BACKGROUND: Metal-hyperaccumulating plant species are plants that are endemic to metalliferous soils and are able to tolerate and accumulate metals in their above-ground tissues to very high ...concentrations. One such hyperaccumulator, Thlaspi caerulescens, has been widely studied for its remarkable properties to tolerate toxic levels of zinc (Zn), cadmium (Cd) and sometimes nickel (Ni) in the soil, and accumulate these metals to very high levels in the shoot. The increased awareness regarding metal-hyperaccumulating plants by the plant biology community has helped spur interest in the possible use of plants to remove heavy metals from contaminated soils, a process known as phytoremediation. Hence, there has been a focus on understanding the mechanisms that metal-hyperaccumulator plant species such as Thlaspi caerulescens employ to absorb, detoxify and store metals in order to use this information to develop plants better suited for the phytoremediation of metal-contaminated soils. SCOPE: In this review, an overview of the findings from recent research aimed at better understanding the physiological mechanisms of Thlaspi caerulescens heavy-metal hyperaccumulation as well as the underlying molecular and genetic determinants for this trait will be discussed. Progress has been made in understanding some of the fundamental Zn and Cd transport physiology in T. caerulescens. Furthermore, some interesting metal-related genes have been identified and characterized in this plant species, and regulation of the expression of some of these genes may be important for hyperaccumulation. CONCLUSIONS: Thlaspi caerulescens is a fascinating and useful model system not only for studying metal hyperaccumulation, but also for better understanding micronutrient homeostasis and nutrition. Considerable future research is still needed to elucidate the molecular, genetic and physiological bases for the extreme metal tolerance and hyperaccumulation exhibited by plant species such as T. caerulescens.
The ability of metal hyperaccumulating plants to tolerate and accumulate heavy metals results from adaptations of metal homeostasis. NRAMP metal transporters were found to be highly expressed in some ...hyperaccumulating plant species. Here, we identified TcNRAMP3 and TcNRAMP4, the closest homologues to AtNRAMP3 and AtNRAMP4 in Thlaspi caerulescens and characterized them by expression analysis, confocal imaging and heterologous expression in yeast and Arabidopsis thaliana. TcNRAMP3 and TcNRAMP4 are expressed at higher levels than their A. thaliana homologues. When expressed in yeast TcNRAMP3 and TcNRAMP4 transport the same metals as their respective A. thaliana orthologues: iron (Fe), manganese (Mn) and cadmium (Cd) but not zinc (Zn) for NRAMP3; Fe, Mn, Cd and Zn for NRAMP4. They also localize at the vacuolar membrane in A. thaliana protoplasts. Inactivation of AtNRAMP3 and AtNRAMP4 in A. thaliana results in strong Cd and Zn hypersensitivity, which is fully rescued by TcNRAMP3 or TcNRAMP4 expression. However, metal tolerance conferred by TcNRAMP expression in nramp3nramp4 mutant does not exceed that of wild-type A. thaliana. Our data indicate that the difference between TcNRAMP3 and TcNRAMP4 and their A. thaliana orthologues does not lie in a different protein function, but probably resides in a different expression level or expression pattern.
The mechanisms of enhanced root to shoot metal transport in heavy metal hyperaccumulators are incompletely understood. Here, we compared the distribution of nickel (Ni) over root segments and tissues ...in the hyperaccumulator Thlaspi caerulescens and the nonhyperaccumulator Thlaspi arvense, and investigated the role of free histidine in Ni xylem loading and Ni transport across the tonoplast. Nickel accumulation in mature cortical root cells was apparent in T. arvense and in a high-Ni-accumulating T. caerulescens accession, but not in a low-accumulating T. caerulescens accession. Compared with T. arvense, the concentration of free histidine in T. caerulescens was 10-fold enhanced in roots, but was only slightly higher in leaves, regardless of Ni exposure. Nickel uptake in MgATP-energized root- and shoot-derived tonoplast vesicles was almost completely blocked in T. caerulescens when Ni was supplied as a 1 : 1 Ni-histidine complex, but was uninhibited in T. arvense. Exogenous histidine supply enhanced Ni xylem loading in T. caerulescens but not in T. arvense. The high rate of root to shoot translocation of Ni in T. caerulescens compared with T. arvense seems to depend on the combination of two distinct characters, that is, a greatly enhanced root histidine concentration and a strongly decreased ability to accumulate histidine-bound Ni in root cell vacuoles.
ABSTRACT
Thlaspi caerulescens J. & C. Presl is a distinctive metallophyte of central and western Europe that almost invariably hyperaccumulates Zn to> 1.0% of shoot dry biomass in its natural ...habitats, and can hyperaccumulate Ni to> 0.1% when growing on serpentine soils. Populations from the Ganges region of southern France also have a remarkable ability to accumulate Cd in their shoots to concentrations well in excess of 0.01% without apparent toxicity symptoms. Because hyperaccumulation of Cd appears to be highly variable in this species, the relationship between Cd tolerance and metal accumulation was investigated for seven contrasting populations of T. caerulescens grown under controlled conditions in solution culture. The populations varied considerably in average plant biomass (3.1‐fold), shoot : root ratio (2.2‐fold), Cd hyperaccumulation (3.5‐fold), shoot : root Cd‐concentration ratio (3.1‐fold), and shoot Cd : Zn ratio (2.6‐fold), but the degree of hyperaccumulation of Cd and Zn were strongly correlated. Two populations from the Ganges region were distinct in exhibiting high degrees of both Cd tolerance and hyperaccumulation (one requiring 3 µM Cd for optimal growth), whereas across the other five populations there was an inverse relationship between Cd tolerance and hyperaccumulation, as has been noted previously for Zn. Metal hyperaccumulation was negatively correlated with shoot : root ratio, which could account quantitatively for the differences between populations in shoot Zn (but not Cd) concentrations. On exposure to 30 µM Cd, the two Ganges populations showed marked reductions in shoot Zn and Fe concentrations, although Cd accumulation was not inhibited by elevated Zn; in the other five populations, 30 µM Cd had little or no effect on Zn or Fe accumulation but markedly reduced shoot Ca concentration. These results support a proposal that Cd is taken up predominantly via a high‐affinity uptake system for Fe in the Ganges populations, but via a lower‐affinity pathway for Ca in other populations. Total shoot Cd accumulated per plant was much more closely related to population Cd tolerance than Cd hyperaccumulation, indicating that metal tolerance may be the more important selection criterion in developing lines with greatest phytoremediation potential.
Background, aim, and scope Trace elements (heavy metals and metalloids) are important environmental pollutants, and many of them are toxic even at very low concentrations. Pollution of the biosphere ...with trace elements has accelerated dramatically since the Industrial Revolution. Primary sources are the burning of fossil fuels, mining and smelting of metalliferous ores, municipal wastes, agrochemicals, and sewage. In addition, natural mineral deposits containing particularly large quantities of heavy metals are found in many regions. These areas often support characteristic plant species thriving in metal-enriched environments. Whereas many species avoid the uptake of heavy metals from these soils, some of them can accumulate significantly high concentrations of toxic metals, to levels which by far exceed the soil levels. The natural phenomenon of heavy metal tolerance has enhanced the interest of plant ecologists, plant physiologists, and plant biologists to investigate the physiology and genetics of metal tolerance in specialized hyperaccumulator plants such as Arabidopsis halleri and Thlaspi caerulescens. In this review, we describe recent advances in understanding the genetic and molecular basis of metal tolerance in plants with special reference to transcriptomics of heavy metal accumulator plants and the identification of functional genes implied in tolerance and detoxification. Results Plants are susceptible to heavy metal toxicity and respond to avoid detrimental effects in a variety of different ways. The toxic dose depends on the type of ion, ion concentration, plant species, and stage of plant growth. Tolerance to metals is based on multiple mechanisms such as cell wall binding, active transport of ions into the vacuole, and formation of complexes with organic acids or peptides. One of the most important mechanisms for metal detoxification in plants appears to be chelation of metals by low-molecular-weight proteins such as metallothioneins and peptide ligands, the phytochelatins. For example, glutathione (GSH), a precursor of phytochelatin synthesis, plays a key role not only in metal detoxification but also in protecting plant cells from other environmental stresses including intrinsic oxidative stress reactions. In the last decade, tremendous developments in molecular biology and success of genomics have highly encouraged studies in molecular genetics, mainly transcriptomics, to identify functional genes implied in metal tolerance in plants, largely belonging to the metal homeostasis network. Discussion Analyzing the genetics of metal accumulation in these accumulator plants has been greatly enhanced through the wealth of tools and the resources developed for the study of the model plant Arabidopsis thaliana such as transcript profiling platforms, protein and metabolite profiling, tools depending on RNA interference (RNAi), and collections of insertion line mutants. To understand the genetics of metal accumulation and adaptation, the vast arsenal of resources developed in A. thaliana could be extended to one of its closest relatives that display the highest level of adaptation to high metal environments such as A. halleri and T. caerulescens. Conclusions This review paper deals with the mechanisms of heavy metal accumulation and tolerance in plants. Detailed information has been provided for metal transporters, metal chelation, and oxidative stress in metal-tolerant plants. Advances in phytoremediation technologies and the importance of metal accumulator plants and strategies for exploring these immense and valuable genetic and biological resources for phytoremediation are discussed. Recommendations and perspectives A number of species within the Brassicaceae family have been identified as metal accumulators. To understand fully the genetics of metal accumulation, the vast genetic resources developed in A. thaliana must be extended to other metal accumulator species that display traits absent in this model species. A. thaliana microarray chips could be used to identify differentially expressed genes in metal accumulator plants in Brassicaceae. The integration of resources obtained from model and wild species of the Brassicaceae family will be of utmost importance, bringing most of the diverse fields of plant biology together such as functional genomics, population genetics, phylogenetics, and ecology. Further development of phytoremediation requires an integrated multidisciplinary research effort that combines plant biology, genetic engineering, soil chemistry, soil microbiology, as well as agricultural and environmental engineering.
Fe deficiency may increase Cd accumulation in peanuts. However, the mechanisms are not yet fully understood. In the present study, two contrasting peanut cultivars, Luhua 8 (low seed-Cd cultivar) and ...Zhenghong 3 (high seed-Cd cultivar) were used to investigate the effect of Fe deficiency on the uptake and accumulation of cadmium (Cd) by hydroponic experiments. Under Fe-sufficient conditions, compared with Luhua 8, Zhenghong 3 had higher specific root length (SRL) and proportion of fine roots with a lower Km for Cd and showed slightly higher expression of AhIRT1 and AhNRAMP1 in the roots. These traits may be responsible for high capacity for Cd accumulation in Zhenghong 3. Under Fe deficiency, the increase of Cd accumulation was much larger in Zhenghong 3 than in Luhua 8. Kinetics studies revealed that the Vmax for Cd influx was 1.56-fold higher in Fe-deficient plants than in Fe-sufficient plants for Zhenghong 3, versus 0.48-fold higher for Luhua 8. Moreover, the increased expression levels of AhIRT1 and AhNRAMP1 induced by Fe deficiency was higher in Zhenghong 3 than in Luhua 8. Yeast complementation assays suggested that the AhIRT1 and AhNRAMP1 may function as transporters involved in Cd uptake. In conclusion, the different Cd accumulation between the two cultivars under Fe deficiency may be correlated with Vmax value for Cd uptake and the expression levels of AhIRT1 and AhNRAMP1 in the roots.
Nitrate fertilization has been shown to increase Zn hyperaccumulation by Noccaea caerulescens (Prayon) (formerly Thlaspi caerulescens). However, it is unknown whether this increased hyperaccumulation ...is a direct result of NO₃ ⁻ nutrition or due to changes in rhizosphere pH as a result of NO₃ ⁻ uptake. This paper investigated the mechanism of NO₃ ⁻-enhanced Zn hyperaccumulation in N. caerulescens by assessing the response of Zn uptake to N form and solution pH. Plants were grown in nutrient solution with 300 μM Zn and supplied with either (NH₄)₂SO₄, NH₄NO₃ or Ca(NO₃)₂. The solutions were buffered at either pH 4.5 or 6.5. The Zn concentration and content were much higher in shoots of NO₃ ⁻-fed plants than in NH₄ ⁺-fed plants at pH 4.5 and 6.5. The Zn concentration in the shoots was mainly enhanced by NO₃ ⁻, whereas the Zn concentration in the roots was mainly enhanced by pH 6.5. Nitrate increased Zn uptake in the roots at pH 6.5 and increased apoplastic Zn at pH 4.5. Zinc and Ca co-increased and was found co-localized in leaf cells of NO₃ ⁻-fed plants. We conclude that NO₃ ⁻ directly enhanced Zn uptake and translocation from roots to shoots in N. caerulescens.
Pennisetum
grasses (
P. purpureum
Schumach. ‘Purple’,
P. alopecuroides
(L.) Spreng. ‘Liren’ and
P. alopecuroides
(L.) Spreng. ‘Changsui’), and a cadmium (Cd) hyperaccumulator (
Thlaspi caerulescens
...J.Presl & C.Presl), were grown in soil with four Cd addition levels of 0, 2, 20 and 200 mg/kg. Toxicity symptoms were not observed although growth of all plants decreased as Cd addition increased. Shoot bioconcentration factor (BCFS), the translocation factor (TF) and shoot accumulation of Cd for most plants first increased and then declined as Cd concentrations increased. In contrast, the root bioconcentration factor (BCFR) for
T. caerulescens
declined and root Cd accumulation for
T. caerulescens
and two
P. alopecuroides
cultivars increased consistently as Cd levels increased.
P. purpureum
had the largest biomass with shoot Cd accumulation similar to that of
T. caerulescens
, despite lower foliar Cd concentration. Although shoot Cd concentrations of two
P. alopecuroides
cultivars were lower than for
P. purpureum
, root Cd concentrations were greater.
P. purpureum
had Cd BCFS and TF (> 1) at 2- and 20-mg/kg Cd addition treatments, similar to
T. caerulescens
.
P. alopecuroides
cultivars had Cd BCFR (> 1) and TF (< 1) at all Cd levels. Roots did not affect rhizosphere pH. However, concentrations of acid extractable Cd in rhizosphere soil were lower than those of corresponding non-rhizosphere soil at all Cd levels for
T. caerulescens
and
P. purpureum
;
T. caerulescens
and
P. purpureum
did not affect less bioavailable Cd fractions. Concentrations of acid extractable Cd in the rhizosphere of the
P. alopecuroides
cultivars were not reduced at any Cd level. Differences in Cd accumulation among the three
Pennisetum
grasses were mainly attributable to root biomass and Cd TFs rather than rhizosphere Cd mobility.
BACKGROUND: Many plant species can modify their root architecture to enable them to forage for heterogeneously distributed nutrients in the soil. The foraging response normally involves increased ...proliferation of lateral roots within nutrient-rich soil patches, but much remains to be understood about the signalling mechanisms that enable roots to sense variations in the external concentrations of different mineral nutrients and to modify their patterns of growth and development accordingly. SCOPE: In this review we consider different aspects of the way in which the nitrogen supply can modify root branching, focusing on Arabidopsis thaliana. Our current understanding of the mechanism of nitrate stimulation of lateral root growth and the role of the ANR1 gene are summarized. In addition, evidence supporting the possible role of auxin in regulating the systemic inhibition of early lateral root development by high rates of nitrate supply is presented. Finally, we examine recent evidence that an amino acid, L-glutamate, can act as an external signal to elicit complex changes in root growth and development. CONCLUSIONS: It is clear that plants have evolved sophisticated pathways for sensing and responding to changes in different components of the external nitrogen supply as well as their own internal nitrogen status. We speculate on the possibility that the effects elicited by external L-glutamate represent a novel form of foraging response that could potentially enhance a plant's ability to compete with its neighbours and micro-organisms for localized sources of organic nitrogen.
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