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.
The zinc homeostasis network of land plants Sinclair, Scott Aleksander; Krämer, Ute
Biochimica et biophysica acta,
September 2012, 2012-Sep, 2012-09-00, Letnik:
1823, Številka:
9
Journal Article
Recenzirano
Odprti dostop
The use of the essential element zinc (Zn) in the biochemistry of land plants is widespread, and thus comparable to that in other eukaryotes. Plants have evolved the ability to adjust to vast ...fluctuations in external Zn supply, and they can store considerable amounts of Zn inside cell vacuoles. Moreover, among plants there is overwhelming, but yet little explored, natural genetic diversity that phenotypically affects Zn homeostasis. This results in the ability of specific races or species to thrive in different soils ranging from extremely Zn-deficient to highly Zn-polluted. Zn homeostasis is maintained by a tightly regulated network of low-molecular-weight ligands, membrane transport and Zn-binding proteins, as well as regulators. Here we review Zn homeostasis of land plants largely based on the model plant Arabidopsis thaliana, for which our molecular understanding is most developed at present. There is some evidence for substantial conservation of Zn homeostasis networks among land pants, and this review can serve as a reference for future comparisons. Major progress has recently been made in our understanding of the regulation of transcriptional Zn deficiency responses and the role of the low-molecular-weight chelator nicotianamine in plant Zn homeostasis. Moreover, we have begun to understand how iron (Fe) and Zn homeostasis interact as a consequence of the chemical similarity between their divalent cations and the lack of specificity of the major root iron uptake transporter IRT1. The molecular analysis of Zn-hyperaccumulating plants reveals how metal homeostasis networks can be effectively modified. These insights are important for sustainable bio-fortification approaches. This article is part of a Special Issue entitled: Cell Biology of Metals.
► Zn homeostasis factors ► Zn deficiency response regulator ► systemic signalling ► Novel imaging tools
The metal hyperaccumulator Arabidopsis halleri exhibits naturally selected zinc (Zn) and cadmium (Cd) hypertolerance and accumulates extraordinarily high Zn concentrations in its leaves. With these ...extreme physiological traits, A. halleri phylogenetically belongs to the sister clade of Arabidopsis thaliana. Using a combination of genome-wide cross species microarray analysis and real-time reverse transcription-PCR, a set of candidate genes is identified for Zn hyperaccumulation, Zn and Cd hypertolerance, and the adjustment of micronutrient homeostasis in A. halleri. Eighteen putative metal homeostasis genes are newly identified to be more highly expressed in A. halleri than in A. thaliana, and 11 previously identified candidate genes are confirmed. The encoded proteins include HMA4, known to contribute to root-shoot transport of Zn in A. thaliana. Expression of either AtHMA4 or AhHMA4 confers cellular Zn and Cd tolerance to yeast (Saccharomyces cerevisiae). Among further newly implicated proteins are IRT3 and ZIP10, which have been proposed to contribute to cytoplasmic Zn influx, and FRD3 required for iron partitioning in A. thaliana. In A. halleri, the presence of more than a single genomic copy is a hallmark of several highly expressed candidate genes with possible roles in metal hyperaccumulation and metal hypertolerance. Both A. halleri and A. thaliana exert tight regulatory control over Zn homeostasis at the transcript level. Zn hyperaccumulation in A. halleri involves enhanced partitioning of Zn from roots into shoots. The transcriptional regulation of marker genes suggests that in the steady state, A. halleri roots, but not the shoots, act as physiologically Zn deficient under conditions of moderate Zn supply.
The vascular plant Arabidopsis thaliana is a central genetic model and universal reference organism in plant and crop science. The successful integration of different fields of research in the study ...of A. thaliana has made a large contribution to our molecular understanding of key concepts in biology. The availability and active development of experimental tools and resources, in combination with the accessibility of a wealth of cumulatively acquired knowledge about this plant, support the most advanced systems biology approaches among all land plants. Research in molecular ecology and evolution has also brought the natural history of A. thaliana into the limelight. This article showcases our current knowledge of the natural history of A. thaliana from the perspective of the most closely related plant species, providing an evolutionary framework for interpreting novel findings and for developing new hypotheses based on our knowledge of this plant.
Leaf mineral composition, the leaf ionome, reflects the complex interaction between a plant and its environment including local soil composition, an influential factor that can limit species ...distribution and plant productivity. Here we addressed within-species variation in plant–soil interactions and edaphic adaptation using Arabidopsis halleri, a well-suited model species as a facultative metallophyte and metal hyperaccumulator.
We conducted multi-element analysis of 1972 paired leaf and soil samples from 165 European populations of A. halleri, at individual resolution to accommodate soil heterogeneity. Results were further confirmed under standardized conditions upon cultivation of 105 field-collected genotypes on an artificially metal-contaminated soil in growth chamber experiments.
Soil-independent between- and within-population variation set apart leaf accumulation of zinc, cadmium and lead from all other nutrient and nonessential elements, concurring with differential hypothesized ecological roles in either biotic interaction or nutrition. For these metals, soil–leaf relationships were element-specific, differed between metalliferous and non-metalliferous soils and were geographically structured both in the field and under standardized growth conditions, implicating complex scenarios of recent ecological adaptation.
Our study provides an example and a reference for future related work and will serve as a basis for the molecular–genetic dissection and ecological analysis of the observed phenotypic variation.
Little is known about the types of mutations underlying the evolution of species-specific traits. The metal hyperaccumulator Arabidopsis halleri has the rare ability to colonize heavy-metal-polluted ...soils, and, as an extremophile sister species of Arabidopsis thaliana, it is a powerful model for research on adaptation. A. halleri naturally accumulates and tolerates leaf concentrations as high as 2.2% zinc and 0.28% cadmium in dry biomass. On the basis of transcriptomics studies, metal hyperaccumulation in A. halleri has been associated with more than 30 candidate genes that are expressed at higher levels in A. halleri than in A. thaliana. Some of these genes have been genetically mapped to broad chromosomal segments of between 4 and 24 cM co-segregating with Zn and Cd hypertolerance. However, the in planta loss-of-function approaches required to demonstrate the contribution of a given candidate gene to metal hyperaccumulation or hypertolerance have not been pursued to date. Using RNA interference to downregulate HMA4 (HEAVY METAL ATPASE 4) expression, we show here that Zn hyperaccumulation and full hypertolerance to Cd and Zn in A. halleri depend on the metal pump HMA4. Contrary to a postulated global trans regulatory factor governing high expression of numerous metal hyperaccumulation genes, we demonstrate that enhanced expression of HMA4 in A. halleri is attributable to a combination of modified cis-regulatory sequences and copy number expansion, in comparison to A. thaliana. Transfer of an A. halleri HMA4 gene to A. thaliana recapitulates Zn partitioning into xylem vessels and the constitutive transcriptional upregulation of Zn deficiency response genes characteristic of Zn hyperaccumulators. Our results demonstrate the importance of cis-regulatory mutations and gene copy number expansion in the evolution of a complex naturally selected extreme trait. The elucidation of a natural strategy for metal hyperaccumulation enables the rational design of technologies for the clean-up of metal-contaminated soils and for bio-fortification.
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•The presence of heavy metals may shape plant-herbivore interactions.•We investigated the effects of soil Cd and Zn on herbivore and plant responses.•Chewing and sucking herbivores ...are negatively impacted by metal (hyper)accumulation.•Leaf glucosinolates and elements respond differently to soil-treatment and herbivory.•Most glucosinolates and elements are higher in young leaves in line with the optimal defense theory.
Abiotic and biotic factors can significantly influence and modify the chemical composition of a plant. In this study the influences of exposure to cadmium and zinc and of herbivory on plant-insect interactions were investigated. We studied the performance of two herbivore species with different feeding modes (chewing versus sucking) on the metal-hyperaccumulator species Arabidopsis halleri (Brassicaceae) as well as individual glucosinolate (GLS) and element concentrations of young and old leaves in response to different soil and herbivore treatments. The performance of both insect species was reduced on plants grown on metal-amended soil compared to plants grown on unamended soil. This result supports the elemental defense hypothesis, which postulates that high internal metal concentrations can protect plants from herbivores and which was mostly tested with chewing herbivores so far. Alongside higher levels of heavy metals in plants grown on metal-amended soil, GLS and element concentrations were differentially affected in young versus old leaves and responded differently to herbivory. Concentrations of most GLS and elements were higher in young compared to old leaves, which is in line with the optimal defense theory, which predicts a better defense in more valuable tissue. Our results highlight that various organic as well as inorganic compounds in plants can be affected in different directions by the complex interplay between plants, herbivores, and heavy metal contamination of soil.
The notion of species as reproductively isolated units related through a bifurcating tree implies that gene trees should generally agree with the species tree and that sister taxa should not share ...polymorphisms unless they diverged recently and should be equally closely related to outgroups. It is now possible to evaluate this model systematically. We sequenced multiple individuals from 27 described taxa representing the entire Arabidopsis genus. Cluster analysis identified seven groups, corresponding to described species that capture the structure of the genus. However, at the level of gene trees, only the separation of Arabidopsis thaliana from the remaining species was universally supported, and, overall, the amount of shared polymorphism demonstrated that reproductive isolation was considerably more recent than the estimated divergence times. We uncovered multiple cases of past gene flow that contradict a bifurcating species tree. Finally, we showed that the pattern of divergence differs between gene ontologies, suggesting a role for selection.
Zinc ions are required to maintain the biological activity of numerous proteins. However, when mislocalized or accumulated in excess, Zn²⁺ ions are toxic because of adventitious binding to proteins ...and displacement of other metal ions, among them Fe²⁺, from their binding sites. Heterologous expression of a previously uncharacterized Arabidopsis thaliana metal tolerance protein, MTP3, in the zrc1 cot1 mutant of budding yeast restores tolerance to, and cellular accumulation of, zinc and cobalt. An MTP3-GFP fusion protein localizes to the vacuolar membrane when expressed in Arabidopsis. Ectopic over-expression of MTP3 increases Zn accumulation in both roots and rosette leaves of A. thaliana, and enhances Zn tolerance. Exposure of wild-type plants to high but non-toxic concentrations of Zn or Co, or Fe deficiency, strongly induce MTP3 expression specifically in epidermal and cortex cells of the root hair zone. Silencing of MTP3 by RNA interference causes Zn hypersensitivity and enhances Zn accumulation in above-ground organs of soil-grown plants and of seedlings exposed to excess Zn or to Fe deficiency. Our data indicate that, in wild-type A. thaliana, the AtMTP3 protein contributes to basic cellular Zn tolerance and controls Zn partitioning, particularly under conditions of high rates of Zn influx into the root symplasm.
Abstract
The mineral micronutrients zinc (Zn) and iron (Fe) are essential for plant growth and human nutrition, but interactions between the homeostatic networks of these two elements are not fully ...understood. Here we show that loss of function of BTSL1 and BTSL2, which encode partially redundant E3 ubiquitin ligases that negatively regulate Fe uptake, confers tolerance to Zn excess in Arabidopsis thaliana. Double btsl1 btsl2 mutant seedlings grown on high Zn medium accumulated similar amounts of Zn in roots and shoots to the wild type, but suppressed the accumulation of excess Fe in roots. RNA-sequencing analysis showed that roots of mutant seedlings had relatively higher expression of genes involved in Fe uptake (IRT1, FRO2, and NAS) and in Zn storage (MTP3 and ZIF1). Surprisingly, mutant shoots did not show the transcriptional Fe deficiency response which is normally induced by Zn excess. Split-root experiments suggested that within roots the BTSL proteins act locally and downstream of systemic Fe deficiency signals. Together, our data show that constitutive low-level induction of the Fe deficiency response protects btsl1 btsl2 mutants from Zn toxicity. We propose that BTSL protein function is disadvantageous in situations of external Zn and Fe imbalances, and formulate a general model for Zn–Fe interactions in plants.
Mutation of two E3 ligases that suppress iron uptake in roots also confers tolerance to zinc toxicity, identifying a regulatory point of interaction between iron and zinc homeostasis.
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