Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri.
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ABSTRACT:
SUBMITTER: Meyer CL
PROVIDER: S-EPMC4449548 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:In Arabidopsis halleri, the HMA4 gene has an essential function in Zn/Cd hypertolerance and hyperaccumulation by mediating root-to-shoot translocation of metals. Constitutive high expression of AhHMA4 results from a tandem triplication and cis-activation of the promoter of all three copies. The three AhHMA4 copies possess divergent promoter sequences, but highly conserved coding sequences, and display identical expression profiles in the root and shoot vascular system. Here, an AhHMA4::GFP fusion was expressed under the control of each of the three A. halleri HMA4 promoters in a hma2hma4 double mutant of A. thaliana to individually examine the function of each AhHMA4 copy. The protein showed non-polar localization at the plasma membrane of the root pericycle cells of both A. thaliana and A. halleri. The expression of each AhHMA4::GFP copy complemented the severe Zn-deficiency phenotype of the hma2hma4 mutant by restoring root-to-shoot translocation of Zn. However, each copy had a different impact on metal homeostasis in the A. thaliana genetic background: AhHMA4 copies 2 and 3 were more highly expressed and provided higher Zn tolerance in roots and accumulation in shoots than copy 1, and AhHMA4 copy 3 also increased Cd tolerance in roots. These data suggest a certain extent of functional differentiation among the three A. halleri HMA4 copies, stemming from differences in expression levels rather than in expression profile. HMA4 is a key node of the Zn homeostasis network and small changes in expression level can have a major impact on Zn allocation to root or shoot tissues.
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Project description: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.
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Project description:Anthropogenic activities are among the main drivers of global change and result in drastic habitat modifications, which represent strong evolutionary challenges for biological species that can either migrate, adapt, or disappear. In this context, understanding the genetics of adaptive traits is a prerequisite to enable long-term maintenance of populations under strong environmental constraints. To examine these processes, a QTL approach was developed here using the pseudometallophyte Arabidopsis halleri, which displays among-population adaptive divergence for tolerance to metallic pollution in soils. An F2 progeny was obtained by crossing individuals from metallicolous and non-metallicolous populations from Italian Alps, where intense metallurgic activities have created strong landscape heterogeneity. Then, we combined genome de novo assembly and genome resequencing of parental genotypes to obtain single-nucleotide polymorphism markers and achieve high-throughput genotyping of the progeny. QTL analysis was performed using growth parameters and photosynthetic yield to assess zinc tolerance levels. One major QTL was identified for photosynthetic yield. It explained about 27% of the phenotypic variance. Functional annotation of the QTL and gene expression analyses highlighted putative candidate genes. Our study represents a successful approach combining evolutionary genetics and advanced molecular tools, helping to better understand how a species can face new selective pressures of anthropogenic origin.
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Project description:Cardamine violifolia (family Brassicaceae) is the first discovered selenium hyperaccumulator from the genus Cardamine with unique properties in terms of selenium accumulation, i.e., high abundance of selenolanthionine. In our study, a fully comprehensive experiment was conducted with the comparison of a non-hyperaccumulator Cardamine species, Cardamine pratensis, covering growth characteristics, chlorophyll fluorescence, spatial selenium/sulfur distribution patterns through elemental analyses (synchrotron-based X-Ray Fluorescence and ICP-OES) and speciation data through selenium K-edge micro X-ray absorption near-edge structure analysis (?XANES) and strong cation exchange (SCX)-ICP-MS. The results revealed remarkable differences in contrast to other selenium hyperaccumulators as neither Cardamine species showed evidence of growth stimulation by selenium. Also, selenite uptake was not inhibited by phosphate for either of the Cardamine species. Sulfate inhibited selenate uptake, but the two Cardamine species did not show any difference in this respect. However, ?XRF derived speciation maps and selenium/sulfur uptake characteristics provided results that are similar to other formerly reported hyperaccumulator and non-hyperaccumulator Brassicaceae species. ?XANES showed organic selenium, "C-Se-C", in seedlings of both species and also in mature C. violifolia plants. In contrast, selenate-supplied mature C. pratensis contained approximately half "C-Se-C" and half selenate. SCX-ICP-MS data showed evidence of the lack of selenocystine in any of the Cardamine plant extracts. Thus, C. violifolia shows clear selenium-related physiological and biochemical differences compared to C. pratensis and other selenium hyperaccumulators.
| S-EPMC7060786 | biostudies-literature
Project description:Engineering enhanced transport of zinc to the aerial parts of plants is a major goal in bio-fortification. In Arabidopsis halleri, high constitutive expression of the AhHMA4 gene encoding a metal pump of the P(1B)-ATPase family is necessary for both Zn hyperaccumulation and the full extent of Zn and Cd hypertolerance that are characteristic of this species. In this study, an AhHMA4 cDNA was introduced into N. tabacum var. Xanthi for expression under the control of its endogenous A. halleri promoter known to confer high and cell-type specific expression levels in both A. halleri and the non-hyperaccumulator A. thaliana. The transgene was expressed at similar levels in both roots and shoots upon long-term exposure to low Zn, control, and increased Zn concentrations. A down-regulation of AhHMA4 transcript levels was detected with 10 muM Zn resupply to tobacco plants cultivated in low Zn concentrations. In general, a transcriptional regulation of AhHMA4 in tobacco contrasted with the constitutively high expression previously observed in A. halleri. Differences in root/shoot partitioning of Zn and Cd between transgenic lines and the wild type were strongly dependent on metal concentrations in the hydroponic medium. Under low Zn conditions, an increased Zn accumulation in the upper leaves in the AhHMA4-expressing lines was detected. Moreover, transgenic plants exposed to cadmium accumulated less metal than the wild type. Both modifications of zinc and cadmium accumulation are noteworthy outcomes from the biofortification perspective and healthy food production. Expression of AhHMA4 may be useful in crops grown on soils poor in Zn.
| S-EPMC2892146 | biostudies-literature
Project description:This application is from a NERC-funded consortium (Mark MacNair, Nick Smirnoff, Exeter) and (Brian Ford-Lloyd, John Newbury, Birmingham). Metal tolerance is one of the classic examples of micro-evolution. Despite extensive research the physiological bases of the adaptation in plants are largely unknown. Arabidopsis halleri is a zinc tolerant, zinc accumulating species whereas Arabidopsis petraea is non-accumulating and non-tolerant. The objective of our programme is to identify: a) those key genes that act to determine Zn tolerance and accumulation in Arabidopsis (and which account for the difference in performance of A. halleri and A. petraea grown in the presence of elevated Zn), and b) those _downstream_ genes that are expressed as part of the tolerance or accumulation response. Phase 1: Total of 24 chips: Material ready by May 2003. The results will: a) tell us how effectively material derived from other Arabidopsis species hybridises to the chips, and b) identify genes that are differentially expressed in the two species in the presence and absence of Zn stress (thus providing initial lists of genes that may be responsible for Zn tolerance or accumulation- (but see phase 2). A. halleri exposed to low and high Zn; root and leaf mRNAs extracted: 3 replicates of each: = 12 slides. A. petraea exposed to low and high Zn; root and leaf mRNAs extracted: 3 replicates of each: = 12 slides. Phase 2: Total of 48 chips: Material ready by September 2003. The results will tell us which genes, identified as having appropriate expression patterns, co-segregate with the Zn tolerance or accumulation phenotype and will provide firmer candidate genes for intensive study. Bulks will be produced from F3 progeny (from the halleri x petraea cross) following phentoypic analyses for Zn tolerance and accumulation. A bulk of F3 progeny all exhibiting high Zn tolerance: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides. A bulk of F3 progeny all exhibiting low Zn tolerance: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides. A bulk of F3 progeny all exhibiting high Zn accumulation: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides. A bulk of F3 progeny all exhibiting low Zn accumulation: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides. Experimenter name = H. John Newbury Experimenter phone = 0121 414 5581 Experimenter fax = 0121 414 5925 Experimenter institute = University of Birmingham Experimenter address = School of Biosciences Experimenter address = University of Birmingham Experimenter address = Edgbaston Experimenter address = Birmingham Experimenter zip/postal_code = B15 2TT Experimenter country = UK Keywords: stimulus_or_stress_design; organism_part_comparison_design; strain_or_line_design
2007-01-08 | GSE5738 | GEO
Project description:Approximately 0.2% of all angiosperms are classified as metal hyperaccumulators based on their extraordinarily high leaf metal contents, for example >1% zinc, >0.1% nickel or >0.01% cadmium (Cd) in dry biomass. So far, metal hyperaccumulation has been considered to be a taxon-wide, constitutively expressed trait, the extent of which depends solely on available metal concentrations in the soil. Here we show that in the facultative metallophyte Arabidopsis halleri, both insect herbivory and mechanical wounding of leaves trigger an increase specifically in leaf Cd accumulation. Moreover, the Cd concentrations accumulated in leaves can serve as an elemental defense against herbivory by larvae of the Brassicaceae specialist small white (Pieris rapae), thus allowing the plant to take advantage of this non-essential trace element and toxin. Metal homeostasis genes are overrepresented in the systemic transcriptional response of roots to the wounding of leaves in A. halleri, supporting that leaf Cd accumulation is preceded by systemic signaling events. A similar, but quantitatively less pronounced transcriptional response was observed in A. thaliana, suggesting that the systemically regulated modulation of metal homeostasis in response to leaf wounding also occurs in non-hyperaccumulator plants. This is the first report of an environmental stimulus influencing metal hyperaccumulation.
| S-EPMC4427619 | biostudies-literature
Project description:The Sedum alfredii Hance hyperaccumulating ecotype (HE) has the ability to hyperaccumulate cadmium (Cd), as well as zinc (Zn) and lead (Pb) in above-ground tissues. Although many physiological studies have been conducted with these plants, the molecular mechanisms underlying their hyper-tolerance to heavy metals are largely unknown. Here we report on the generation of 9.4 gigabases of adaptor-trimmed raw sequences and the assembly of 57,162 transcript contigs in S. alfredii Hance (HE) shoots by the combination of Roche 454 and Illumina/Solexa deep sequencing technologies. We also have functionally annotated the transcriptome and analyzed the transcriptome changes upon Cd hyperaccumulation in S. alfredii Hance (HE) shoots. There are 110 contigs and 123 contigs that were up-regulated (Fold Change ? 2.0) and down-regulated (Fold Change </=0.5) by chronic Cd treatment in S. alfredii Hance (HE) at q-value cutoff of 0.005, respectively. Quantitative RT-PCR was employed to compare gene expression patterns between S. alfredii Hance (HE) and non-hyperaccumulating ecotype (NHE). Our results demonstrated that several genes involved in cell wall modification, metal translocation and remobilization were more induced or constitutively expressed at higher levels in HE shoots than that in NHE shoots in response to Cd exposure. Together, our study provides large-scale expressed sequence information and genome-wide transcriptome profiling of Cd responses in S. alfredii Hance (HE) shoots.
| S-EPMC3670878 | biostudies-literature
Project description:P1B-ATPases are decisive for metal accumulation phenotypes, but mechanisms of their regulation are only partially understood. Here, we studied the Cd/Zn transporting ATPases NcHMA3 and NcHMA4 from Noccaea caerulescens as well as AhHMA3 and AhHMA4 from Arabidopsis halleri. Protein biochemistry was analyzed on HMA4 purified from roots of N. caerulescens in active state. Metal titration of NcHMA4 protein with an electrochromic dye as charge indicator suggested that HMA4 reaches maximal ATPase activity when all internal high-affinity Cd2+ binding sites are occupied. Although HMA4 was reported to be mainly responsible for xylem loading of heavy metals for root to shoot transport, the current study revealed high expression of NcHMA4 in shoots as well. Further, there were additional 20 and 40 kD fragments at replete Zn2+ and toxic Cd2+, but not at deficient Zn2+ concentrations. Altogether, the protein level expression analysis suggested a more multifunctional role of NcHMA4 than previously assumed. Organ-level transcription analysis through quantitative PCR of mRNA in N. caerulescens and A. halleri confirmed the strong shoot expression of both NcHMA4 and AhHMA4. Further, in shoots NcHMA4 was more abundant in 10 μM Zn2+ and AhHMA4 in Zn2+ deficiency. In roots, NcHMA4 was up-regulated in response to deficient Zn2+ when compared to replete Zn2+ and toxic Cd2+ treatment. In both species, HMA3 was much more expressed in shoots than in roots, and HMA3 transcript levels remained rather constant regardless of Zn2+ supply, but were up-regulated by 10 μM Cd2+. Analysis of cellular expression by quantitative mRNA in situ hybridisation showed that in A. halleri, both HMA3 and HMA4 mRNA levels were highest in the mesophyll, while in N. caerulescens they were highest in the bundle sheath of the vein. This is likely related to the different final storage sites for hyperaccumulated metals in both species: epidermis in N. caerulescens, mesophyll in A. halleri.
| S-EPMC5438989 | biostudies-literature
Project description:This application is from a NERC-funded consortium (Mark MacNair, Nick Smirnoff, Exeter) and (Brian Ford-Lloyd, John Newbury, Birmingham). Metal tolerance is one of the classic examples of micro-evolution. Despite extensive research the physiological bases of the adaptation in plants are largely unknown. Arabidopsis halleri is a zinc tolerant, zinc accumulating species whereas Arabidopsis petraea is non-accumulating and non-tolerant. The objective of our programme is to identify a) those key genes that act to determine Zn tolerance and accumulation in Arabidopsis (and which account for the difference in performance of A. halleri and A. petraea grown in the presence of elevated Zn) and b) those _downstream_ genes that are expressed as part of the tolerance or accumulation response. Phase 1: Total of 24 chips: Material ready by May 2003 The results will a) tell us how effectively material derived from other Arabidopsis species hybridises to the chips, and b) identify genes that are differentially expressed in the two species in the presence and absence of Zn stress (thus providing initial lists of genes that may be responsible for Zn tolerance or accumulation- but see phase 2)· A. halleri exposed to low and high Zn; root and leaf mRNAs extracted: 3 replicates of each: = 12 slides· A. petraea exposed to low and high Zn; root and leaf mRNAs extracted: 3 replicates of each: = 12 slides Phase 2: Total of 48 chips: Material ready by September 2003 The results will tell us which genes, identified as having appropriate expression patterns, co-segregate with the Zn tolerance or accumulation phenotype and will provide firmer candidate genes for intensive study. Bulks will be produced from F3 progeny (from the halleri x petraea cross) following phentoypic analyses for Zn tolerance and accumulation.· A bulk of F3 progeny all exhibiting high Zn tolerance: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides· A bulk of F3 progeny all exhibiting low Zn tolerance: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides· A bulk of F3 progeny all exhibiting high Zn accumulation: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides· A bulk of F3 progeny all exhibiting low Zn accumulation: exposed to low and high Zn; leaf and root mRNAs: 3 replicates: = 12 slides Experimenter name = H. John Newbury Experimenter phone = 0121 414 5581 Experimenter fax = 0121 414 5925 Experimenter department = Newbury lab Experimenter institute = University of Birmingham Experimenter address = School of Biosciences Experimenter address = University of Birmingham Experimenter address = Edgbaston Experimenter address = Birmingham Experimenter zip/postal_code = B15 2TT Experimenter country = UK Keywords: stimulus_or_stress_design; organism_part_comparison_design; strain_or_line_design
2007-01-08 | GSE5613 | GEO