When plants are subjected to high metal exposure, different plant species take different strategies in response to metal-induced stress. Largely, plants can be distinguished in four groups: ...metal-sensitive species, metal-resistant excluder species, metal-tolerant non-hyperaccumulator species, and metal-hypertolerant hyperaccumulator species, each having different molecular mechanisms to accomplish their resistance/tolerance to metal stress or reduce the negative consequences of metal toxicity. Plant responses to heavy metals are molecularly regulated in a process called metal homeostasis, which also includes regulation of the metal-induced reactive oxygen species (ROS) signaling pathway. ROS generation and signaling plays an important duel role in heavy metal detoxification and tolerance. In this review, we will compare the different molecular mechanisms of nutritional (Zn) and non-nutritional (Cd) metal homeostasis between metal-sensitive and metal-adapted species. We will also include the role of metal-induced ROS signal transduction in this comparison, with the aim to provide a comprehensive overview on how plants cope with Zn/Cd stress at the molecular level.
Zinc in plants Broadley, Martin R.; White, Philip J.; Hammond, John P. ...
The New phytologist,
March 2007, Volume:
173, Issue:
4
Journal Article
Peer reviewed
Contents
Summary 677
I.
Physical and chemical properties of zinc 678
II.
Biochemical properties of zinc 678
III.
Proteins interacting with zinc 678
IV.
Zinc fluxes in the soil–root–shoot ...continuum 679
V.
Zinc in plants 684
VI.
Plant responses to elevated soil Zn 686
Acknowledgements 695
References 696
Summary
Zinc (Zn) is an essential component of thousands of proteins in plants, although it is toxic in excess. In this review, the dominant fluxes of Zn in the soil–root–shoot continuum are described, including Zn inputs to soils, the plant availability of soluble Zn2+ at the root surface, and plant uptake and accumulation of Zn. Knowledge of these fluxes can inform agronomic and genetic strategies to address the widespread problem of Zn‐limited crop growth. Substantial within‐species genetic variation in Zn composition is being used to alleviate human dietary Zn deficiencies through biofortification. Intriguingly, a meta‐analysis of data from an extensive literature survey indicates that a small proportion of the genetic variation in shoot Zn concentration can be attributed to evolutionary processes whose effects manifest above the family level. Remarkable insights into the evolutionary potential of plants to respond to elevated soil Zn have recently been made through detailed anatomical, physiological, chemical, genetic and molecular characterizations of the brassicaceous Zn hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri.
We report here the first purification of a P sub(1) sub(B) type ATPase, a group of transporters that occurs in bacteria, plants and animals incl. humans, from a eukaryotic organism in native state. ...TcHMA4 is a P sub(1) sub(B) type ATPase that is highly expressed in the Cd/Zn hyperaccumulator plant Thlaspi caerulescens and contains a C-terminal 9-histidine repeat. After isolation from roots, we purified TcHMA4 protein via metal affinity chromatography. The purified protein exhibited Cd- and Zn-activated ATPase activity after reconstitution into lipid vesicles, showing that it was in its native state. Gels of crude root extract and of the purified protein revealed TcHMA4-specific bands of about 50 and 60kDa, respectively, while the TcHMA4 mRNA predicts a single protein with a size of 128kDa. This indicates the occurrence of post-translational processing; the properties of the two bands were characterised by their activity and binding properties.
Changes in the fatty acid (FAs) composition in response to the extent of Cd contamination of soils (0, 30, 60 and 90mgCdkg−1) differed between ecotypes of Noccaea caerulescens originating from France ...– Ganges, Slovenia – Mežica and Austria – Redlschlag. Mežica ecotype accumulated more Cd in aboveground biomass compared to Ganges and Redlschlag ecotypes. Hyperaccumulators contained saturated fatty acids (SFAs) rarely occurring in plants, as are cerotic (26:0), montanic (28:0), melissic (30:0) acids, and unusual unsaturated fatty acids (USFAs), as are 16:2, 16:3, 20:2 and 20:3. Typical USFAs occurring in the family Brassicaceae, such as erucic, oleic and arachidonic acids, were missing in tested plants. Our results clearly indicate a relationship between Cd accumulation and the FAs composition. The content of SFAs decreased and the content of USFAs increased in aboveground biomass of Ganges and Mežica ecotypes with increasing Cd concentration. Opposite trend of FAs content was determined in Redlschlag ecotype. Linoleic (18:2n−6), α-linolenic (18:3n−3) and palmitic (16:0) acids were found in all ecotypes. The results observed in N. caerulescens ecotypes, showed that mainly Mežica ecotype has an efficient defense strategies which can be related on changes in FAs composition, mainly in VLCFAs synthesis. The most significant effect of ecotype on FAs composition was confirmed using multivariate analysis of variance.
Metal hyperaccumulation is a trait present in over 450 higher plant species. Hyperaccumulators are also tolerant to metals, but hyperaccumulation and tolerance are genetically independent traits. The ...ecological and biological significance of hyperaccumulation is not clear yet. To provide new insights, this review examines recent literature, in particular focusing on the Cd and Zn hyperaccumulator species
Arabidopsis halleri (L.) O’Kane and Al Shehbaz and
Thlaspi caerulescens J. et C. Presl. in comparison with the model plant species
Arabidopsis thaliana (L.) Heynh. The main aspects considered in the discussion on hyperaccumulation and tolerance involve: (i) uptake of metals, (ii) vacuolar sequestration, (iii) xylem loading, and (iv) chelation with ligands. The review discusses the advancement of knowledge obtained through genetic analysis and molecular biology, together with the use of transgenic approaches and transcriptomics. The most important genes which have been correlated to hyperaccumulation and tolerance in plant species are described and discussed. From the in depth analysis of published results, the main topics for future research are highlighted. Ecological relevance of the hyperaccumulation and tolerance traits in the environment is discussed, with the advantages they can confer to individuals, the possible disadvantages, and the trade-offs between these genetic traits and the environmental conditions.
The metal hyperaccumulator Noccaea caerulescens is an established model to study the adaptation of plants to metalliferous soils. Various comparators have been used in these studies. The choice of ...suitable comparators is important and depends on the hypothesis to be tested and methods to be used. In high-throughput analyses such as microarray, N. caerulescens has been compared to non-tolerant, non-accumulator plants like Arabidopsis thaliana or Thlaspi arvense rather than to the related hypertolerant or hyperaccumulator plants. An underutilized source is N. caerulescens populations with considerable variation in their capacity to accumulate and tolerate metals. Whole transcriptome sequencing (RNA-Seq) is revealing interesting variation in their gene expression profiles. Combining physiological characteristics of N. caerulescens accessions with their RNA-Seq has a great potential to provide detailed insight into the underlying molecular mechanisms, including entirely new gene products. In this review we will critically consider comparative transcriptome analyses carried out to explore metal hyperaccumulation and hypertolerance of N. caerulescens, and demonstrate the potential of RNA-Seq analysis as a tool in evolutionary genomics.
Cadmium (Cd) is a heavy metal that is of great concern in the environment, because of its toxicity to animals and humans. This article reviews recent papers showing how soil factors (such as pH, ...phosphate, zinc, and organic matter), Cd hyperaccumulation, and soil amendments affect Cd availability. The studies confirm that the pH of the soil is usually the most important factor that controls uptake, with low pH favoring Cd accumulation, and that phosphate and zinc decrease Cd uptake. The work reveals that the availability of Cd is increased by the application of chloride and reduced by application of silicon. The most striking result of this review is the elevated levels of Cd in plants that are being reported in recent studies. Data for concentrations of Cd in soils and plants under variously polluted conditions are presented in a table and show that all plants have Cd concentrations ≥
0.1 mg/kg, the normal concentration in plants. Concentrations ranged from two low concentrations of 0.1 mg/kg Cd (in grain of corn,
Zea mays, on an abandoned sludge disposal site that had not received sludge for 10 years, and in roots of hybrid poplar,
Populus deltoides x P. nigra, at a 25-year old active sludge farm) to 380 mg/kg Cd in leaves of penny-cress (
Thlaspi caerulescens). Plants that hyperaccumulate Cd (i.e., have 100 mg/kg Cd in the tissue or more) belong to the genus
Thalspi, the only known Cd hyperaccumulator. Of particular concern for humans are the high concentrations of Cd in rice grain and tobacco leaves. Even if Cd availability is decreased by adding amendments, it is still in the soil and a potential hazard. The best solution for maintaining non-contaminated soils and plants is to remove the sources of Cd in the environment. Given that that is essentially impossible at this time, further research needs to determine how soil and plant factors affect Cd availability on polluted soils.
Prompt regulation of transition metal transporters is crucial for plant zinc homeostasis. NcZNT1 is one of such transporters, found in the metal hyperaccumulator Brassicaceae species Noccaea ...caerulescens. It is orthologous to AtZIP4 from Arabidopsis thaliana, an important actor in Zn homeostasis. We examined if the NcZNT1 function contributes to the metal hyperaccumulation of N. caerulescens. NcZNT1 was found to be a plasma-membrane located metal transporter. Constitutive overexpression of NcZNT1 in A. thaliana conferred enhanced tolerance to exposure to excess Zn and Cd supply, as well as increased accumulation of Zn and Cd and induction of the Fe deficiency response, when compared to non-transformed wild-type plants. Promoters of both genes were induced by Zn deficiency in roots and shoots of A. thaliana. In A. thaliana, the AtZIP4 and NcZNT1 promoters were mainly active in cortex, endodermis and pericycle cells under Zn deficient conditions. In N. caerulescens, the promoters were active in the same tissues, though the activity of the NcZNT1 promoter was higher and not limited to Zn deficient conditions. Common cis elements were identified in both promoters by 5' deletion analysis. These correspond to the previously determined Zinc Deficiency Responsive Elements found in A. thaliana to interact with two redundantly acting transcription factors, bZIP19 and bZIP23, controlling the Zn deficiency response. In conclusion, these results suggest that NcZNT1 is an important factor in contributing to Zn and Cd hyperaccumulation in N. caerulescens. Differences in cis- and trans-regulators are likely to account for the differences in expression between A. thaliana and N. caerulescens. The high, constitutive NcZNT1 expression in the stele of N. caerulescens roots implicates its involvement in long distance root-to-shoot metal transport by maintaining a Zn/Cd influx into cells responsible for xylem loading.
Nitrate has been shown to enhance Zn hyperaccumulation in the shoots of Noccaea caerulescens (formerly Thlaspi caerulescens) (Prayon); however, the mechanisms beyond the effect of nitrogen form are ...unknown. This study used synchrotron X-ray absorption near-edge spectroscopy (XANES) on alive and intact plants at room temperature to examine whether enhanced Zn hyperaccumulation in nitrate-fed plants was associated with differences in Zn speciation, and to correlate Zn species with mechanisms of Zn uptake, translocation and hyperaccumulation. The higher Zn concentration in plants supplied with nitrate compared to ammonium, or with high Zn exposure (300 μM), was not due to differences in Zn speciation. The importance of carboxylates for Zn hyperaccumulation in the shoots was supported by a predominance of Zn-malate or Zn-citrate. Zinc-phytate was detected for the first time in this species and may assist Zn-tolerance in the roots. The feasible presence of Zn-histidine in the roots but not in the xylem sap suggests a mechanism for Zn binding and non-toxic transport through the cytoplasm and release of aqueous Zn into the xylem vessels. Zinc was translocated in the xylem as Zn-malate and weakly complexed or aqueous Zn forms. Zinc speciation in roots, shoots and xylem did not differ between nitrate- and ammonium-fed plants.
Summary
Calamine accessions of the zinc/cadmium/nickel hyperaccumulator, Noccaea caerulescens, exhibit striking variation in foliar cadmium accumulation in nature. The Ganges accession (GA) from ...Southern France displays foliar cadmium hyperaccumulation (>1000 μg g−1 DW), whereas the accession La Calamine (LC) from Belgium, with similar local soil metal composition, does not (<100 μg g−1 DW). All calamine accessions are cadmium hypertolerant. To find out the differences between LC and GA in their basic adaptation mechanisms, we bypassed the cadmium excluding phenotype of LC by exposing the plants to 50 μm cadmium in hydroponics, achieving equal cadmium accumulation in the shoots. The iron content increased in the roots of both accessions. GA exhibited significant decreases in manganese and zinc contents in the roots and shoots, approaching those in LC. Altogether 702 genes responded differently to cadmium exposure between the accessions, 157 and 545 in the roots and shoots, respectively. Cadmium‐exposed LC showed a stress response and had decreased levels of a wide range of photosynthesis‐related transcripts. GA showed less changes, mainly exhibiting an iron deficiency‐like response. This included increased expression of genes encoding five iron deficiency‐regulated bHLH transcription factors, ferric reduction oxidase FRO2, iron transporters IRT1 and OPT3, and nicotianamine synthase NAS1, and decreased expression of genes encoding ferritins and NEET (a NEET family iron‐sulfur protein), which is possibly involved in iron transfer, distribution and/or management. The function of the IRT1 gene in the accessions was compared. We conclude that the major difference between the two accessions is in the way they cope with iron under cadmium exposure.
Significance statement
Both the cadmium hyperaccumulator and the cadmium excluder Noccaea caerulescens of the ‘cabbage’ family (Brassicaceae) can have a full capacity to accumulate cadmium under certain conditions, while exhibiting major differences in their transcriptome response. This study highlights the critical importance of understanding the mechanisms of metal accumulation in order to prevent the uptake of toxic metals and maintain proper metal homeostasis in crops cultivated in contaminated soils and also in the increasingly popular hydroponic systems.
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