Ionomic Variation Research Articles

Machine learning technique unraveled subspecies‐specific ionomic variation with the preferential mineral enrichment in rice

AbstractBackground and ObjectivesTo enrich micronutrients in rice through breeding and to identify biofortified donor lines, screening a large diversity panel of major subspecies of rice accessions for their ionomes is necessary.FindingsInductively coupled plasma optical emission spectroscopy was deployed to profile grain ionomes from 1100 rice accessions. Classification models derived for multidimensional ionomics data using a random forest model, support vector machine, and artificial neural network predicted three distinct groups that differ in ionomic levels with higher prediction accuracy (76.8%–85.1%). While class A showed inferior lines in mineral content, class B and C represent superior lines with enriched multiple minerals. The identified contrasting lines from the modeling classifications were milled and profiled for minerals and toxic elements using inductively coupled plasma mass spectrometry and revealed donors with an elevated mineral content even higher than the Zn‐biofortified rice lines.ConclusionOverall, the result of this study provided new insights into ionomic variation among subspecies with a preferential enrichment of minerals in temperate japonica and admixed populations coincided with increased grain protein content, while in indica median mineral content is low while selected for increased amylose content.Significance and NoveltyArtificial intelligence models were developed to predict grains enriched with multiple minerals.

As(III)-Oxidizing Bacteria Alleviate Arsenite Toxicity via Reducing As Accumulation, Elevating Antioxidative Activities and Modulating Ionome in Rice (Oryza sativa L.).

Paddy rice trends to accumulate more arsenic (As) from soils than other terrestrial crops. The toxicity and mobility of As mainly depend on its chemical species. Transformation of arsenite [As(III)] into arsenate [As(V)] would be a promising method to mitigate As toxicity. In the current study, As(III)-oxidizing strain SMS11 isolated from As-contaminated soils was employed for As remediation. Co-cultured with SMS11 alleviated As(III) stress to the rice plants by increasing the length and biomass of rice shoots up to 10% and 15%, respectively. Evaluation of oxidative stress indices showed that the activity of catalase in the rice shoots was weakened when exposed to As(III), increasing the risk of hydroxyl radical (·OH) formation. When co-cultivated with the bacteria, ·OH formation was significantly inhibited in the rice shoots. The ionomes of the rice plants were impacted by the external conditions. As(III) stress significantly disturbed ionome homeostasis in the rice plants. Uptake of As simultaneously elevated the levels of macro and nutrient elements such as Mg, P, K, Ca, and Zn in the rice shoots. The ionomic variation in the rice plants under As(III) stress was mitigated by inoculated with SMS11. The results represented that the As(III)-oxidizing bacteria alleviated external As(III) stress to the rice plants through elevating antioxidative activities and modulating ionome homeostasis.

Integration of eQTL and GWAS analysis uncovers a genetic regulation of natural ionomic variation in Arabidopsis.

This study provided important insights into the genetic architecture of variations in A. thaliana leaf ionome in a cell-type-specific manner. The functional interpretation of traits associated variants by expression quantitative trait loci (eQTL) analysis is usually performed in bulk tissue samples. While the regulation of gene expression is context-dependent, such as cell-type-specific manner. In this study, we estimated cell-type abundances from 728 bulk tissue samples using single-cell RNA-sequencing dataset, and performed cis-eQTL mapping to identify cell-type-interaction eQTL (cis-eQTLs(ci)) in A. thaliana. Also, we performed Genome-wide association studies (GWAS) analyses for 999 accessions to identify the genetic basis of variations in A. thaliana leaf ionome. As a result, a total of 5,664 unique eQTL genes and 15,038 unique cis-eQTLs(ci) were significant. The majority (62.83%) of cis-eQTLs(ci) were cell-type-specific eQTLs. Using colocalization, we uncovered one interested gene AT2G25590 in Phloem cell, encoding a kind of plant Tudor-like protein with possible chromatin-associated functions, which colocalized with the most significant cis-eQTL(ci) of a Mo-related locus (Chr2:10,908,806:A:C; P = 3.27 × 10-27). Furthermore, we prioritized eight target genes associated with AT2G25590, which were previously reported in regulating the concentration of Mo element in A. thaliana. This study revealed the genetic regulation of ionomic variations and provided a foundation for further studies on molecular mechanisms of genetic variants controlling the A. thaliana ionome.

Ionomic Variation Among Tissues in Fallow Deer (Dama dama) by Sex and Age.

(1) In mammals, the mineral nutrient and trace elemental composition of the body - the ionome - differs among individuals. It has been hypothesized that these differences may be related to age and sex, both for ecotoxic and essential elements. (2) We investigated whether and how intraspecific ionomic variation is related to age and sex in Fallow deer (Dama dama). We tested the predictions that concentrations of ecotoxic elements increase with age, that ionomic variation is lower among young individuals than among older individuals, and that reproductive females (does) have the lowest concentrations of essential elements. (3) Culled animals of different sex and age were obtained from a single protected area. The animals were dissected to collect 13 tissues, and concentrations of 22 different elements were measured in a sample of each tissue. (4) We described substantial ionomic variation between individuals. Some of this variation was related to age and sex, as predicted. Based on the limited existing knowledge on chemical element allocation and metabolism in the body, sex-related differences were more difficult to interpret than age-related differences. Since reference values are absent, we could not judge about the consequences of the elemental values that we found. (5) More extensive ionomic surveys, based on a wide range of elements and tissues, are needed to enlarge the understanding of within-species ionomic variation and potential biological, ecological, and metabolic consequences.

Genome-wide association studies reveal genetic basis of ionomic variation in cassava.

As one of the most important food crops, cassava (Manihot esculenta) is the main dietary source of micronutrients for about 1 billion people. However, the ionomic variation in cassava and the underlying genetic mechanisms remain unclear so far. Herein, genome-wide association studies were performed to reveal the specific single nucleotide polymorphisms (SNPs) that affect the ionomic variation in cassava. We identified 164 SNPs with P-values lower than the threshold located in 88 loci associated with divergent ionomic variations. Among them, 13 SNPs are related to both calcium (Ca) and magnesium (Mg), and many loci for different ionomic traits seem to be clustered on specific chromosome regions. Moreover, we identified the peak SNPs in the promoter regions of Sc10g003170 (encoding methionyl-tRNA synthetase [MetRS]) and Sc18g015190 (encoding the transcriptional regulatory protein AlgP) for nitrogen (N) and phosphorus (P) accumulation, respectively. Notably, these two SNPs (chr10_32807962 and chr18_31343738) were directly correlated with the transcript levels of Sc10g003170 (MetRS) and Sc18g015190 (AlgP), which positively modulated N accumulation and P concentration in cassava, respectively. Taken together, this study provides important insight into the genetic basis of cassava natural ionomic variation, which will promote genetic breeding to improve nutrient use and accumulation of elements in cassava.

Microbiome-wide association studies between phyllosphere microbiota and ionome highlight the beneficial symbiosis of Lactococcus lactis in alleviating aluminium in cassava

The phyllosphere is one of the most abundant habitats for global microbiota. The ionome is the composition of mineral elements in plants. The correlation between phyllosphere microbiota and the ionome remains elusive in plants, especially in the most important tropical crop cassava. In this study, microbiome-wide association studies (MWASs) of thirty varieties were performed to reveal the association between phyllosphere microbiota and ionomic variations in cassava. Annotation of metagenomic species identified some species that were significantly correlated with ionomic variations in cassava. Among them, Lactococcus lactis abundance was negatively associated with leaf aluminium (Al) levels but positively related to leaf potassium (K) levels. Notably, both the reference and isolated L. lactis showed strong binding capacity to Al. Further bacterial transplantation of isolated L. lactis could significantly decrease endogenous Al levels but increase K levels in cassava, and it can also lead to increased citric acid and lactic acid levels as well as higher transcript levels of K uptake-related genes. Taken together, this study reveals the involvement of phyllosphere microbiota in ionomic variation in cassava, and the correlation between L. lactis abundance and Al and K levels provides novel insights into alleviating Al accumulation and promoting K uptake simultaneously.

Genetic architecture of root and shoot ionomes in rice (Oryza sativa L.)

Key messageAssociation analysis for ionomic concentrations of 20 elements identified independent genetic factors underlying the root and shoot ionomes of rice, providing a platform for selecting and dissecting causal genetic variants.Understanding the genetic basis of mineral nutrient acquisition is key to fully describing how terrestrial organisms interact with the non-living environment. Rice (Oryza sativa L.) serves both as a model organism for genetic studies and as an important component of the global food system. Studies in rice ionomics have primarily focused on above ground tissues evaluated from field-grown plants. Here, we describe a comprehensive study of the genetic basis of the rice ionome in both roots and shoots of 6-week-old rice plants for 20 elements using a controlled hydroponics growth system. Building on the wealth of publicly available rice genomic resources, including a panel of 373 diverse rice lines, 4.8 M genome-wide single-nucleotide polymorphisms, single- and multi-marker analysis pipelines, an extensive tome of 321 candidate genes and legacy QTLs from across 15 years of rice genetics literature, we used genome-wide association analysis and biparental QTL analysis to identify 114 genomic regions associated with ionomic variation. The genetic basis for root and shoot ionomes was highly distinct; 78 loci were associated with roots and 36 loci with shoots, with no overlapping genomic regions for the same element across tissues. We further describe the distribution of phenotypic variation across haplotypes and identify candidate genes within highly significant regions associated with sulfur, manganese, cadmium, and molybdenum. Our analysis provides critical insight into the genetic basis of natural phenotypic variation for both root and shoot ionomes in rice and provides a comprehensive resource for dissecting and testing causal genetic variants.

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, IonExplorer, 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.

Ionomic variation in leaves of 819 plant species growing in the botanical garden of Hokkaido University, Japan.

Ionomics is the measurement of total metal, metalloid, and nonmetal accumulation in living organisms. Plant ionomics has been applied to various types of research in the last decade. It has been reported that the ionome of a plant is strongly affected by its evolution and by environmental factors. In this study, we analyzed the concentration of 23 elements in leaves of 819 plant species (175 families) growing in the Botanic Garden of Hokkaido University, Japan. Relative variation estimated by the coefficient of variation in foliar concentrations of essential elements among various plant species tended to be low, whereas nickel concentration showed exceptionally large relative variation. By contrast, the relative variation in nonessential elements was high, particularly in sodium, aluminum, and arsenic. The higher relative variations in these element concentrations can be explained by the occurrence of plants that are hyperaccumulators for these elements. Differences in life forms such as herbaceous/woody species, deciduous/evergreen woody species and annual/perennial herbaceous species affected the concentration of several elements in the leaves. These differences were considered to be due to the combined factors including differences in lifespan, growth rate, and cell wall thickness of the leaves. Results of principal component analyses (based on concentration data of essential and nonessential elements in leaf samples) indicated phylogenetic influences on plant ionomes at the family level in Polypodiales, Pinales, Poales, and Ericales. Furthermore, when analyzing correlations among concentrations of all elements in each order and comparing among different orders, the results also suggested that Polypodiales, Pinales, and Poales each had a specific ion homeostasis network.

Ionomic responses of rice plants to the stresses of different arsenic species in hydroponics.

Different ionomic profiles of plants are associated with different external stresses to which they are exposed. Investigation of ionomic variation is necessary for understanding the migration and detoxification of toxic elements in plants. In the current study, rice plants were treated with arsenite, arsenate, monomethylarsonic acid and dimethylarsinic acid in hydroponics. The ionomic responses of the rice plants to different arsenic (As) species stresses were measured and analyzed. The multielement approach is more sensitive at detecting significant variations from external environmental stresses than the consideration of several individual elements. The pairs of significant correlations between elements varied based on the rice tissues and As species used in treatment, resulting in specific correlation networks. However, some pairs of correlations existed regardless of As species treatment used in this study. Positive correlations between P and Fe were observed in rice roots treated with any of the As species, implying that P and Fe share similar biological processes. The heatmap from hierarchical cluster analysis (HCA) agreed with the principal component analysis (PCA) results in ionomic differentiation between roots and shoots. Furthermore, ionomic differences between rice plants treated with different As species were identified through PCA. This study revealed that the ionomic profiles in rice plants are sufficient to detect responses to environmental perturbations. Association studies between ionomics and genomics are necessary to further understand the potential mechanisms that promote uptake or exclusion of elements in plants.

GWAS and Coexpression Network Reveal Ionomic Variation in Cultivated Peanut.

Peanut is an important legume providing products with nutrient dense including mineral nutrition. However, the genetic basis underlying the variations in the mineral composition in peanut is still unknown. Genome-wide association studies (GWAS) of the concentrations of 13 mineral elements combined with coexpression network were performed using a diverse panel of 120 genotypes mainly selected from the U.S. peanut mini core collection. A total of 36 significant quantitative trait loci (QTLs) associated with five elemental concentrations were identified with phenotypic variation explained (PVE) from 18.35% to 27.56%, in which 24 QTLs were for boron (B), 2 QTLs for copper (Cu), 6 QTLs for sodium (Na), 3 QTLs for sulfur (S), and 1 QTL for zinc (Zn). A total of 110 nonredundant candidate causal genes identified were significantly associated with elemental accumulation, which included one high-priority overlap (HPO) candidate gene arahy.KQD4NT, an important elemental/metal transporter gene located on LGB04 with position 5,413,913-5,417,353.

Understanding variation in salamander ionomes: A nutrient balance approach

AbstractEcological stoichiometry uses information on a few key biological elements (C, N and P) to explain complex ecological patterns. Although factors driving variation in these elements are well established, expanding stoichiometric principles to explore dynamics of the many other essential elements comprising biological tissues (i.e. the ionome) is needed to determine their metabolic relationships and better understand biological control of elemental flows through ecosystems.In this paper, we report observations of ionomic variation in two species of salamander (Ambystoma opacumandA. talpoideum) across ontogenic stages using specimens from biological collections of two wetlands sampled over a 30‐year period. This unique data set allowed us to explore the extent of ionomic variation between species, among ontogenic stages, between sites and through time.We found species‐ and, to a lesser extent, site‐specific differences in C, N and P along with 13 other elements forming salamander ionomes but saw no evidence of temporal changes. Salamander ionomic composition was most strongly related to ontogeny with relatively higher concentrations of many elements in adult males (i.e. Ca, P, S, Mg, Zn and Cu) compared to metamorphic juveniles, which had greater amounts of C, Fe and Mn.In addition to patterns of individual elements, covariance among elements was used to construct multi‐elemental nutrient balances, which revealed differences in salamander elemental composition between species and sites and changes in elemental proportions across ontogenic development. These multi‐elemental balances distinguished among species‐site‐ontogenic stage groups better than using only C, N and P.Overall, this study highlights the responsiveness of consumer ionomes to life‐history and environmental variation while reflecting underlying relationships among elements tied to biological function. As such, ionomic studies can provide important insights into factors shaping consumer elemental composition and for predicting how these changes might affect higher‐order ecological processes.

Genome-Wide Association Studies Reveal the Genetic Basis of Ionomic Variation in Rice.

Rice (Oryza sativa) is an important dietary source of both essential micronutrients and toxic trace elements for humans. The genetic basis underlying the variations in the mineral composition, the ionome, in rice remains largely unknown. Here, we describe a comprehensive study of the genetic architecture of the variation in the rice ionome performed using genome-wide association studies (GWAS) of the concentrations of 17 mineral elements in rice grain from a diverse panel of 529 accessions, each genotyped at ∼6.4 million single nucleotide polymorphism loci. We identified 72 loci associated with natural ionomic variations, 32 that are common across locations and 40 that are common within a single location. We identified candidate genes for 42 loci and provide evidence for the causal nature of three genes, the sodium transporter gene Os-HKT1;5 for sodium, Os-MOLYBDATE TRANSPORTER1;1 for molybdenum, and Grain number, plant height, and heading date7 for nitrogen. Comparison of GWAS data from rice versus Arabidopsis (Arabidopsis thaliana) also identified well-known as well as new candidates with potential for further characterization. Our study provides crucial insights into the genetic basis of ionomic variations in rice and serves as an important foundation for further studies on the genetic and molecular mechanisms controlling the rice ionome.

Worldwide Genetic Diversity for Mineral Element Concentrations in Rice Grain

ABSTRACTWith the aim of identifying rice (Oryza spp.) germplasm having enhanced grain nutritional value, the mineral nutrient and trace element concentrations (or ionome) of whole (unmilled) grains from a set of 1763 rice accessions of diverse geographic and genetic origin were evaluated. Seed for analysis of P, Mg, K, S, Ca, As, Cd, Co, Cu, Fe, Mn, Mo, Ni, Rb, Sr, and Zn concentrations by inductively coupled plasma mass spectrometry was produced over 2 yr in Beaumont, TX, under both flooded and unflooded watering regimes. The distributions of all element concentrations analyzed were skewed toward higher concentration. A significant portion of this ionomic variation has a genetic basis (broad sense heritabilities 0.14–0.75), indicating an ability to breed for improved grain concentration of all elements except possibly Ni. Variation in grain elemental concentrations was not strongly associated with plant height, heading time, or grain shape, suggesting these physiological factors are not of primary importance in controlling ionomic variation in rice grain. Accessions high in specific elements were sometimes found to have similar genetic or geographic origins, suggesting they share a heritable mechanism underlying their enhanced ionomes. For example, accessions with high Ca, Mg, or K were more common in the indica than in the japonica subgroup; low As was most common among temperate japonica accessions; and several lines high in Mo originated in Malaysia or adjacent Brunei.

An update on magnesium homeostasis mechanisms in plants

Worldwide, nearly two-thirds of the population do not consume the recommended amount of magnesium (Mg) in their diet. Furthermore, low Mg status (hypomagnesaemia) is known to contribute to a number of human chronic disease conditions. Because the principal dietary Mg source is of plant origin, agronomic and genetic biofortification strategies are aimed at improving nutritional Mg content in food crops to overcome this mineral deficiency in humans. This update incorporates the contributions of annotated permeases involved in Mg uptake, storage and recycling with a schematic model of Mg movement at the organ and cellular levels in the model species Arabidopsis thaliana. Furthermore, approaches using mutagenesis or natural ionomic variation to identify loci involved in Mg homeostasis in roots, leaves and seeds will be summarised. A brief overview will be presented on how Arabidopsis research can help to develop strategies for biofortification of crops.

Ionomic variation characterization in African leafy vegetables for micronutrients using xrf and hplc

Beside the phytochemical, ionomic fingerprinting represents the inorganic trace element composition of the cellular and organismal component. High-throughput elemental analysis technologies, such as X-Ray Fluorescence (XRF), are applied to ionomic analysis whereas phyto-chemical analyses tend to be in vitro. Both could contribute to: (a) insights on ionome-phytochem micronutrient composition; (b) genetic diversity variant discrimination among accessions to allow simple grouping;(c) core and/or reserve collections rationalization; (d) integration of bioinformatic and genetic tools; and (e) micronutrient-dense varietal improvement and/or cropping decisions. First, variant discrimination was appraised on individual element criterion (e.g. K or Ca or Fe or Zn). Second, on a multiple element (K & Ca & Fe & Zn) condition upon which nutrahealth-implied ionomic variant conditions were rationalized as: (a) Core ‘exceptional’ grade collections scored between E8 and E10;(b) Core ‘Medium’ grades (M5-M7); and (c) ‘Least’ exceptional (Ll-L4) scored and regarded as reserve collections. Objectives were to: (1) Investigate a phyotchem background among the selected African Leafy Vegetables (ALVs) for coupling with ionome grading; (2) Assess variation among accessions based on single element criterion; (3) Characterize cumulative nutrahealth-implied ionomic variation among ALVs. Eleven ALV accessions were raised from seed at the University of Nairobi Greenhouse (2006) and leafy parts harvested. XRF was carried out at the Institute ofNuclear Science and Technology, University of Nairobi. High Performance Liquid Chromatographic (HPLC) analyses were done at the Tanzania Food and Nutritional Centre. Highly significant density variation (p< 0.001) among accessions due to Lutein and â-carotene suggested the phytochem effectiveness for variant discrimination accounting for 0.79 and 0.87 of (R2) variation. The single element K discriminator basis was highly significant (p