Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives

Charlier, Jean-Benoit; Polese, Catherine; Nouet, Cécile; Carnol, Monique; Bosman, Bernard; Krämer, Ute; Motté, Patrick; Hanikenne, Marc

doi:10.1093/jxb/erv188

Cited by 27 publications

(26 citation statements)

References 63 publications

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“…FRD3 gene expression and the corresponding citrate-loading activity into the xylem correlated positively with the shoot Fe status and primary root growth when Arabidopsis accessions were grown under high Zn supply. In our experiments, FRD3 expression was not altered significantly under high Zn (Supplemental Table S2), which may be due to the fact that elevated Zn triggers a complex posttranscriptional regulation of FRD3 (Charlier et al, 2015). Nevertheless, some effects of Zn surpassed those caused by Fe deficiency, as especially the length of lateral roots was more susceptible to increasing Zn supplies (Figs.…”

Section: Zn Strongly Induces Fe Deficiency Signaling and Related Physmentioning

confidence: 61%

Heavy Metals Induce Iron Deficiency Responses at Different Hierarchic and Regulatory Levels

et al. 2017

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In plants, the excess of several heavy metals mimics iron (Fe) deficiency-induced chlorosis, indicating a disturbance in Fe homeostasis. To examine the level at which heavy metals interfere with Fe deficiency responses, we carried out an in-depth characterization of Fe-related physiological, regulatory, and morphological responses in Arabidopsis (Arabidopsis thaliana) exposed to heavy metals. Enhanced zinc (Zn) uptake closely mimicked Fe deficiency by leading to low chlorophyll but high ferric-chelate reductase activity and coumarin release. These responses were not caused by Zn-inhibited Fe uptake via IRON-REGULATED TRANSPORTER (IRT1). Instead, Zn simulated the transcriptional response of typical Fe-regulated genes, indicating that Zn affects Fe homeostasis at the level of Fe sensing. Excess supplies of cobalt and nickel altered root traits in a different way from Fe deficiency, inducing only transient Fe deficiency responses, which were characterized by a lack of induction of the ethylene pathway. Cadmium showed a rather inconsistent influence on Fe deficiency responses at multiple levels. By contrast, manganese evoked weak Fe deficiency responses in wild-type plants but strongly exacerbated chlorosis in irt1 plants, indicating that manganese antagonized Fe mainly at the level of transport. These results show that the investigated heavy metals modulate Fe deficiency responses at different hierarchic and regulatory levels and that the interaction of metals with physiological and morphological Fe deficiency responses is uncoupled. Thus, this study not only emphasizes the importance of assessing heavy metal toxicities at multiple levels but also provides a new perspective on how Fe deficiency contributes to the toxic action of individual heavy metals.

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Section: Zn Strongly Induces Fe Deficiency Signaling and Related Physmentioning

confidence: 61%

Heavy Metals Induce Iron Deficiency Responses at Different Hierarchic and Regulatory Levels

et al. 2017

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“…FRD3 also showed higher expression and was induced by Cd in I16 roots. FRD3 , encoding a citrate transporter, may be involved in the maintenance of Fe homeostasis during Cd treatment (Durrett et al ., ; Pineau et al ., ; Charlier et al ., ). Finally, lower activation of antioxidative defences and stress‐related genes in I16 than in PL22 is probably attributable to the low Cd uptake and lower Cd accumulation in roots and shoot, respectively.…”

Section: Discussionmentioning

confidence: 89%

Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri

et al. 2018

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While cadmium (Cd) tolerance is a constitutive trait in the Arabidopsis halleri species, Cd accumulation is highly variable. Recent adaptation to anthropogenic metal stress has occurred independently within the genetic units of A. halleri and the evolution of different mechanisms involved in Cd tolerance and accumulation has been suggested. To gain a better understanding of the mechanisms underlying Cd tolerance and accumulation in A. halleri, ionomic inductively coupled plasma mass spectrometry (ICP-MS), transcriptomic (RNA sequencing) and metabolomic (high-performance liquid chromatography-mass spectrometry) profiles were analysed in two A. halleri metallicolous populations from different genetic units (PL22 from Poland and I16 from Italy). The PL22 and I16 populations were both hypertolerant to Cd, but PL22 hyperaccumulated Cd while I16 behaved as an excluder both in situ and when grown hydroponically. The observed hyperaccumulator vs excluder behaviours were paralleled by large differences in the expression profiles of transporter genes. Flavonoid-related transcripts and metabolites were strikingly more abundant in PL22 than in I16 shoots. The role of novel A. halleri candidate genes possibly involved in Cd hyperaccumulation or exclusion was supported by the study of corresponding A. thaliana knockout mutants. Taken together, our results are suggestive of the evolution of divergent strategies for Cd uptake, transport and detoxification in different genetic units of A. halleri.

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“…NAS4 contributes to NA synthesis (Curie et al ., ) and is required under Fe deficiency and for tolerance to Zn excess (Palmer et al ., ). FRD3 is a citrate transporter, loading citrate into the xylem in roots, which is required for proper Fe homeostasis and Zn tolerance (Rogers & Guerinot, ; Green & Rogers, ; Durrett et al ., ; Pineau et al ., ; Charlier et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…A number of major candidate genes, involved in metal transport and metal chelator synthesis and all constitutively highly expressed in A. halleri compared with its nonaccumulator relatives Arabidopsis thaliana and Arabidopsis lyrata , were further characterized functionally (e.g. Dräger et al ., ; Hanikenne et al ., ; Shahzad et al ., ; Deinlein et al ., ; Baliardini et al ., ; Charlier et al ., ). Briefly, several Zinc‐Regulated Transporter Iron‐Regulated Transporter‐Like Protein (ZIP) transporters presumably contribute to enhanced rates of root metal uptake, enhanced Zn radial transport towards the root xylem and Zn distribution in shoots (Talke et al ., ; Krämer et al ., ; Lin et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri

Schvartzman

Corso²,

Fataftah

et al. 2018

New Phytologist

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Zinc (Zn) hyperaccumulation and hypertolerance are highly variable traits in Arabidopsis halleri. Metallicolous populations have evolved from nearby nonmetallicolous populations in multiple independent adaptation events. To determine whether these events resulted in similar or divergent adaptive strategies to high soil Zn concentrations, we compared two A. halleri metallicolous populations from distant genetic units in Europe (Poland (PL22) and Italy (I16)). The ionomic (Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP-AES)) and transcriptomic (RNA sequencing (RNA-Seq)) responses to growth at 5 and 150 μM Zn were analyzed in root and shoot tissues to examine the contribution of the geographic origin and treatment to variation among populations. These analyses were enabled by the generation of a reference A. halleri transcriptome assembly. The genetic unit accounted for the largest variation in the gene expression profile, whereas the two populations had contrasting Zn accumulation phenotypes and shared little common response to the Zn treatment. The PL22 population displayed an iron deficiency response at high Zn in roots and shoots, which may account for higher Zn accumulation. By contrast, I16, originating from a highly Zn-contaminated soil, strongly responded to control conditions. Our data suggest that distinct mechanisms support adaptation to high Zn in soils among A. halleri metallicolous populations.

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Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives

Abstract: HighlightHigh expression of the FRD3 gene in the metal hyperaccumulator Arabidopsis halleri stems from complex zinc-regulated transcriptional and post-transcriptional mechanisms present in the non-hyperaccumulating Arabidopsis thaliana.

Cited by 27 publications

References 63 publications

Heavy Metals Induce Iron Deficiency Responses at Different Hierarchic and Regulatory Levels

Heavy Metals Induce Iron Deficiency Responses at Different Hierarchic and Regulatory Levels

Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri

Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri

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