Noccaea caerulescens populations adapted to grow in metalliferous and non-metalliferous soils: Ni tolerance, accumulation and expression analysis of genes involved in metal homeostasis

Visioli, Giovanna; Gullì, Mariolina; Marmiroli, Nelson

doi:10.1016/j.envexpbot.2014.04.001

Cited by 28 publications

(10 citation statements)

References 47 publications

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“…Firstly, Ni absorption by leaf cells may involve trans-porters from the ZIP family, e.g. ZNT1 and ZNT2, as the gene expression of these transporters can be up regulated by Ni exposure (Visioli et al 2014). Nickel is preferentially distributed in epidermal cells, the least active tissue of leaf symplast (Küpper et al 2001;Tappero et al 2007), while palisade mesophyll cells become an increasingly important compartment as Ni concentrations in leaves increase (Broadhurst et al 2004).…”

Section: Xylem Unloading and Leaf Compartmentation Processesmentioning

confidence: 99%

Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

et al. 2017

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Background Hyperaccumulator plants are unusual plants that accumulate particular metals or metalloids, such as nickel, zinc, cadmium and arsenic, in their living tissues to concentrations that are hundreds to thousands of times greater than what is normal for most plants. The hyperaccumulation phenomenon is rare (exhibited by less than 0.2% of all angiosperms), with most of the ~500 hyperaccumulator species known globally for nickel. Scope This review highlights the contemporary understanding of nickel hyperaccumulation processes, which include root uptake and sequestration, xylem loading and transport, leaf compartmentation and phloem translocation processes. Conclusions Hyperaccumulator plants have evolved highly efficient physiological mechanisms for taking up nickel in their roots followed by rapid translocation and sequestration into the aerial shoots. The uptake of nickel is mainly involved with low affinity transport systems, presumably from the ZIP family. The presence of high concentrations of histidine prevents nickel sequestration in roots. Nickel is efficiently loaded into the xylem, where it mainly presents as Ni 2+. The leaf is the main storage organ, which sequestrates nickel in nonactive sites, e.g. vacuoles and apoplast. Recent studies show that phloem translocates high levels of nickel, which has a strong impact on nickel accumulation in young growing tissues. Nickel hyperaccumulator plants: Discovery and application Nickel (Ni) is the latest element to be considered essential for higher plants (Brown et al. 1987; Marschner 1995; Gerendas et al. 1999), due to its key role in urease, an enzyme that is widely distributed in higher plants (Hogan et al. 1983). The presence of urease prevents the accumulation of urea, which is generated during metabolic processes and is toxic to plants when presents in high concentrations. Apart from its function in urease activation, other physiological functions of Ni are poorly understood in higher plants (Gerendas et al. 1999). Although Ni is an essential micronutrient, its physiological requirement is extremely low. It is shown that 0.1 mg kg −1 or lower is sufficient for seed germination and plant growth (Brown et al. 1987; Gerendas et al. 1999). Hence, Ni deficiency in naturally-grown plants rarely occurs, and the only known case is for the pecan (Wood et al. 2004). Plants usually contain low concentrations of Ni, normally ranging from 0.01-5 mg kg −1 (Welch 1981). In contrast to the low Ni accumulation in normal plants, there is a group of plant species (hyperaccumulators) that can accumulate exceptional concentrations of Ni (>1000 mg kg −1 dry weight) in their living shoots without symptoms of toxicity (Brooks et al. 1977). Amazingly, up to 60.2 and 66.7 g kg −1 foliar Ni concentrations in the Ni hyperaccumulator Phyllanthus × pallidus from Cuba and Alyssum cassium from Turkey have been recorded (Reeves et al. 1996; Reeves and Adıgüzel 2008); while 25% Ni is found in the latex of the New Caledonian tree Pycnandra acuminata, and 16.9% Ni in the phloem sap exu...

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Section: Xylem Unloading and Leaf Compartmentation Processesmentioning

confidence: 99%

Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

et al. 2017

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“…Noccaea caerulescens is a variable species [6,22–24] whose European populations differ in both morphological and physiological features, including metal hyperaccumulation [25–30]. Populations exhibit variable degrees of metal tolerance and of metal accumulation, which are thought to be genetically independent traits [6,31].…”

Section: Introductionmentioning

confidence: 99%

Variation in defence strategies in the metal hyperaccumulator plant Noccaea caerulescens is indicative of synergies and trade-offs between forms of defence

Fones

Preston

Smith³

2019

R. Soc. open sci.

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In the metal hyperaccumulator plant Noccaea caerulescens, zinc may provide a defence against pathogens. However, zinc accumulation is a variable trait in this species. We hypothesize that this variability affects the outcome of interactions between metal accumulation and the various constitutive and inducible defences that N. caerulescens shares with non-accumulator plants. We compare zinc concentrations, glucosinolate concentrations and inducible stress responses, including reactive oxygen species (ROS) and cell death, in four N. caerulescens populations, and relate these to the growth of the plant pathogen Pseudomonas syringae, its zinc tolerance mutants and Pseudomonas pathogens isolated from a natural population of N. caerulescens. The populations display strikingly different combinations of defences. Where defences are successful, pathogens are limited primarily by metals, cell death or organic defences; there is evidence of population-dependent trade-offs or synergies between these. In addition, we find evidence that Pseudomonas pathogens have the capacity to overcome any of these defences, indicating that the arms race continues. These data indicate that defensive enhancement, joint effects and trade-offs between different forms of defence are all plausible explanations for the variation we observe between populations, with factors including metal availability and metal-tolerant pathogen load probably shaping the response of each population to infection.

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“…Recently, Ni has been identified to have high binding affinity to NA, particularly in the Ni and Zn hyperaccumulator species T. caerulescens (Vacchina et al, 2003). The NAS3 gene was found to be overexpressed and high levels of NA were produced in T. caerulescens, Arabidopsis halleri, Noccaea caerulescens exposed to Ni (Vacchina et al, 2003;Deinlein et al, 2012;Visioli et al, 2014). It appears that an increase in nicotianamine contributes to metal tolerance in hyperaccumulator plants via metal chelation and facilitates metal translocation (Weber et al, 2004;Deinlein et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

High Level of Nicotianamine Synthase (NAS3) and Natural Resistance Associated Macrophage Protein (NRAMP4) Gene Transcription Induced by Potassium Nitrate in Trembling Aspen (Populus tremuloides)

Czajka¹,

Nkongolo²

2018

American Journal of Biochemistry and Biotechnology

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Changes in gene transcription in response to excess metal concentrations have been reported in many organisms, including yeast, microorganisms and plants. Most investigations on the effects of nickel toxicity in plants use commercial salts whose effects have not been analyzed in detail. The main objective of the present study was to determine the effects of different doses of nickel nitrate and potassium nitrates on gene transcription in Populus tremuloides. Four month-old P. tremuloides seedlings were treated with different doses of nitrate salts including 150 mg/kg, 500 mg/kg, 800 mg/kg and 1, 600 mg/kg. A significant increase of Nicotianamine Synthase (NAS3) gene transcription was induced by the 400 mg/kg and 800 mg/kg of nickel nitrate doses compared to water. This upregulation was driven by nitrate rather than nickel. Likewise, the 800 mg/kg and 1,600 mg/kg doses of potassium nitrate resulted in significant increase in the transcription of Natural Resistance Associated Macrophage Protein (NRAMP4) gene compared to water control and the 150 mg/kg dose. This differential transcription of this gene was caused by potassium. Our results also confirmed that the low level of bioavailable nickel in metalcontaminated soils (<150 mg/kg) cannot induce differential transcription of NAS3 and NRAMP4. The use of nitrate without nickel should be required as additional controls in any study assessing effects of Ni using nickel nitrate salts.

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Noccaea caerulescens populations adapted to grow in metalliferous and non-metalliferous soils: Ni tolerance, accumulation and expression analysis of genes involved in metal homeostasis

Cited by 28 publications

References 47 publications

Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

Variation in defence strategies in the metal hyperaccumulator plant Noccaea caerulescens is indicative of synergies and trade-offs between forms of defence

High Level of Nicotianamine Synthase (NAS3) and Natural Resistance Associated Macrophage Protein (NRAMP4) Gene Transcription Induced by Potassium Nitrate in Trembling Aspen (Populus tremuloides)

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