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.     

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.     

Plant hydraulic lift of soil water – implications for crop production and land restoration

Zinc deficiency is a well-documented problem in food crops, causing decreased crop yields and nutritional quality. Generally, the regions in the world with Zn-deficient soils are also characterized by widespread Zn deficiency in humans. Recent estimates indicate that nearly half of world population suffers from Zn deficiency. Cereal crops play an important role in satisfying daily calorie intake in developing world, but they are inherently very low in Zn concentrations in grain, particularly when grown on Zn-deficient soils. The reliance on cereal-based diets may induce Zn deficiency-related health problems in humans, such as impairments in physical development, immune system and brain function. Among the strategies being discussed as major solution to Zn deficiency, plant breeding strategy (e.g., genetic biofortification) appears to be a most sustainable and cost-effective approach useful in improving Zn concentrations in grain. The breeding approach is, however, a long-term process requiring a substantial effort and resources. A successful breeding program for biofortifying food crops with Zn is very much dependent on the size of plant-available Zn pools in soil. In most parts of the cereal-growing areas, soils have, however, a variety of chemical and physical problems that significantly reduce availability of Zn to plant roots. Hence, the genetic capacity of the newly developed (biofortified) cultivars to absorb sufficient amount of Zn from soil and accumulate it in the grain may not be expressed to the full extent. It is, therefore, essential to have a short-term approach to improve Zn concentration in cereal grains. Application of Zn fertilizers or Zn-enriched NPK fertilizers (e.g., agronomic biofortification) offers a rapid solution to the problem, and represents useful complementary approach to on-going breeding programs. There is increasing evidence showing that foliar or combined soil+foliar application of Zn fertilizers under field conditions are highly effective and very practical way to maximize uptake and accumulation of Zn in whole wheat grain, raising concentration up to 60 mg Zn kg⁻¹. Zinc-enriched grains are also of great importance for crop productivity resulting in better seedling vigor, denser stands and higher stress tolerance on potentially Zn-deficient soils. Agronomic biofortification strategy appears to be essential in keeping sufficient amount of available Zn in soil solution and maintaining adequate Zn transport to the seeds during reproductive growth stage. Finally, agronomic biofortification is required for optimizing and ensuring the success of genetic biofortification of cereal grains with Zn. In case of greater bioavailability of the grain Zn derived from foliar applications than from soil, agronomic biofortification would be a very attractive and useful strategy in solving Zn deficiency-related health problems globally and effectively.     

Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana

In order to grow on soils that vary widely in chemical composition, plants have evolved mechanisms for regulating the elemental composition of their tissues to balance the mineral nutrient and trace element bioavailability in the soil with the requirements of the plant for growth and development. The biodiversity that exists within a species can be utilized to investigate how regulatory mechanisms of individual elements interact and to identify genes important for these processes. We analyzed the elemental composition (ionome) of a set of 96 wild accessions of the genetic model plant Arabidopsis thaliana grown in hydroponic culture and soil using inductively coupled plasma mass spectrometry (ICP-MS). The concentrations of 17-19 elements were analyzed in roots and leaves from plants grown hydroponically, and leaves and seeds from plants grown in artificial soil. Significant genetic effects were detected for almost every element analyzed. We observed very few correlations between the elemental composition of the leaves and either the roots or seeds. There were many pairs of elements that were significantly correlated with each other within a tissue, but almost none of these pairs were consistently correlated across tissues and growth conditions, a phenomenon observed in several previous studies. These results suggest that the ionome of a plant tissue is variable, yet tightly controlled by genes and gene × environment interactions. The dataset provides a valuable resource for mapping studies to identify genes regulating elemental accumulation. All of the ionomic data is available at www.ionomicshub.org.     

Carotenoid biofortification in crop plants: citius,altius, fortius

Carotenoids are indispensable for human health, required as precursors of vitamin A and efficient antioxidants. However, these plant pigments that play a vital role in photosynthesis are represented at insufficient levels in edible parts of several crops, which creates a need for increasing their content or optimizing their composition through biofortification. In particular, vitamin A deficiency, a severe health problem affecting the lives of millions in developing countries, has triggered the development of a series of high-provitamin A crops, including Golden Rice as the best-known example. Further carotenoid-biofortified crops have been generated by using genetic engineering approaches or through classical breeding. In this review, we depict carotenoid metabolism in plants and provide an update on the development of carotenoid-biofortified plants and their potential to meet needs and expectations. Furthermore, we discuss the possibility of using natural variation for carotenoid biofortification and the potential of gene editing tools. This article is part of a Special Issue entitled Carotenoids recent advances in cell and molecular biology edited by Johannes von Lintig and Loredana Quadro.     

Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine

The diets of over two-thirds of the world's population lack one or more essential mineral elements. This can be remedied through dietary diversification, mineral supplementation, food fortification, or increasing the concentrations and/or bioavailability of mineral elements in produce (biofortification). This article reviews aspects of soil science, plant physiology and genetics underpinning crop biofortification strategies, as well as agronomic and genetic approaches currently taken to biofortify food crops with the mineral elements most commonly lacking in human diets: iron (Fe), zinc (Zn), copper (Cu), calcium (Ca), magnesium (Mg), iodine (I) and selenium (Se). Two complementary approaches have been successfully adopted to increase the concentrations of bioavailable mineral elements in food crops. First, agronomic approaches optimizing the application of mineral fertilizers and/or improving the solubilization and mobilization of mineral elements in the soil have been implemented. Secondly, crops have been developed with: increased abilities to acquire mineral elements and accumulate them in edible tissues; increased concentrations of 'promoter' substances, such as ascorbate, β-carotene and cysteine-rich polypeptides which stimulate the absorption of essential mineral elements by the gut; and reduced concentrations of 'antinutrients', such as oxalate, polyphenolics or phytate, which interfere with their absorption. These approaches are addressing mineral malnutrition in humans globally.     

Plant nutrition for sustainable development and global health

Background

Plants require at least 14 mineral elements for their nutrition. These include the macronutrients nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg) and sulphur (S) and the micronutrients chlorine (Cl), boron (B), iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), nickel (Ni) and molybdenum (Mo). These are generally obtained from the soil. Crop production is often limited by low phytoavailability of essential mineral elements and/or the presence of excessive concentrations of potentially toxic mineral elements, such as sodium (Na), Cl, B, Fe, Mn and aluminium (Al), in the soil solution.

Scope

This article provides the context for a Special Issue of the Annals of Botany on ‘Plant Nutrition for Sustainable Development and Global Health’. It provides an introduction to plant mineral nutrition and explains how mineral elements are taken up by roots and distributed within plants. It introduces the concept of the ionome (the elemental composition of a subcellular structure, cell, tissue or organism), and observes that the activities of key transport proteins determine species-specific, tissue and cellular ionomes. It then describes how current research is addressing the problems of mineral toxicities in agricultural soils to provide food security and the optimization of fertilizer applications for economic and environmental sustainability. It concludes with a perspective on how agriculture can produce edible crops that contribute sufficient mineral elements for adequate animal and human nutrition.     

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.     

Mechanism of Zinc absorption in plants: uptake,transport, translocation and accumulation

Zinc (Zn) is an essential micronutrient for plants and animals. Unfortunately, deficiency of Zn in humans has increased on a global scale. The main reason of this micronutrient deficiency is dietary intakes of food with low Zn levels. Adoption of biofortification approaches would result in Zn enrichment of target tissue to a considerable extent. However, there is a basic need to understand Zn absorption mechanisms in plants prior to exploitation of such practical approaches. Zn absorption is a complex physiological trait which is mainly governed by Zn transporters and metal chelators of plant system. Plant growth stage, edaphic factors, season etc. also influence Zn efficiency of particular species. Molecular studies in Zn hyperaccumulators have already demonstrated the participation of specific Zn transporters, vacuolar sequestration and detoxification mechanisms in maintenance of Zn homeostasis. These have been described in detail in present review and provide opportunities for utilization in biofortification programmes. However, issues such as lesser bioavailability of Zn in target organ, uptake of toxic divalent cations (Cd, Ni, Pb, As etc.) along with Zn, sink activity and dilution in Zn concentration in response to sink number etc. in biofortified crops need further investigation. In order to design novel strategy in biofortification programmes, future researches should focus on physiological performance and yield penalties in concerned crop, metabolic load in term of organic acid production and crosstalk of Zn with other mineral nutrients under low and high Zn conditions.     

Systematic age‐, organ‐, and diet‐associated ionome remodeling and the development of ionomic aging clocks

Aging involves coordinated yet distinct changes in organs and systems throughout life, including changes in essential trace elements. However, how aging affects tissue element composition (ionome) and how these changes lead to dysfunction and disease remain unclear. Here, we quantified changes in the ionome across eight organs and 16 age groups of mice. This global profiling revealed novel interactions between elements at the level of tissue, age, and diet, and allowed us to achieve a broader, organismal view of the aging process. We found that while the entire ionome steadily transitions along the young‐to‐old trajectory, individual organs are characterized by distinct element changes. The ionome of mice on calorie restriction (CR) moved along a similar but shifted trajectory, pointing that at the organismal level this dietary regimen changes metabolism in order to slow down aging. However, in some tissues CR mimicked a younger state of control mice. Even though some elements changed with age differently in different tissues, in general aging was characterized by the reduced levels of elements as well as their increased variance. The dataset we prepared also allowed to develop organ‐specific, ionome‐based markers of aging that could help monitor the rate of aging. In some tissues, these markers reported the lifespan‐extending effect of CR. These aging biomarkers have the potential to become an accessible tool to test the age‐modulating effects of interventions.     

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.     

Biofortifying crops with essential mineral elements

Humans require more than 22 mineral elements, which can all be supplied by an appropriate diet. However, the diets of populations subsisting on cereals, or inhabiting regions where soil mineral imbalances occur, often lack Fe, Zn, Ca, Mg, Cu, I or Se. Traditional strategies to deliver these minerals to susceptible populations have relied on supplementation or food fortification programs. Unfortunately, these interventions have not always been successful. An alternative solution is to increase mineral concentrations in edible crops. This is termed 'biofortification'. It can be achieved by mineral fertilization or plant breeding. There is considerable genetic variation in crop species that can be harnessed for sustainable biofortification strategies. Varieties with increased mineral concentrations in their edible portions are already available, and new genotypes with higher mineral densities are being developed.     

The Influence of Iron Availability on Human Salivary Microbial Community Composition

It is a well-recognized fact that the composition of human salivary microbial community is greatly affected by its nutritional environment. However, most studies are currently focused on major carbon or nitrogen sources with limited attention to trace elements like essential mineral ions. In this study, we examined the effect of iron availability on the bacterial profiles of an in vitro human salivary microbial community as iron is an essential trace element for the survival and proliferation of virtually all microorganisms. Analysis via a combination of PCR with denaturing gradient gel electrophoresis demonstrated a drastic change in species composition of an in vitro human salivary microbiota when iron was scavenged from the culture medium by addition of the iron chelator 2,2'-bipyridyl. This shift in community profile was prevented by the presence of excessive ferrous iron (Fe(2+)). Most interestingly, under iron deficiency, the in vitro grown salivary microbial community became dominated by several hemolytic bacterial species, including Streptococcus spp., Gemella spp., and Granulicatella spp. all of which have been implicated in infective endocarditis. These data provide evidence that iron availability can modulate host-associated oral microbial communities, resulting in a microbiota with potential clinical impact.     

植物缺铁应答bHLH转录因子研究进展

铁是植物生命活动必需的微量元素之一,土壤中有效铁含量较低,易导致植物缺铁。bHLH转录因子家族多个成员参与植物缺铁响应,发挥重要的调控作用。为深入了解植物对缺铁的反应机制,文中对植物缺铁胁迫应答的bHLH转录因子的结构、分类和功能及其调控机制、介导的缺铁胁迫信号通路进行综述,为应用bHLH转录因子培育缺铁耐受作物或富铁作物提供理论依据和设计策略。     

Phenotypic profile linked to inhibition of the major Zn influx system in Salmonella enterica: proteomics and ionomics investigations

Zinc is required for a wide variety of cellular functions and plays a key role in bacterial metabolism and virulence. However, Zn can also be toxic and, therefore, its influx is tightly regulated. The high affinity zinc uptake transporter ZnuABC is the main Zn influx system in Salmonella enterica under conditions of Zn starvation. It has been shown that deletion of the gene encoding for its periplasmic subunit ZnuA significantly affects S. Typhimurium growth rate and virulence, highlighting the importance of this system in the host-pathogen interaction. To gain further insight into the mechanisms involved in Zn influx regulation, we characterized the main alterations in the ionome and proteome of S. Typhimurium wild type and znuA mutant strains grown either under Zn starvation or under Zn-replete conditions. We found significant differences in the element profile and protein expression that were reversed by Zn supplementation. In particular, several of the differentially regulated proteins are predicted to be metal-binding proteins. Interestingly, their over-expression in the znuA mutant strain strictly depends on Zn starvation and correlates with the differences found at the ionome level. In conclusion, our data demonstrate that inhibition of Zn influx has relevant effects either on the bacterial ionome or proteome and shed new light on the role of the ZnuABC system and Zn influx in S. Typhimurium pathogenicity.     

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.     

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。     

Formation of folates by microorganisms: towards the biotechnological production of this vitamin

Folates (vitamin B₉) are essential micronutrients which function as cofactors in one-carbon transfer reactions involved in the synthesis of nucleotides and amino acids. Folate deficiency is associated with important diseases such as cancer, anemia, cardiovascular diseases, or neural tube defects. Epidemiological data show that folate deficiency is still highly prevalent in many populations. Hence, food fortification with synthetic folic acid (i.e., folic acid supplementation) has become mandatory in many developed countries. However, folate biofortification of staple crops and dairy products as well as folate bioproduction using metabolically engineered microorganisms are promising alternatives to folic acid supplementation. Here, we review the current strategies aimed at overproducing folates in microorganisms, in view to implement an economic feasible process for the biotechnological production of the vitamin.

     

Critical evaluation of strategies for mineral fortification of staple food crops

Staple food crops, in particular cereal grains, are poor sources of key mineral nutrients. As a result, the world’s poorest people, generally those subsisting on a monotonous cereal diet, are also those most vulnerable to mineral deficiency diseases. Various strategies have been proposed to deal with micronutrient deficiencies including the provision of mineral supplements, the fortification of processed food, the biofortification of crop plants at source with mineral-rich fertilizers and the implementation of breeding programs and genetic engineering approaches to generate mineral-rich varieties of staple crops. This review provides a critical comparison of the strategies that have been developed to address deficiencies in five key mineral nutrients—iodine, iron, zinc, calcium and selenium—and discusses the most recent advances in genetic engineering to increase mineral levels and bioavailability in our most important staple food crops.