinabalu Park, where its presence has been overlooked). The range of the species in mainland Southeast Asia, previously extended from Peninsular Malaysia to Thailand and Vietnam, is here further extended to Laos and China. Christisonia wightii Elmer (relevant to the Philippines) and C. sinensis Beck (China) are reduced to synonymy.
Fulltext Pittosporum peridoticola (Pittosporaceae), a new ultramafic obligate species restricted to Kinabalu Park (Sabah, Malaysia)

Sugau JB, van der Ent A

Bot Stud, 2015 Dec;57(1):4.
PMID: 28510789 DOI: 10.1186/s40529-016-0119-9

BACKGROUND: Kinabalu Park, in Sabah (Malaysia) on Borneo Island, is renowned for the exceptionally high plant diversity it protects, with at least 5000 plant species enumerated to date. Discoveries of plant novelties continue to be made in Sabah, especially on isolated ultramafic outcrops, including in the genus Pittosporum (Pittosporaceae) with P. linearifolium from Bukit Hampuan on the southern border of the Park, and P. silamense from Bukit Silam in Eastern Sabah, both narrow endemics restricted to ultramafic soils.
RESULTS: A distinctive new species of Pittosporum (P. peridoticola J.B.Sugau and Ent, sp. nov.) was discovered on Mount Tambuyukon in the north of Kinabalu Park during ecological fieldwork. The diagnostic morphological characters of this taxon are discussed and information about the habitat in which it grows is provided. The soil chemistry in the rooting zone of P. peridoticola has high magnesium to calcium quotients, high extractable nickel and manganese concentrations, but low potassium and phosphorus concentrations, as is typical for ultramafic soils. Analysis of foliar samples of various Pittosporum-species originating from ultramafic and non-ultramafic soils showed a comparable foliar elemental stoichiometry that is suggestive of 'Excluder-type' ecophysiology.
CONCLUSION: Pittosporum peridoticola is an ultramafic obligate species restricted to Kinabalu Park with only two known populations within the boundaries of the protected area. It is vulnerable to any future stochastic landscape disturbance events, such as forest fires or severe droughts, and therefore its conservation status is 'Near Threatened'.
Fulltext Convergent patterns of tissue-level distribution of elements in different tropical woody nickel hyperaccumulator species from Borneo Island

Abubakari F, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, van der Ent A

AoB Plants, 2020 Dec;12(6):plaa058.
PMID: 33408845 DOI: 10.1093/aobpla/plaa058

The Malaysian state of Sabah on the Island of Borneo has recently emerged as a global hotspot of nickel hyperaccumulator plants. This study focuses on the tissue-level distribution of nickel and other physiologically relevant elements in hyperaccumulator plants with distinct phylogenetical affinities. The roots, old stems, young stems and leaves of Flacourtia kinabaluensis (Salicaceae), Actephila alanbakeri (Phyllanthaceae), Psychotria sarmentosa (Rubiaceae) and young stems and leaves of Glochidion brunneum (Phyllanthaceae) were studied using nuclear microprobe (micro-PIXE and micro-BS) analysis. The tissue-level distribution of nickel found in these species has the same overall pattern as in most other hyperaccumulator plants studied previously, with substantial enrichment in the epidermal cells and in the phloem. This study also revealed enrichment of potassium in the spongy and palisade mesophyll of the studied species. Calcium, chlorine, manganese and cobalt were found to be enriched in the phloem and also concentrated in the epidermis and cortex of the studied species. Although hyperaccumulation ostensibly evolved numerous times independently, the basic mechanisms inferred from tissue elemental localization are convergent in these tropical woody species from Borneo Island.
Fulltext Extreme nickel hyperaccumulation in the vascular tracts of the tree Phyllanthus balgooyi from Borneo

Mesjasz-Przybylowicz J, Przybylowicz W, Barnabas A, van der Ent A

New Phytol, 2016 Mar;209(4):1513-26.
PMID: 26508435 DOI: 10.1111/nph.13712

Phyllanthus balgooyi (Phyllanthaceae), one of > 20 nickel (Ni) hyperaccumulator plant species known in Sabah (Malaysia) on the island of Borneo, is remarkable because it contains > 16 wt% Ni in its phloem sap, the second highest concentration of Ni in any living material in the world (after Pycnandra acuminata (Sapotaceae) from New Caledonia with 25 wt% Ni in latex). This study focused on the tissue-level distribution of Ni and other elements in the leaves, petioles and stem of P. balgooyi using nuclear microprobe imaging (micro-PIXE). The results show that in the stems and petioles of P. balgooyi Ni concentrations were very high in the phloem, while in the leaves there was significant enrichment of this element in the major vascular bundles. In the leaves, cobalt (Co) was codistributed with Ni, while the distribution of manganese (Mn) was different. The highest enrichment of calcium (Ca) in the stems was in the periderm, the epidermis and subepidermis of the petiole, and in the palisade mesophyll of the leaf. Preferential accumulation of Ni in the vascular tracts suggests that Ni is present in a metabolically active form. The elemental distribution of P. balgooyi differs from those of many other Ni hyperaccumulator plant species from around the world where Ni is preferentially accumulated in leaf epidermal cells.
Fulltext Frequency distribution of foliar nickel is bimodal in the ultramafic flora of Kinabalu Park (Sabah, Malaysia)

van der Ent A, Echevarria G, Nkrumah PN, Erskine PD

Ann Bot, 2020 10 30;126(6):1017-1027.
PMID: 32597938 DOI: 10.1093/aob/mcaa119

BACKGROUND AND AIMS: The aim of this study was to test the frequency distributions of foliar elements from a large dataset from Kinabalu Park (Sabah, Malaysia) for departure from unimodality, indicative of a distinct ecophysiological response associated with hyperaccumulation.
METHODS: We collected foliar samples (n = 1533) comprising 90 families, 198 genera and 495 plant species from ultramafic soils, further foliar samples (n = 177) comprising 45 families, 80 genera and 120 species from non-ultramafic soils and corresponding soil samples (n = 393 from ultramafic soils and n = 66 from non-ultramafic soils) from Kinabalu Park (Sabah, Malaysia). The data were geographically (Kinabalu Park) and edaphically (ultramafic soils) constrained. The inclusion of a relatively high proportion (approx. 14 %) of samples from hyperaccumulator species [with foliar concentrations of aluminium and nickel (Ni) >1000 μg g-1, cobalt, copper, chromium and zinc >300 μg g-1 or manganese (Mn) >10 mg g-1] allowed for hypothesis testing.
KEY RESULTS: Frequency distribution graphs for most elements [calcium (Ca), magnesium (Mg) and phosphorus (P)] were unimodal, although some were skewed left (Mg and Mn). The Ni frequency distribution was bimodal and the separation point for the two modes was between 250 and 850 μg g-1.
CONCLUSIONS: Accounting for statistical probability, the established empirical threshold value (>1000 μg g-1) remains appropriate. The two discrete modes for Ni indicate ecophysiologically distinct behaviour in plants growing in similar soils. This response is in contrast to Mn, which forms the tail of a continuous (approximately log-normal) distribution, suggestive of an extension of normal physiological processes.
Impacts of ultramafic outcrops in Peninsular Malaysia and Sabah on soil and water quality

Tashakor M, Modabberi S, van der Ent A, Echevarria G

Environ Monit Assess, 2018 May 08;190(6):333.
PMID: 29737421 DOI: 10.1007/s10661-018-6668-5

This study focused on the influence of ultramafic terrains on soil and surface water environmental chemistry in Peninsular Malaysia and in the State of Sabah also in Malaysia. The sampling included 27 soils from four isolated outcrops at Cheroh, Bentong, Bukit Rokan, and Petasih from Peninsular Malaysia and sites near Ranau in Sabah. Water samples were also collected from rivers and subsurface waters interacting with the ultramafic bodies in these study sites. Physico-chemical parameters (including pH, EC, CEC) as well as the concentration of major and trace elements were measured in these soils and waters. Geochemical indices (geoaccumulation index, enrichment factor, and concentration factor) were calculated. Al2O3 and Fe2O3 had relatively high concentrations in the samples. A depletion in MgO, CaO, and Na2O was observed as a result of leaching in tropical climate, and in relation to weathering and pedogenesis processes. Chromium, Ni, and Co were enriched and confirmed by the significant values obtained for Igeo, EF, and CF, which correspond to the extreme levels of contamination for Cr and high to moderate levels of contamination for Ni and Co. The concentrations of Cr, Ni, and Co in surface waters did not reflect the local geochemistry and were within the permissible ranges according to WHO and INWQS standards. Subsurface waters were strongly enriched by these elements and exceeded these standards. The association between Cr and Ni was confirmed by factor analysis. The unexpected enrichment of Cu in an isolated component can be explained by localized mineralization in Sabah.
Fulltext Actephila alanbakeri (Phyllanthaceae): a new nickel hyperaccumulating plant species from localised ultramafic outcrops in Sabah (Malaysia)

van der Ent A, van Balgooy M, van Welzen P

Bot Stud, 2015 Dec;57(1):6.
PMID: 28510791 DOI: 10.1186/s40529-016-0122-1

The Malaysian state of Sabah on the Island of Borneo is emerging as a hotspot for nickel hyperaccumulator species with at least 25 such species discovered to date. New discoveries of the hyperaccumulation trait in described taxa, as well as taxonomical novelties that are nickel hyperaccumulators, continue to be made. Here we describe a new nickel hyperaccumulating species of Actephila (Phyllanthaceae) originating from two known populations on ultramafic soils in Sabah. The most characteristic feature of Actephila alanbakeri are its knobbly fruits, but other diagnostic morphological characters are discussed and information about its ecology and rhizosphere and plant tissue chemistry is provided. This new species is one of the strongest known nickel hyperaccumulator plants in Southeast Asia with up to 14,700 μg g(-1) (1.47 %) nickel in its leaves. The occurrences of Actephila alanbakeri on just two sites, both of which lie outside protected areas and are disturbed by recurring forest fires, combined with the small total numbers of individuals, render this species Endangered (EN) on the basis of IUCN Red List Criteria.
Fulltext Phyllanthus rufuschaneyi: a new nickel hyperaccumulator from Sabah (Borneo Island) with potential for tropical agromining

Bouman R, van Welzen P, Sumail S, Echevarria G, Erskine PD, van der Ent A

Bot Stud, 2018 Mar 27;59(1):9.
PMID: 29589161 DOI: 10.1186/s40529-018-0225-y

BACKGROUND: Nickel hyperaccumulator plants are of much interest for their evolution and unique ecophysiology, and also for potential applications in agromining-a novel technology that uses plants to extract valuable metals from soil. The majority of nickel hyperaccumulators are known from ultramafic soils in tropical regions (Cuba, New Caledonia and Southeast Asia), and one genus, Phyllanthus (Phyllanthaceae), is globally the most represented taxonomic entity. A number of tropical Phyllanthus-species have the potential to be used as 'metal crops' in agromining operations mainly because of their ease in cultivation and their ability to attain high nickel concentrations and biomass yields.
RESULTS: One of the most promising species globally for agromining, is the here newly described species Phyllanthus rufuschaneyi. This species can be classified in subgenus Gomphidium on account of its staminate nectar disc and pistillate entire style and represents the most western species of this diverse group. The flower structure indicates that this species is probably pollinated by Epicephala moths.
CONCLUSIONS: Phyllanthus rufuschaneyi is an extremely rare taxon in the wild, restricted to Lompoyou Hill near Kinabalu Park in Sabah, Malaysia. Its utilization in agromining will be a mechanism for conservation of the taxon, and highlights the importance of habitat and germplasm preservation if rare species are to be used in novel green technologies.
Capture of mammal excreta by Nepenthes is an effective heterotrophic nutrition strategy

Cross AT, van der Ent A, Wickmann M, Skates LM, Sumail S, Gebauer G, et al.

Ann Bot, 2022 Dec 31;130(7):927-938.
PMID: 36306274 DOI: 10.1093/aob/mcac134

BACKGROUND AND AIMS: While isotopic enrichment of nitrogen (15N) and carbon (13C) is often used to determine whether carnivorous plant species capture and assimilate nutrients from supplemental sources such as invertebrate prey or mammal excreta (heterotrophic nutrition), little is known about how successful the different strategies deployed by carnivorous plants are at obtaining supplemental nutrition. The collection of mammalian faeces by Nepenthes (tropical pitcher plants) is the result of a highly specialized biological mutualism that results in heterotrophic nitrogen gain; however, it remains unknown how effective this strategy is in comparison to Nepenthes species not known to collect mammalian faeces.
METHODS: We examined how isotopic enrichment varied in the diverse genus Nepenthes, among species producing pitchers for invertebrate capture and species exhibiting mutualisms for the collection of mammal excreta. Enrichment factors were calculated from δ15N and δ13C values from eight Nepenthes species and naturally occurring hybrids along with co-occurring reference (non-carnivorous) plants from three mountain massifs in Borneo: Mount Kinabalu, Mount Tambuyukon and Mount Trus Madi.
RESULTS: All Nepenthes examined, except N. edwardsiana, were significantly enriched in 15N compared to co-occurring non-carnivorous plants, and 15N enrichment was more than two-fold higher in species with adaptations for the collection of mammal excreta compared with other Nepenthes.
CONCLUSIONS: The collection of mammal faeces clearly represents a highly effective strategy for heterotrophic nitrogen gain in Nepenthes. Species with adaptations for capturing mammal excreta occur exclusively at high elevation (i.e. are typically summit-occurring) where previous studies suggest invertebrate prey are less abundant and less frequently captured. As such, we propose this strategy may maximize nutritional return by specializing towards ensuring the collection and retention of few but higher-value N sources in environments where invertebrate prey may be scarce.
Fulltext Contrasting patterns of nickel distribution in the hyperaccumulators Phyllanthus balgooyi and Phyllanthus rufuschaneyi from Malaysian Borneo

van der Ent A, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Barnabas AD, de Jonge MD, Harris HH

Metallomics, 2022 May 13;14(5).
PMID: 35556136 DOI: 10.1093/mtomcs/mfac020

Globally, the majority of Ni hyperaccumulator plants occur on ultramafic soils in tropical regions, and the genus Phyllanthus, from the Phyllanthaceae family, is globally the most represented taxonomical group. Two species from Sabah (Malaysia) are remarkable because Phyllanthus balgooyi can attain >16 wt% of Ni in its phloem exudate, while Phyllanthus rufuschaneyi reaches foliar concentrations of up to 3.5 wt% Ni, which are amongst the most extreme concentrations of Ni in any plant tissue. Synchrotron X-ray fluorescence microscopy, nuclear microbe (micro-PIXE+BS) and (cryo) scanning electron microscopy with energy dispersive spectroscopy were used to spatially resolve the elemental distribution in the plant organs of P. balgooyi and P. rufuschaneyi. The results show that P. balgooyi has extraordinary enrichment of Ni in the (secondary) veins of the leaves, whereas in contrast, in P. rufuschaneyi Ni occurs in interveinal areas. In the roots and stems, Ni is localized mainly in the cortex and phloem but is much lower in the xylem. The findings of this study show that, even within the same genus, the distribution of nickel and other elements, and inferred processes involved with metal hyperaccumulation, can differ substantially between species.
Fulltext Simultaneous hyperaccumulation of nickel and cobalt in the tree Glochidion cf. sericeum (Phyllanthaceae): elemental distribution and chemical speciation

van der Ent A, Mak R, de Jonge MD, Harris HH

Sci Rep, 2018 Jun 26;8(1):9683.
PMID: 29946061 DOI: 10.1038/s41598-018-26891-7

Hyperaccumulation is generally highly specific for a single element, for example nickel (Ni). The recently-discovered hyperaccumulator Glochidion cf. sericeum (Phyllanthaceae) from Malaysia is unusual in that it simultaneously accumulates nickel and cobalt (Co) with up to 1500 μg g-1 foliar of both elements. We set out to determine whether distribution and associated ligands for Ni and Co complexation differ in this species. We postulated that Co hyperaccumulation coincides with Ni hyperaccumulation operating on similar physiological pathways. However, the ostensibly lower tolerance for Co at the cellular level results in the exudation of Co on the leaf surface in the form of lesions. The formation of such lesions is akin to phytotoxicity responses described for manganese (Mn). Hence, in contrast to Ni, which is stored principally inside the foliar epidermal cells, the accumulation response to Co consists of an extracellular mechanism. The chemical speciation of Ni and Co, in terms of the coordinating ligands involved and principal oxidation state, is similar and associated with carboxylic acids (citrate for Ni and tartrate or malate for Co) and the hydrated metal ion. Some oxidation to Co3+, presumably on the surface of leaves after exudation, was observed.
Fulltext Nickel stocks and fluxes in a tropical agromining 'metal crop' farming system in Sabah (Malaysia)

Tisserand R, van der Ent A, Nkrumah PN, Didier S, Sumail S, Morel JL, et al.

Sci Total Environ, 2024 Apr 01;919:170691.
PMID: 38325468 DOI: 10.1016/j.scitotenv.2024.170691

Nickel hyperaccumulator plants play a major role in nickel recycling in ultramafic ecosystems, and under agromining the nickel dynamics in the farming system will be affected by removal of nickel-rich biomass. We investigated the biogeochemical cycling of nickel as well as key nutrients in an agromining operation that uses the metal crop Phyllanthus rufuschaneyi in the first tropical metal farm located in Borneo (Sabah, Malaysia). For two years, this study monitored nine 25-m2 plots and collected information on weather, biomass exportation, water, and litter fluxes to the soil. Without harvesting, nickel inputs and outputs had only minor contributions (<1 %) to the total nickel budget in this system. The nickel cycle was mainly driven by internal fluxes, particularly plant uptake, litterfall and throughfall. After two years of cropping, the nickel litter flux corresponded to 50 % of the total nickel stock in the aerial biomass (3.1 g m-2 year-1). Nickel was slowly released from the litter; after 15 months of degradation, 60 % of the initial biomass and the initial nickel quantities were still present in the organic layer. Calcium, phosphorus and potassium budgets in the system were negative without fertilisation. Unlike what is observed for nickel, sustained agromining would thus lead to a strong depletion of calcium stocks if mineral weathering cannot replenish it.
Bacterial community diversity in the rhizosphere of nickel hyperaccumulator plant species from Borneo Island (Malaysia)

Lopez S, van der Ent A, Sumail S, Sugau JB, Buang MM, Amin Z, et al.

Environ Microbiol, 2020 04;22(4):1649-1665.
PMID: 32128926 DOI: 10.1111/1462-2920.14970

The Island of Borneo is a major biodiversity hotspot, and in the Malaysian state of Sabah, ultramafic soils are extensive and home to more than 31 endemic nickel hyperaccumulator plants. The aim of this study was to characterize the structure and the diversity of the rhizosphere bacterial communities of several of these nickel hyperaccumulator plants and factors that affect these bacterial communities in Sabah. The most abundant phyla were Proteobacteria, Acidobacteria and Actinobacteria. At family level, Burkholderiaceae and Xanthobacteraceae (Proteobacteria phylum) were the most abundant families in the hyperaccumulator rhizospheres. Redundancy analysis based on soil chemical analyses and relative abundances of the major bacterial phyla showed that abiotic factors of the studied sites drove the bacterial diversity. For all R. aff. bengalensis rhizosphere soil samples, irrespective of studied site, the bacterial diversity was similar. Moreover, the Saprospiraceae family showed a high representativeness in the R. aff. bengalensis rhizosphere soils and was linked with the nickel availability in soils. The ability of R. aff. bengalensis to concentrate nickel in its rhizosphere appears to be the major factor driving the rhizobacterial community diversity unlike for other hyperaccumulator species.
Fulltext Isotopic signatures reveal zinc cycling in the natural habitat of hyperaccumulator Dichapetalum gelonioides subspecies from Malaysian Borneo

van der Ent A, Nkrumah PN, Aarts MGM, Baker AJM, Degryse F, Wawryk C, et al.

BMC Plant Biol, 2021 Sep 27;21(1):437.
PMID: 34579652 DOI: 10.1186/s12870-021-03190-4

BACKGROUND: Some subspecies of Dichapetalum gelonioides are the only tropical woody zinc (Zn)-hyperaccumulator plants described so far and the first Zn hyperaccumulators identified to occur exclusively on non-Zn enriched 'normal' soils. The aim of this study was to investigate Zn cycling in the parent rock-soil-plant interface in the native habitats of hyperaccumulating Dichapetalum gelonioides subspecies (subsp. pilosum and subsp. sumatranum). We measured the Zn isotope ratios (δ66Zn) of Dichapetalum plant material, and associated soil and parent rock materials collected from Sabah (Malaysian Borneo).
RESULTS: We found enrichment in heavy Zn isotopes in the topsoil (δ66Zn 0.13 ‰) relative to deep soil (δ66Zn -0.15 ‰) and bedrock (δ66Zn -0.90 ‰). This finding suggests that both weathering and organic matter influenced the Zn isotope pattern in the soil-plant system, with leaf litter cycling contributing significantly to enriched heavier Zn in topsoil. Within the plant, the roots were enriched in heavy Zn isotopes (δ66Zn ~ 0.60 ‰) compared to mature leaves (δ66Zn ~ 0.30 ‰), which suggests highly expressed membrane transporters in these Dichapetalum subspecies preferentially transporting lighter Zn isotopes during root-to-shoot translocation. The shoots, mature leaves and phloem tissues were enriched in heavy Zn isotopes (δ66Zn 0.34-0.70 ‰) relative to young leaves (δ66Zn 0.25 ‰). Thisindicates that phloem sources are enriched in heavy Zn isotopes relative to phloem sinks, likely because of apoplastic retention and compartmentalization in the Dichapetalum subspecies.
CONCLUSIONS: The findings of this study reveal Zn cycling in the rock-soil-plant continuum within the natural habitat of Zn hyperaccumulating subspecies of Dichapetalum gelonioides from Malaysian Borneo. This study broadens our understanding of the role of a tropical woody Zn hyperaccumulator plant in local Zn cycling, and highlights the important role of leaf litter recycling in the topsoil Zn budget. Within the plant, phloem plays key role in Zn accumulation and redistribution during growth and development. This study provides an improved understanding of the fate and behaviour of Zn in hyperaccumulator soil-plant systems, and these insights may be applied in the biofortification of crops with Zn.
Fulltext Nickel biopathways in tropical nickel hyperaccumulating trees from Sabah (Malaysia)

van der Ent A, Callahan DL, Noller BN, Mesjasz-Przybylowicz J, Przybylowicz WJ, Barnabas A, et al.

Sci Rep, 2017 Feb 16;7:41861.
PMID: 28205587 DOI: 10.1038/srep41861

The extraordinary level of accumulation of nickel (Ni) in hyperaccumulator plants is a consequence of specific metal sequestering and transport mechanisms, and knowledge of these processes is critical for advancing an understanding of transition element metabolic regulation in these plants. The Ni biopathways were elucidated in three plant species, Phyllanthus balgooyi, Phyllanthus securinegioides (Phyllanthaceae) and Rinorea bengalensis (Violaceae), that occur in Sabah (Malaysia) on the Island of Borneo. This study showed that Ni is mainly concentrated in the phloem in roots and stems (up to 16.9% Ni in phloem sap in Phyllanthus balgooyi) in all three species. However, the species differ in their leaves - in P. balgooyi the highest Ni concentration is in the phloem, but in P. securinegioides and R. bengalensis in the epidermis and in the spongy mesophyll (R. bengalensis). The chemical speciation of Ni2+ does not substantially differ between the species nor between the plant tissues and transport fluids, and is unambiguously associated with citrate. This study combines ion microbeam (PIXE and RBS) and metabolomics techniques (GC-MS, LC-MS) with synchrotron methods (XAS) to overcome the drawbacks of the individual techniques to quantitatively determine Ni distribution and Ni2+ chemical speciation in hyperaccumulator plants.

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