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Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches

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A special issue of Plants (ISSN 2223-7747).

Deadline for manuscript submissions: closed (30 November 2019) | Viewed by 81006

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Dr. Eleonora Cominelli

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Istituto di Biologia e Biotecnologia Agraria, CNR, Milano, Italy
Interests: seed nutritional quality; phytic acid metabolism; ABC-MRP type phytic acid transporter; lpa mutants; abiotic stresses; mineral accumulation
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Dr. Francesca Sparvoli

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Istituto di Biologia e Biotecnologia Agraria, CNR, Milano, Italy
Interests: legumes; Phaseolus vulgaris; seed; seed protein; seed nutritional quality; phytic acid metabolism; ABC-MRP type phytic acid transporter; lpa mutants
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Prof. Dr. Roberto Pilu

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Department of Agricultural and Environmental Sciences—Production, Landscape, Agroenergy, Università degli Studi di Milano, Via G. Celoria 2, 20133 Milan, Italy
Interests: breeding; molecular plant breeding; plant genetics; plant genomics; agrobiodiversity; germplasm bank
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Special Issue Information

Dear Colleagues,

One of the main “antinutrients” that affects mineral bioavailability is phytic acid, the main phosphorous storage form, a strong cation chelator. Different low phytic acid (lpa) mutants have been isolated in different crops and in some cases the increased mineral bioavailability from these mutant seeds was shown. Phytic acid is not only a storage compound, but also a very important signalling molecule, involved in different regulatory processes. For this reason, some lpa mutants show negative pleiotropic effects.

Another goal of biofortification is to enhance the seed mineral concentration, modulating mineral uptake, chelation and storage, without interfering with general mineral homeostasis in the plant. Different genes have been described as good candidates to reach this objective, such as genes encoding for metal transporters (i.e. vacuolar iron transporter, VIT; zinc-regulated transporter, ZRT), mineral storage proteins (i.e. Ferritin), transcription factors regulating seed mineral concentration (i.e. bHLH, bZIP, NAC) and genes involved in the synthesis of metal chelators (i.e. nicothianamine synthase, NAS).

Breeding programs or transgenic approaches aimed to develop biofortified crops should exploit basic plant science results in order to maximize the utility of the modified crops, avoiding the display of negative pleiotropic effects.

This Special Issue aims to highlight new developments in our understanding of how perturbation in phytic acid content or in seed mineral accumulation contributes to plant function, growth, and response to the environment.

Contributions to this Special Issue are invited from scientists working at all system levels, including the molecule, cell, organism and environment/ecological perspectives.

Dr. Eleonora Cominelli
Dr. Francesca Sparvoli
Dr. Roberto Pilu
Guest Editors

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Keywords

biofortification
low phytic acid (lpa) mutants
metal chelators
metal transporter
mineral deficiencies
mineral storage protein
phytic acid
signal transduction

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Published Papers (12 papers)

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Editorial

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8 pages, 250 KiB

Open AccessEditorial

Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches

by Eleonora Cominelli, Roberto Pilu and Francesca Sparvoli

Plants 2020, 9(5), 553; https://doi.org/10.3390/plants9050553 - 26 Apr 2020

Cited by 21 | Viewed by 3503

Abstract

Mineral deficiencies, particularly for iron and zinc, affect over two billion people worldwide, mainly in developing countries where diets are based on the consumption of staple crops. Mineral biofortification includes different approaches aimed to increase mineral concentration and to improve mineral bioavailability in the edible parts of plants, particularly the seeds. A multidisciplinary approach, including agronomic, genetic, physiological, and molecular expertise, is necessary to obtain detailed knowledge of the complex homeostatic mechanisms that tightly regulate seed mineral concentrations and the molecules and mechanisms that determine mineral bioavailability, necessary to reach the biofortification objectives. To increase bioavailability, one strategy is to decrease seed content of phytic acid, a highly electronegative molecule present in the cell that chelates positively charged metal ions, many of which are important for human nutrition. All the contributions of the current Special Issue aim at describing new results, reviewing the literature, and also commenting on some of the economic and sociological aspects concerning biofortification research. A number of contributions are related to the study of mineral transport, seed accumulation, and approaches to increase seed micronutrient concentration. The remaining ones are mainly focused on the study of low phytic acid mutants. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

Research

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15 pages, 2635 KiB

Open AccessArticle

Gene Expression Pattern of Vacuolar-Iron Transporter-Like (VTL) Genes in Hexaploid Wheat during Metal Stress

by Shivani Sharma, Gazaldeep Kaur, Anil Kumar, Varsha Meena, Hasthi Ram, Jaspreet Kaur and Ajay Kumar Pandey

Plants 2020, 9(2), 229; https://doi.org/10.3390/plants9020229 - 11 Feb 2020

Cited by 29 | Viewed by 5347

Abstract

Iron is one of the important micronutrients that is required for crop productivity and yield-related traits. To address the Fe homeostasis in crop plants, multiple transporters belonging to the category of major facilitator superfamily are being explored. In this direction, earlier vacuolar iron transporters (VITs) have been reported and characterized functionally to address biofortification in cereal crops. In the present study, the identification and characterization of new members of vacuolar iron transporter-like proteins (VTL) was performed in wheat. Phylogenetic distribution demonstrated distinct clustering of the identified VTL genes from the previously known VIT genes. Our analysis identifies multiple VTL genes from hexaploid wheat with the highest number genes localized on chromosome 2. Quantitative expression analysis suggests that most of the VTL genes are induced mostly during the Fe surplus condition, thereby reinforcing their role in metal homeostasis. Interestingly, most of the wheat VTL genes were also significantly up-regulated in a tissue-specific manner under Zn, Mn and Cu deficiency. Although, no significant changes in expression of wheat VTL genes were observed in roots under heavy metals, but TaVTL2, TaVTL3 and TaVTL5 were upregulated in the presence of cobalt stress. Overall, this work deals with the detailed characterization of wheat VTL genes that could provide an important genetic framework for addressing metal homeostasis in bread wheat. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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11 pages, 2124 KiB

Open AccessArticle

Genotypic Differences in the Effect of P Fertilization on Phytic Acid Content in Rice Grain

by Ayaka Fukushima, Ishara Perera, Koki Hosoya, Tatsuki Akabane and Naoki Hirotsu

Plants 2020, 9(2), 146; https://doi.org/10.3390/plants9020146 - 23 Jan 2020

Cited by 6 | Viewed by 3208

Abstract

Phytic acid (PA) prevents the absorption of minerals in the human intestine, and it is regarded as an antinutrient. Low PA rice is beneficial because of its higher Zn bioavailability and it is suggested that the gene expression level of myo-inositol 3-phosphate synthase 1 (INO1) in developing grain is a key factor to explain the genotypic difference in PA accumulation among natural variants of rice. P fertilization is also considered to affect the PA content, but it is not clear how it affects INO1 gene expression and the PA content in different genotypes. Here, we investigated the effect of P fertilization on the PA content in two contrasting rice genotypes, with low and high PA accumulation, respectively. Based on the results of the analysis of the PA content, inorganic P content, INO1 gene expression, and xylem sap inorganic P content, we concluded that the effect of P fertilization on PA accumulation in grain differed with the genotype, and it was regulated by multiple mechanisms. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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14 pages, 2687 KiB

Open AccessArticle

Mineral Element Composition in Grain of Awned and Awnletted Wheat (Triticum aestivum L.) Cultivars: Tissue-Specific Iron Speciation and Phytate and Non-Phytate Ligand Ratio

by Paula Pongrac, Iztok Arčon, Hiram Castillo-Michel and Katarina Vogel-Mikuš

Plants 2020, 9(1), 79; https://doi.org/10.3390/plants9010079 - 8 Jan 2020

Cited by 20 | Viewed by 3861

Abstract

In wheat (Triticum aestivum L.), the awns—the bristle-like structures extending from lemmas—are photosynthetically active. Compared to awned cultivars, awnletted cultivars produce more grains per unit area and per spike, resulting in significant reduction in grain size, but their mineral element composition remains unstudied. Nine awned and 11 awnletted cultivars were grown simultaneously in the field. With no difference in 1000-grain weight, a larger calcium and manganese—but smaller iron (Fe) concentrations—were found in whole grain of awned than in awnletted cultivars. Micro X-ray absorption near edge structure analysis of different tissues of frozen-hydrated grain cross-sections revealed that differences in total Fe concentration were not accompanied by differences in Fe speciation (64% of Fe existed as ferric and 36% as ferrous species) or Fe ligands (53% were phytate and 47% were non-phytate ligands). In contrast, there was a distinct tissue-specificity with pericarp containing the largest proportion (86%) of ferric species and nucellar projection (49%) the smallest. Phytate ligand was predominant in aleurone, scutellum and embryo (72%, 70%, and 56%, respectively), while nucellar projection and pericarp contained only non-phytate ligands. Assuming Fe bioavailability depends on Fe ligands, we conclude that Fe bioavailability from wheat grain is tissue specific. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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14 pages, 1390 KiB

Open AccessArticle

lpa1-5525: A New lpa1 Mutant Isolated in a Mutagenized Population by a Novel Non-Disrupting Screening Method

by Giulia Borlini, Cesare Rovera, Michela Landoni, Elena Cassani and Roberto Pilu

Plants 2019, 8(7), 209; https://doi.org/10.3390/plants8070209 - 6 Jul 2019

Cited by 12 | Viewed by 3468

Abstract

Phytic acid, or myo-inositol 1,2,3,4,5,6-hexakisphosphate, is the main storage form of phosphorus in plants. It is localized in seeds, deposited as mixed salts of mineral cations in protein storage vacuoles; during germination, it is hydrolyzed by phytases to make available P together with all the other cations needed for seed germination. When seeds are used as food or feed, phytic acid and the bound cations are poorly bioavailable for human and monogastric livestock due to their lack of phytase activity. Therefore, reducing the amount of phytic acid is one strategy in breeding programs aimed to improve the nutritional properties of major crops. In this work, we present data on the isolation of a new maize (Zea mays L.) low phytic acid 1 (lpa1) mutant allele obtained by transposon tagging mutagenesis with the Ac element. We describe the generation of the mutagenized population and the screening to isolate new lpa1 mutants. In particular, we developed a fast, cheap and non-disrupting screening method based on the different density of lpa1 seed compared to the wild type. This assay allowed the isolation of the lpa1-5525 mutant characterized by a new mutation in the lpa1 locus associated with a lower amount of phytic phosphorus in the seeds in comparison with the wild type. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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13 pages, 1104 KiB

Open AccessEditor’s ChoiceArticle

Effect of Phosphorus Fertilization on the Growth, Photosynthesis, Nitrogen Fixation, Mineral Accumulation, Seed Yield, and Seed Quality of a Soybean Low-Phytate Line

by Nisar Ahmad Taliman, Qin Dong, Kohei Echigo, Victor Raboy and Hirofumi Saneoka

Plants 2019, 8(5), 119; https://doi.org/10.3390/plants8050119 - 8 May 2019

Cited by 88 | Viewed by 9597

Abstract

Crop seed phosphorus (P) is primarily stored in the form of phytate, which is generally indigestible by monogastric animals. Low-phytate soybean lines have been developed to solve various problems related to seed phytate. There is little information available on the effects of P fertilization on productivity, physiological characteristics, and seed yield and quality in low-phytate soybeans. To address this knowledge gap, studies were conducted with a low-phytate line and two normal-phytate cultivars from western Japan when grown under high- and low-P fertilization. The whole plant dry weight, leaf photosynthesis, dinitrogen fixation, and nodule dry weight at the flowering stage were higher in the higher P application level, but were not different between the low-phytate line and normal-phytate cultivars. As expected, seed yield was higher in the higher level of P application for all lines. Notably, it was higher in the low-phytate line as compared with the normal-phytate cultivars at both levels of fertilizer P. The total P concentration in the seeds of the low-phytate line was the same as that of the normal-phytate cultivars, but the phytate P concentration in the low-phytate line was about 50% less than that of the normal-phytate cultivars. As a result the molar ratio of phytic acid to Zn, Fe, Mn, and Cu in seed were also significantly lower in the low-phytate line. From these results, it can be concluded that growth after germination, leaf photosynthesis, nitrogen fixation, yield and seed quality were not less in the low-phytate soybean line as compared with two unrelated normal-phytate cultivars currently grown in Japan, and that low-phytate soybeans may improve the bioavailability of microelements. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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12 pages, 2643 KiB

Open AccessEditor’s ChoiceArticle

Mutation of Inositol 1,3,4-trisphosphate 5/6-kinase6 Impairs Plant Growth and Phytic Acid Synthesis in Rice

by Meng Jiang, Yang Liu, Yanhua Liu, Yuanyuan Tan, Jianzhong Huang and Qingyao Shu

Plants 2019, 8(5), 114; https://doi.org/10.3390/plants8050114 - 29 Apr 2019

Cited by 63 | Viewed by 6108

Abstract

Inositol 1,3,4-trisphosphate 5/6-kinase (ITPK) is encoded by six genes in rice (OsITPK1-6). A previous study had shown that nucleotide substitutions of OsITPK6 could significantly lower the phytic acid content in rice grains. In the present study, the possibility of establishing a genome editing-based method for breeding low-phytic acid cultivars in rice was explored, in conjunction with the functional determination of OsITPK6. Four OsITPK6 mutant lines were generated by targeted mutagenesis of the gene’s first exon using the CRISPR/Cas9 method, one (ositpk6_1) with a 6-bp in-frame deletion, and other three with frameshift mutations (ositpk6_2, _3, and _4). The frameshift mutations severely impaired plant growth and reproduction, while the effect of ositpk6_1 was relatively limited. The mutant lines ositpk6_1 and _2 had significantly lower levels (−10.1% and −32.1%) of phytic acid and higher levels (4.12- and 5.18-fold) of inorganic phosphorus compared with the wild-type (WT) line. The line ositpk6_1 also showed less tolerance to osmotic stresses. Our research demonstrates that mutations of OsITPK6, while effectively reducing phytic acid biosynthesis in rice grain, could significantly impair plant growth and reproduction. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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Review

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11 pages, 1419 KiB

Open AccessEditor’s ChoiceReview

Can Inositol Pyrophosphates Inform Strategies for Developing Low Phytate Crops?

by Catherine Freed, Olusegun Adepoju and Glenda Gillaspy

Plants 2020, 9(1), 115; https://doi.org/10.3390/plants9010115 - 17 Jan 2020

Cited by 18 | Viewed by 6790

Abstract

Inositol pyrophosphates (PP-InsPs) are an emerging class of “high-energy” intracellular signaling molecules, containing one or two diphosphate groups attached to an inositol ring, that are connected with phosphate sensing, jasmonate signaling, and inositol hexakisphosphate (InsP₆) storage in plants. While information regarding this new class of signaling molecules in plants is scarce, the enzymes responsible for their synthesis have recently been elucidated. This review focuses on InsP₆ synthesis and its conversion into PP-InsPs, containing seven and eight phosphate groups (InsP₇ and InsP₈). These steps involve two types of enzymes: the ITPKs that phosphorylate InsP₆ to InsP₇, and the PPIP5Ks that phosphorylate InsP₇ to InsP₈. This review also considers the potential roles of PP-InsPs in plant hormone and inorganic phosphate (Pi) signaling, along with an emerging role in bioenergetic homeostasis. PP-InsP synthesis and signaling are important for plant breeders to consider when developing strategies that reduce InsP₆ in plants, as this will likely also reduce PP-InsPs. Thus, this review is primarily intended to bridge the gap between the basic science aspects of PP-InsP synthesis/signaling and breeding/engineering strategies to fortify foods by reducing InsP₆. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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29 pages, 556 KiB

Open AccessFeature PaperEditor’s ChoiceReview

Biofortification of Pulse Crops: Status and Future Perspectives

by Ambuj B. Jha and Thomas D. Warkentin

Plants 2020, 9(1), 73; https://doi.org/10.3390/plants9010073 - 6 Jan 2020

Cited by 164 | Viewed by 17214

Abstract

Biofortification through plant breeding is a sustainable approach to improve the nutritional profile of food crops. The majority of the world’s population depends on staple food crops; however, most are low in key micronutrients. Biofortification to improve the nutritional profile of pulse crops has increased importance in many breeding programs in the past decade. The key micronutrients targeted have been iron, zinc, selenium, iodine, carotenoids, and folates. In recent years, several biofortified pulse crops including common beans and lentils have been released by HarvestPlus with global partners in developing countries, which has helped in overcoming micronutrient deficiency in the target population. This review will focus on recent research advances and future strategies for the biofortification of pulse crops. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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20 pages, 2345 KiB

Open AccessEditor’s ChoiceReview

Phytic Acid and Transporters: What Can We Learn from low phytic acid Mutants?

by Eleonora Cominelli, Roberto Pilu and Francesca Sparvoli

Plants 2020, 9(1), 69; https://doi.org/10.3390/plants9010069 - 5 Jan 2020

Cited by 42 | Viewed by 6973

Abstract

Phytic acid has two main roles in plant tissues: Storage of phosphorus and regulation of different cellular processes. From a nutritional point of view, it is considered an antinutritional compound because, being a cation chelator, its presence reduces mineral bioavailability from the diet. In recent decades, the development of low phytic acid (lpa) mutants has been an important goal for nutritional seed quality improvement, mainly in cereals and legumes. Different lpa mutations affect phytic acid biosynthetic genes. However, other lpa mutations isolated so far, affect genes coding for three classes of transporters: A specific group of ABCC type vacuolar transporters, putative sulfate transporters, and phosphate transporters. In the present review, we summarize advances in the characterization of these transporters in cereals and legumes. Particularly, we describe genes, proteins, and mutants for these different transporters, and we report data of in silico analysis aimed at identifying the putative orthologs in some other cereal and legume species. Finally, we comment on the advantage of using such types of mutants for crop biofortification and on their possible utility to unravel links between phosphorus and sulfur metabolism (phosphate and sulfate homeostasis crosstalk). Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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Other

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27 pages, 2161 KiB

Open AccessFeature PaperCommentary

Low phytic acid Crops: Observations Based on Four Decades of Research

by Victor Raboy

Plants 2020, 9(2), 140; https://doi.org/10.3390/plants9020140 - 22 Jan 2020

Cited by 83 | Viewed by 9106

Abstract

The low phytic acid (lpa), or “low-phytate” seed trait can provide numerous potential benefits to the nutritional quality of foods and feeds and to the sustainability of agricultural production. Major benefits include enhanced phosphorus (P) management contributing to enhanced sustainability in non-ruminant (poultry, swine, and fish) production; reduced environmental impact due to reduced waste P in non-ruminant production; enhanced “global” bioavailability of minerals (iron, zinc, calcium, magnesium) for both humans and non-ruminant animals; enhancement of animal health, productivity and the quality of animal products; development of “low seed total P” crops which also can enhance management of P in agricultural production and contribute to its sustainability. Evaluations of this trait by industry and by advocates of biofortification via breeding for enhanced mineral density have been too short term and too narrowly focused. Arguments against breeding for the low-phytate trait overstate the negatives such as potentially reduced yields and field performance or possible reductions in phytic acid’s health benefits. Progress in breeding or genetically-engineering high-yielding stress-tolerant low-phytate crops continues. Perhaps due to the potential benefits of the low-phytate trait, the challenge of developing high-yielding, stress-tolerant low-phytate crops has become something of a holy grail for crop genetic engineering. While there are widely available and efficacious alternative approaches to deal with the problems posed by seed-derived dietary phytic acid, such as use of the enzyme phytase as a feed additive, or biofortification breeding, if there were an interest in developing low-phytate crops with good field performance and good seed quality, it could be accomplished given adequate time and support. Even with a moderate reduction in yield, in light of the numerous benefits of low-phytate types as human foods or animal feeds, should one not grow a nutritionally-enhanced crop variant that perhaps has 5% to 10% less yield than a standard variant but one that is substantially more nutritious? Such crops would be a benefit to human nutrition especially in populations at risk for iron and zinc deficiency, and a benefit to the sustainability of agricultural production. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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10 pages, 707 KiB

Open AccessOpinion

Plant Sulfate Transporters in the Low Phytic Acid Network: Some Educated Guesses

by Gian Attilio Sacchi and Fabio Francesco Nocito

Plants 2019, 8(12), 616; https://doi.org/10.3390/plants8120616 - 17 Dec 2019

Cited by 13 | Viewed by 4268

Abstract

A few new papers report that mutations in some genes belonging to the group 3 of plant sulfate transporter family result in low phytic acid phenotypes, drawing novel strategies and approaches for engineering the low-phytate trait in cereal grains. Here, we shortly review the current knowledge on phosphorus/sulfur interplay and sulfate transport regulation in plants, to critically discuss some hypotheses that could help in unveiling the physiological links between sulfate transport and phosphorus accumulation in seeds. Full article

(This article belongs to the Special Issue Phytic Acid and Mineral Biofortification Strategies: From Plant Science to Breeding and Biotechnological Approaches)

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