The influence of phylogeny and ecology on root,shoot and plant ionomes of 14 native Brazilian species

The ionome is the elemental composition of a living organism, its tissues, cells or cell compartments. The ionomes of roots, stems and leaves of 14 native Brazilian forest species were characterised to examine the relationships between plant and organ ionomes and the phylogenetic and ecological affiliations of species. The null hypothesis that ionomes of Brazilian forest species and their organs do not differ was tested. Concentrations of mineral nutrients in roots, stems and leaves were determined for 14 Brazilian forest species, representing seven angiosperm orders, grown hydroponically in a complete nutrient solution. The 14 species could be differentiated by their ionomes and the partitioning of mineral nutrients between organs. The ionomic differences between the 14 species did not reflect their phylogenetic relationships or successional ecology. Differences between shoot ionomes and root ionomes were greater than differences in the ionome of an organ when compared among genotypes. In conclusion, differences in ionomes of species and their organs reflect a combination of ancient phylogenetic and recent environmental adaptations.     

Soil chemical properties affect the concentration of elements (N,P, K,Ca, Mg,As, Cd,Cr, Cu,Fe, Mn,Ni, Pb,and Zn) and their distribution between organs of Rumex obtusifolius

Background and aims

The ionome (elemental composition) of grassland species has rarely been studied at the level of individual organs and little is known about effects of soil chemical properties on the ionome. Using the model oxalate plant Rumex obtusifolius, we asked how its biomass production and the distribution of elements between its organs is affected by soil chemical properties.

Methods

We established a pot experiment with R. obtusifolius planted in acidic non-contaminated control and in slightly acidic and alkaline soils anthropogenically contaminated by the risk elements As, Cd, Pb, and Zn. Both contaminated soils were untreated and treated by lime and superphosphate. We determined biomass production and the concentrations of elements in its organs.

Results

Biomass production was negatively related to the mobility of micro- and risk elements. Restricted transport of micro- and risk elements from belowground organs into leaves was recorded in untreated contaminated soils. In both lime-treated soils and in superphosphate-treated alkaline soil, elevated transport of micro- and risk elements from belowground organs into leaves was recorded in comparison to untreated contaminated soils. The lowest concentrations of micro- and risk elements were recorded in stems and seeds, followed by belowground organs and leaves.

Conclusions

R. obtusifolius is an As-, Cd-, Pb-, and Zn-excluder and is sensitive to high availability of micro- and risk elements in the soil. Soil chemical properties affect the distribution of essential elements within the plant greatly.     

Variation in phosphorus and sulfur content shapes the genetic architecture and phenotypic associations within the wheat grain ionome

Dissection of the genetic basis of wheat ionome is crucial for understanding the physiological and biochemical processes underlying mineral accumulation in seeds, as well as for efficient crop breeding. Most of the elements essential for plants are metals stored in seeds as chelate complexes with phytic acid or sulfur‐containing compounds. We assume that the involvement of phosphorus and sulfur in metal chelation is the reason for strong phenotypic correlations within ionome. Adjustment of element concentrations for the effect of variation in phosphorus and sulfur seed content resulted in drastic change of phenotypic correlations between the elements. The genetic architecture of wheat grain ionome was characterized by quantitative trait loci (QTL) analysis using a cross between durum and wild emmer wheat. QTL analysis of the adjusted traits and two‐trait analysis of the initial traits paired with either P or S considerably improved QTL detection power and accuracy, resulting in the identification of 105 QTLs and 617 QTL effects for 11 elements. Candidate gene search revealed some potential functional associations between QTLs and corresponding genes within their intervals. Thus, we have shown that accounting for variation in P and S is crucial for understanding of the physiological and genetic regulation of mineral composition of wheat grain ionome and can be implemented for other plants.     

Natural Genetic Variation in Selected Populations of Arabidopsis thaliana Is Associated with Ionomic Differences

Controlling elemental composition is critical for plant growth and development as well as the nutrition of humans who utilize plants for food. Uncovering the genetic architecture underlying mineral ion homeostasis in plants is a critical first step towards understanding the biochemical networks that regulate a plant''s elemental composition (ionome). Natural accessions of Arabidopsis thaliana provide a rich source of genetic diversity that leads to phenotypic differences. We analyzed the concentrations of 17 different elements in 12 A. thaliana accessions and three recombinant inbred line (RIL) populations grown in several different environments using high-throughput inductively coupled plasma- mass spectroscopy (ICP-MS). Significant differences were detected between the accessions for most elements and we identified over a hundred QTLs for elemental accumulation in the RIL populations. Altering the environment the plants were grown in had a strong effect on the correlations between different elements and the QTLs controlling elemental accumulation. All ionomic data presented is publicly available at www.ionomicshub.org.     

植物离子组学及其研究方法与应用进展

植物离子组学是一门研究植物体内元素组成、分布与累积以及这些元素随植物生理状况、生物与非生物刺激、发育阶段、生境和遗传等因素的变化及其机制的新兴学科。离子组学在数量遗传性状定位、生理状况判别以及植物体内调控元素吸收、运输和贮藏的潜在基因鉴别等方面至关重要。该文综述了离子组学的基本概念、研究方法和主要研究进展,并就离子组学的研究热点、面临的挑战和未来发展趋势作了简要评述。     

Multivariate statistical analysis of nutrients and trace elements in plants and soil from northwestern Russia

Results are summarized of several field and greenhouse experiments designed to estimate differences in the ability of some plant species to take up from soil essential nutrients and various trace elements and transfer them from roots to upper plant parts. Instrumental neutron activation analysis was used to determine concentrations of 22 elements in plant and soil samples. Correlation and principal component analysis were applied for interpreting a large volume of experimental results. In many cases there was no statistically significant positive correlation between element concentrations in soil and concentrations of these elements in plants. Moreover, relationships between elements were often different in soil and in different plant parts, thereby suggesting quite different element behaviours in soil and in plants. Our experimental results and data published in the literature revealed that macro- and trace element concentrations might serve as a specific indicator of plant taxonomy, thus allowing for differentiation of the plants in accordance with concentrations of certain elements in roots or in leaves. Short-term variations in concentrations of elements typical for different plant species and factors affecting these variations indicated that diurnal dynamics of plant element concentrations were regular and species-specific.     

Elemental composition of strawberry plants inoculated with the plant growth‐promoting bacterium Azospirillum brasilense REC3, assessed with scanning electron microscopy and energy dispersive X‐ray analysis

The elemental composition of strawberry plants (Fragaria ananassa cv. Macarena) inoculated with the plant growth‐promoting bacterium Azospirillum brasilense REC3, and non‐inoculated controls, was studied using scanning electron microscopy (SEM) and energy dispersive X‐ray (EDS) analysis. This allowed simultaneous semi‐quantification of different elements in a small, solid sample. Plants were inoculated and grown hydroponically in 50% or 100% Hoagland solution, corresponding to limited or optimum nutrient medium, respectively. Bacteria‐inoculated plants increased the growth index 45% and 80% compared to controls when grown in 100% and 50% Hoagland solution, respectively. Thus, inoculation with A. brasilense REC3 in a nutrient‐limited medium had the strongest effect in terms of increasing both shoot and root biomass and growth index, as already described for Azospirillum inoculated into nutrient‐poor soils. SEM‐EDS spectra and maps showed the elemental composition and relative distribution of nutrients in strawberry tissues. Leaves contained C, O, N, Na, P, K, Ca and Cu, while roots also had Si and Cl. The organic fraction (C, O and N) accounted for over 96.3% of the total chemical composition; of the mineral fraction, Na had higher accumulation in both leaves and roots. Azospirillum‐inoculated and control plants had similar elemental quantities; however, in bacteria‐inoculated roots, P was significantly increased (34.33%), which constitutes a major benefit for plant nutrition, while Cu content decreased (35.16%).     

1,135 ionomes reveal the global pattern of leaf and seed mineral nutrient and trace element diversity in Arabidopsis thaliana

Soil is a heterogeneous reservoir of essential elements needed for plant growth and development. Plants have evolved mechanisms to balance their nutritional needs based on availability of nutrients. This has led to genetically based variation in the elemental composition, the ‘ionome’, of plants, both within and between species. We explore this natural variation using a panel of wild-collected, geographically widespread Arabidopsis thaliana accessions from the 1001 Genomes Project including over 1,135 accessions, and the 19 parental accessions of the Multi-parent Advanced Generation Inter-Cross (MAGIC) panel, all with full-genome sequences available. We present an experimental design pipeline for high-throughput ionomic screenings and analyses with improved normalisation procedures to account for errors and variability in conditions often encountered in large-scale, high-throughput data collection. We report quantification of the complete leaf and seed ionome of the entire collection using this pipeline and a digital tool, Ion Explorer , to interact with the dataset. We describe the pattern of natural ionomic variation across the A. thaliana species and identify several accessions with extreme ionomic profiles. It forms a valuable resource for exploratory genetic mapping studies to identify genes underlying natural variation in leaf and seed ionome and genetic adaptation of plants to soil conditions.     

Differences in growth characteristics and dynamics of elements absorbed in seedlings of three spruce species raised on serpentine soil in northern Japan

BACKGROUND AND AIMS: Serpentine soils are characterized by the presence of heavy metals (Ni and Cr) and excess Mg; these elements often suppress plant growth. Picea glehnii is nevertheless distributed widely on serpentine soils in northern Japan. Growth characteristics were compared among P. glehnii, Picea jezoensis (distributed in the same region) and Picea abies (planted for timber production), and concentrations of elements in various tissues over time and the amount of ectomycorrhizal infection in short roots were evaluated. METHODS: Seedlings of three spruce species were planted in two types of experimental plots, comprising serpentine soil and brown forest (non-serpentine) soil, and these seedlings were grown for 3 years. Growth, ectomycorrhizal infection of short roots, and elemental composition of tissues were examined. KEY RESULTS: The total dry mass of P. glehnii planted on serpentine soil was almost the same as on brown forest soil, and a large number of needles survived to reach later age classes. By contrast, growth of P. jezoensis and P. abies in serpentine soil was significantly less than in brown forest soil, and needle shedding was accelerated. Moreover, roots of seedlings of P. glehnii on serpentine soil were highly infected with ectomycorrhiza, and the concentration of Ni in needles and roots of P. glehnii was the lowest of the three species. CONCLUSIONS: Picea glehnii has a high ability to maintain a low concentration of Ni, and the ectomycorrhizal infection may have the positive effect of excluding Ni. As a result, P. glehnii is more tolerant than the other spruce species to serpentine soil conditions.     

Cadmium uptake and bioaccumulation in selected cultivars of durum wheat and flax as affected by soil type

Accumulation of cadmium (Cd) in crop plants is of great concern due to the potential for food chain contamination through the soil-root interface. Although Cd uptake varies considerably with plant species, the processes which determine the accumulation of Cd in plant tissues are affected by soil factors. The influence of soil type on Cd uptake by durum wheat (Triticum turgidum var. durum L.) and flax (Linum usitatissimum L.) was studied in a pot experiment under environmentally controlled growth chamber conditions. Four cultivars/lines of durum wheat (Kyle, Sceptre, DT 627, and DT 637) and three cultivars/lines of flax (Flanders, AC Emerson, and YSED 2) were grown in two Saskatchewan soils: an Orthic Gray Luvisol (low background Cd concentration; total/ABDTPA extractable Cd: 0.12/0.03 mg kg^-1, respectively) and a Dark Brown Chernozem (relatively high background Cd concentration; total/ABDTPA Cd: 0.34/0.17 mg kg^-1 respectively). Plant roots, stems, newly developed heads, and grain/seeds were analyzed for Cd concentration at three stages of plant growth: two and seven weeks after germination, and at plant maturity. The results showed that Cd bioaccumulation and distribution within the plants were strongly affected by both soil type and plant cultivar/line. The Cd concentration in roots leaves and stems varied at different stages of plant growth. However, all cultivars of both plant species grown in the Chernozemic soil accumulated more Cd in grain/seeds than plants grown in the Orthic Gray Luvisol soil. The different Cd accumulation pattern also corresponded to the levels of ABDTPA extractable and metal-organic complex bound soil Cd found in both soils. Large differences were found in grain Cd among the durum wheat cultivars grown in the same soil type, suggesting the importance of rhizosphere processes in Cd bioaccumulation and/or Cd transport processes within the plant. Distribution of Cd in parts of mature plants showed that durum grain contained up to 21 and 36% of the total amount of Cd taken up by the plants for the Orthic Gray Luvisol and Chernozemic soils, respectively. These results indicate the importance of studying Cd speciation, bioaccumulation and cycling in the environment for the management of agricultural soils and crops.     

Mapping of ionomic traits in Mimulus guttatus reveals Mo and Cd QTLs that colocalize with MOT1 homologues

Natural variation in the regulation of the accumulation of mineral nutrients and trace elements in plant tissues is crucial to plant metabolism, development, and survival across different habitats. Studies of the genetic basis of natural variation in nutrient metabolism have been facilitated by the development of ionomics. Ionomics is a functional genomic approach for the identification of the genes and gene networks that regulate the elemental composition, or ionome, of an organism. In this study, we evaluated the genetic basis of divergence in elemental composition between an inland annual and a coastal perennial accession of Mimulus guttatus using a recombinant inbred line (RIL) mapping population. Out of 20 elements evaluated, Mo and Cd were the most divergent in accumulation between the two accessions and were highly genetically correlated in the RILs across two replicated experiments. We discovered two major quantitative trait loci (QTL) for Mo accumulation, the largest of which consistently colocalized with a QTL for Cd accumulation. Interestingly, both Mo QTLs also colocalized with the two M. guttatus homologues of MOT1, the only known plant transporter to be involved in natural variation in molybdate uptake.     

Evolutionary control of leaf element composition in plants

Leaf nitrogen (N) and phosphorus (P) concentrations are correlated in plants. Higher-level phylogenetic effects can influence leaf N and P. By contrast, little is known about the phylogenetic variation in the leaf accumulation of most other elements in plant tissues, including elements with quantitatively lesser roles in metabolism than N, and elements that are nonessential for plant growth. Here the leaf composition of 42 elements is reported from a statistically unstructured data set comprising over 2000 leaf samples, representing 670 species and 138 families of terrestrial plants. Over 25% of the total variation in leaf element composition could be assigned to the family level and above for 21 of these elements. The remaining variation corresponded to differences between species within families, to differences between sites which were likely to be caused by soil and climatic factors, and to variation caused by sampling techniques. While the majority of variation in leaf mineral composition is undoubtedly associated with nonevolutionary factors, identifying higher-level phylogenetic variation in leaf elemental composition increases our understanding of terrestrial nutrient cycles and the transfer of toxic elements from soils to living organisms. Identifying mechanisms by which different plant families control their leaf elemental concentration remains a challenge.     

Relationships between nodulation and auxin level in pea roots

In the roots of 4-day-old pea plants germinated in unsterile soil from Rhizobium-inoculated seeds, a higher level of native IAA was determined than in roots of pea plants germinated in sterile soil from superficially sterilized seeds. The IAA level in plants grown from inoculated seeds increased markedly up to the age of 6 days of the plant, while in plants growing under sterile conditions it did not significantly change during the same period. Between the 6th and 10th days of the age of the plant, a decline in the IAA level was observed in roots of plante growing from inoculated seeds. It was not until after 10 days of age of the plant that the level of IAA in nodulated roots again increased.     

Accumulation of cadmium, zinc, and copper by Helianthus annuus L.: impact on plant growth and uptake of nutritional elements

We investigated the effects on physiological response, trace elements and nutrients accumulation of sunflower plants grown in soil contaminated with: 5 mg kg(-1) of Cd; 5 and 300 mg kg(-1) of Cd and Zn, respectively; 5, 300, and 400 mg kg(-1) of Cd, Zn, and Cu, respectively. Contaminants applied did not produce large effects on growth, except in Cd-Zn-Cu treatment in which leaf area and total dry matter were reduced, by 15%. The contamination with Cd alone did not affect neither growth nor physiological parameters, despite considerable amounts of Cd accumulated in roots and older leaves, with a high bioconcentration factor from soil to plant. By adding Zn and then Cu to Cd in soil, significant were the toxic effects on chlorophyll content and water relations due to greater accumulation of trace elements in tissues, with imbalances in nutrients uptake. Highly significant was the interaction between shoot elements concentration (Cd, Zn, Cu, Fe, Mg, K, Ca) and treatments. Heavy metals concentrations in roots always exceeded those in stem and leaves, with a lower translocation from roots to shoots, suggesting a strategy of sunflower to compartmentalise the potentially toxic elements in physiologically less active parts in order to preserve younger tissues.     

Precipitation of calcium, magnesium, strontium and barium in tissues of four acacia species (leguminosae: mimosoideae)

Precipitation of calcium in plants is common. There are abundant studies on the uptake and content of magnesium, strontium and barium, which have similar chemical properties to calcium, in comparison with those of calcium in plants, but studies on co-precipitation of these elements with calcium in plants are rare. In this study, we compared morphologies, distributional patterns, and elemental compositions of crystals in tissues of four Acacia species grown in the field as well as in the glasshouse. A comparison was also made of field-grown plants and glasshouse-grown plants, and of phyllodes of different ages for each species. Crystals of various morphologies and distributional patterns were observed in the four Acacia species studied. Magnesium, strontium and barium were precipitated together with calcium, mainly in phyllodes of the four Acacia species, and sometimes in branchlets and primary roots. These elements were most likely precipitated in forms of oxalate and sulfate in various tissues, including epidermis, mesophyll, parenchyma, sclerenchyma (fibre cells), pith, pith ray and cortex. In most cases, precipitation of calcium, magnesium, strontium and barium was biologically induced, and elements precipitated differed between soil types, plant species, and tissues within an individual plant; the precipitation was also related to tissue age. Formation of crystals containing these elements might play a role in regulating and detoxifying these elements in plants, and protecting the plants against herbivory.     

Respiratory potential and Se compounds in pea (Pisum sativum L.) plants grown from Se-enriched seeds

Selenium (Se) has been proved to be an essential element for humans and animals. However, less is known about its effects on plants. Pea plants were treated foliarly once (OT) and twice (TT) with Se solution during their flowering period. Seeds obtained from these plants contained 383 and 743 ng Se g(-1), respectively, and, together with control seeds from untreated plants (UT) containing 21 ng Se g(-1), were sown in soil in a greenhouse. Se content and its chemical form in young plants were studied, and its impact on plant respiratory potential, measured as terminal electron transport system (ETS) activity, determined. ETS activity was highest in young pea leaves with the highest Se content. Higher ETS activity possibly reflected increased glutathione peroxidase (GSH-Px) activity in mitochondria. The Se content of leaves and stems of plants grown from control seeds was similar to that in the seed, being around 40 ng Se g(-1). Se concentration in leaves of young plants grown from OT and TT seeds was 605%, and 1340% higher, respectively, than the control, and in their stems 355%, and 680% higher, respectively. The ratio of Se concentrations in OT and TT seeds was the same as in the leaves and stems in the young plants grown from them. SeMet was the major Se compound in Se-rich pea seeds and leaves, comprising 49% and 67% of the total Se content in OT and TT seeds, respectively, and 85% and 79% in the corresponding leaves.     

Visualising the ionome in resistant and susceptible plant–pathogen interactions

At the morphological and anatomical levels, the ionome, or the elemental composition of an organism, is an understudied area of plant biology. In particular, the ionomic responses of plant–pathogen interactions are scarcely described, and there are no studies on immune reactions. In this study we explored two X-ray fluorescence (XRF)-based ionome visualisation methods (benchtop- and synchrotron-based micro-XRF [µXRF]), as well as the quantitative inductively coupled plasma optical emission spectroscopy (ICP-OES) method, to investigate the changes that occur in the ionome of compatible and incompatible plant–pathogen interactions. We utilised the agronomically important and comprehensively studied interaction between potato (Solanum tuberosum) and the late blight oomycete pathogen Phytophthora infestans as an example. We used one late blight-susceptible potato cultivar and two resistant transgenic plant lines (only differing from the susceptible cultivar in one or three resistance genes) both in control and P. infestans-inoculated conditions. In the lesions from the compatible interaction, we observed rearrangements of several elements, including a decrease of the mobile macronutrient potassium (K) and an increase in iron (Fe) and manganese (Mn), compared with the tissue outside the lesion. Interestingly, we observed distinctly different distribution patterns of accumulation at the site of inoculation in the resistant lines for calcium (Ca), magnesium (Mg), Mn and silicon (Si) compared to the susceptible cultivar. The results reveal different ionomes in diseased plants compared to resistant plants. Our results demonstrate a technical advance and pave the way for deeper studies of the plant–pathogen ionome in the future.     

Impact of groundnut rosette disease on nutritive value and elemental composition of four varieties of peanut (Arachis hypogaea)

Proximate and elemental composition of four peanut genotypes infected with groundnut rosette disease (GRD) was examined. Moisture and ash content generally decreased while fat and energy content increased in seeds from diseased plants. Protein and carbohydrate varied between seeds of diseased and healthy plants of the different varieties with no consistent pattern. Instrumental neutron activation analysis of 10 elements within leaves, stems and seeds showed elevated levels of K, Al and Cl in leaves, stems and seeds in at least three of the four varieties infected with GRD while Na was decreased in stems but increased in seeds. While significant differences were found, Mg, Mn, Ca and Zn did not show any consistent change with respect to plant part or genotype, between diseased and healthy plants. V and Fe were found at low levels in leaves and stems and not detected in seeds. This represents the first report on the effect of GRD on the nutritive quality of peanuts.     

Identification of quantitative trait loci for rice grain element composition on an arsenic impacted soil: Influence of flowering time on genetic loci

Elements in grain crops such as iron, zinc and selenium are essential in the human diet, whereas elements such as arsenic are potentially toxic to humans. This study aims to identify quantitative trait loci (QTLs) for trace elements in rice grain. A field experiment was conducted in an arsenic enriched field site in Qiyang, China using the Bala × Azucena mapping population grown under standard field conditions. Grains were subjected to elemental analysis by inductively coupled plasma mass spectroscopy. QTLs were detected for the elemental composition within the rice grains, including for iron and selenium, which have previously been detected in this population grown at another location, indicating the stability of these QTLs. A correlation was observed between flowering time and a number of the element concentrations in grains, which was also revealed as co‐localisation between flowering time QTLs and grain element QTLs. Unravelling the environmental conditions that influence the grain ionome appears to be complex, but from the results in this study one of the major factors which controls the accumulation of elements within the grain is flowering time.