Isotopic signatures reveal zinc cycling in the natural habitat of hyperaccumulator Dichapetalum gelonioides subspecies from Malaysian Borneo

Mark G M Aarts,Philip Nti Nkrumah,Antony Van Der Ent,Fien Degryse,Chris Wawryk,Alan J M Baker,Jason K Kirby

doi:10.1186/s12870-021-03190-4

Abstract

BackgroundSome 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).ResultsWe 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.ConclusionsThe 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.

Highlights

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 phloem tissue was preferentially enriched in heavy Zn isotopes (δ66Zn 0.72–0.77 ‰) compared to all plant parts
Our findings reveal that the Zinc isotope ratio (δ66Zn) values of the soil profile in the native habitat of Dichapetalum subspecies decrease with soil depth, and the decrease is especially pronounced between the bedrock and soil, suggesting that both chemical weathering and organic matter decomposition in this habitat lead to Zn fractionation (Jouvin et al 2009; Moynier et al 2017; Opfergelt et al 2017; Viers et al 2015)

Summary

Introduction

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 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 ‰). For zinc (Zn), the notional hyperaccumulation threshold is set at 3000 μg g− 1 (Krämer et al 2007; van der Ent et al 2013) This contrasts with Zn concentrations in most non-hyperaccumulator plant species that are typically between 30 and 100 μg g− 1 (Nouvas et al 2018). Arabidopsis halleri and N. caerulescens are the two key model species for the study of Zn hyperaccumulation and their ecology, physiology, molecular biology and genetics have broadened our understanding of metal regulation in plants (Bert et al 2000; Assunção et al 2003; Schwartz et al 2003; Lin et al 2014; Stein et al 2017; Ricachenevsky et al 2021)

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