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Iron and Sulfur in Plants
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Iron and Sulfur in Plants

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 March 2020) | Viewed by 43737

Special Issue Editors

Dr. Stefania Astolfi

E-Mail Website
Guest Editor
Department of Agricultural and Forest Sciences (DAFNE), University of Tuscia, Via S. C. de Lellis, 01100 Viterbo, Italy
Interests: plant physiological response to mineral deficiencies (mainly S and Fe); problems related to soil contamination with cadmium; the role of membrane activities in the plant's response to stress and variations in nutrient availability
Special Issues, Collections and Topics in MDPI journals
Dr. Silvia Celletti

E-Mail Website
Co-Guest Editor
Department of Life Sciences, University of Siena, 53100 Siena, Italy
Interests: physiological, biochemical, and molecular responses of plants to abiotic stresses such as deficiencies of natural resources (e.g., nutrients and water) or salinity; analysis of the effects of biofertilizers (i.e., biochar and wood distillate) on the soil–plant system; the use of solid and liquid byproducts of hydrothermal carbonization (HTC) in soilless culture systems; analysis of the impact of bioplastics on plant yield and soil quality
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

In recent years, environmental policies have led to the reduction of S-rich industrial emissions and, consequently, free S deposition to the soil. Thus, soils are progressively becoming S depleted, and the situation is worsening because the increased crop yields and production are using soil S reserves at greater rates. Although the uptake and assimilation pathway of S is well characterized, there are many unresolved questions concerning the regulation of its metabolism in response to both its availability in the environment and the demand of plants for it under certain environmental conditions. Recently, a significant interaction between S and Fe was observed, in which a deficiency in one of the two nutrients induces physiological modifications, allowing the adequate and balanced assimilation of the other. However, the comprehension of the mechanisms underlying the responses to this combined deficiency are still mostly lacking, even though some theories have been postulated.

Therefore, Fe–S interplay should be exploited from both a scientific and an applicative point of view to provide both new knowledge and sustainable agricultural strategies.

Prof. Stefania Astolfi
Dr. Silvia Celletti
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

  • iron
  • sulfur
  • iron deficiency
  • sulfur deficiency
  • strategy I
  • strategy II
  • phytosiderophores
  • biofortification
  • Fe–S clusters
  • chlorosis
  • methionine

Related Special Issue

Published Papers (11 papers)

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Research

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20 pages, 2535 KiB  
Article
Single and Combined Fe and S Deficiency Differentially Modulate Root Exudate Composition in Tomato: A Double Strategy for Fe Acquisition?
by Stefania Astolfi, Youry Pii, Tanja Mimmo, Luigi Lucini, Maria B. Miras-Moreno, Eleonora Coppa, Simona Violino, Silvia Celletti and Stefano Cesco
Int. J. Mol. Sci. 2020, 21(11), 4038; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21114038 - 05 Jun 2020
Cited by 23 | Viewed by 3606
Abstract
Fe chlorosis is considered as one of the major constraints on crop growth and yield worldwide, being particularly worse when associated with S shortage, due to the tight link between Fe and S. Plant adaptation to inadequate nutrient availabilities often relies on the [...] Read more.
Fe chlorosis is considered as one of the major constraints on crop growth and yield worldwide, being particularly worse when associated with S shortage, due to the tight link between Fe and S. Plant adaptation to inadequate nutrient availabilities often relies on the release of root exudates that enhance nutrients, mobilization from soil colloids and favour their uptake by roots. This work aims at characterizing the exudomic profile of hydroponically grown tomato plants subjected to either single or combined Fe and S deficiency, as well as at shedding light on the regulation mechanisms underlying Fe and S acquisition processes by plants. Root exudates have been analysed by untargeted metabolomics, through liquid chromatography–mass spectrometry as well as gas chromatography–mass spectrometry following derivatization. More than 200 metabolites could be putatively annotated. Venn diagrams show that 23%, 10% and 21% of differential metabolites are distinctively modulated by single Fe deficiency, single S deficiency or combined Fe–S deficiency, respectively. Interestingly, for the first time, a mugineic acid derivative is detected in dicot plants root exudates. The results seem to support the hypothesis of the co-existence of the two Fe acquisition strategies in tomato plants. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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22 pages, 3094 KiB  
Article
Examining Short-Term Responses to a Long-Term Problem: RNA-Seq Analyses of Iron Deficiency Chlorosis Tolerant Soybean
by Adrienne N. Moran Lauter, Lindsay Rutter, Dianne Cook, Jamie A. O’Rourke and Michelle A. Graham
Int. J. Mol. Sci. 2020, 21(10), 3591; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21103591 - 19 May 2020
Cited by 9 | Viewed by 2926
Abstract
Iron deficiency chlorosis (IDC) is a global crop production problem, significantly impacting yield. However, most IDC studies have focused on model species, not agronomically important crops. Soybean is the second largest crop grown in the United States, yet the calcareous soils across most [...] Read more.
Iron deficiency chlorosis (IDC) is a global crop production problem, significantly impacting yield. However, most IDC studies have focused on model species, not agronomically important crops. Soybean is the second largest crop grown in the United States, yet the calcareous soils across most of the upper U.S. Midwest limit soybean growth and profitability. To understand early soybean iron stress responses, we conducted whole genome expression analyses (RNA-sequencing) of leaf and root tissue from the iron efficient soybean (Glycine max) cultivar Clark, at 30, 60 and 120 min after transfer to iron stress conditions. We identified over 10,000 differentially expressed genes (DEGs), with the number of DEGs increasing over time in leaves, but decreasing over time in roots. To investigate these responses, we clustered our expression data across time to identify suites of genes, their biological functions, and the transcription factors (TFs) that regulate their expression. These analyses reveal the hallmarks of the soybean iron stress response (iron uptake and homeostasis, defense, and DNA replication and methylation) can be detected within 30 min. Furthermore, they suggest root to shoot signaling initiates early iron stress responses representing a novel paradigm for crop stress adaptations. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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15 pages, 1218 KiB  
Article
Regulation of Sulfur Homeostasis in Mycorrhizal Maize Plants Grown in a Fe-Limited Environment
by Styliani N. Chorianopoulou, Petros P. Sigalas, Niki Tsoutsoura, Anastasia Apodiakou, Georgios Saridis, Yannis E. Ventouris and Dimitris L. Bouranis
Int. J. Mol. Sci. 2020, 21(9), 3249; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21093249 - 04 May 2020
Cited by 3 | Viewed by 2457
Abstract
Sulfur is an essential macronutrient for growth of higher plants. The entry of the sulfate anion into the plant, its importation into the plastids for assimilation, its long-distance transport through the vasculature, and its storage in the vacuoles require specific sulfate transporter proteins. [...] Read more.
Sulfur is an essential macronutrient for growth of higher plants. The entry of the sulfate anion into the plant, its importation into the plastids for assimilation, its long-distance transport through the vasculature, and its storage in the vacuoles require specific sulfate transporter proteins. In this study, mycorrhizal and non-mycorrhizal maize plants were grown for 60 days in an S-deprived substrate, whilst iron was provided to the plants in the sparingly soluble form of FePO4. On day 60, sulfate was provided to the plants. The gene expression patterns of a number of sulfate transporters as well as sulfate assimilation enzymes were studied in leaves and roots of maize plants, both before as well as after sulfate supply. Prolonged sulfur deprivation resulted in a more or less uniform response of the genes’ expressions in the roots of non-mycorrhizal and mycorrhizal plants. This was not the case neither in the roots and leaves after the supply of sulfur, nor in the leaves of the plants during the S-deprived period of time. It is concluded that mycorrhizal symbiosis modified plant demands for reduced sulfur, regulating accordingly the uptake, distribution, and assimilation of the sulfate anion. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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15 pages, 2062 KiB  
Article
Sulfur Deficiency Increases Phosphate Accumulation, Uptake, and Transport in Arabidopsis thaliana
by Alaa Allahham, Satomi Kanno, Liu Zhang and Akiko Maruyama-Nakashita
Int. J. Mol. Sci. 2020, 21(8), 2971; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21082971 - 23 Apr 2020
Cited by 11 | Viewed by 3516
Abstract
Recent studies have shown various metabolic and transcriptomic interactions between sulfur (S) and phosphorus (P) in plants. However, most studies have focused on the effects of phosphate (Pi) availability and P signaling pathways on S homeostasis, whereas the effects of S availability on [...] Read more.
Recent studies have shown various metabolic and transcriptomic interactions between sulfur (S) and phosphorus (P) in plants. However, most studies have focused on the effects of phosphate (Pi) availability and P signaling pathways on S homeostasis, whereas the effects of S availability on P homeostasis remain largely unknown. In this study, we investigated the interactions between S and P from the perspective of S availability. We investigated the effects of S availability on Pi uptake, transport, and accumulation in Arabidopsis thaliana grown under sulfur sufficiency (+S) and deficiency (−S). Total P in shoots was significantly increased under −S owing to higher Pi accumulation. This accumulation was facilitated by increased Pi uptake under −S. In addition, −S increased root-to-shoot Pi transport, which was indicated by the increased Pi levels in xylem sap under −S. The −S-increased Pi level in the xylem sap was diminished in the disruption lines of PHT1;9 and PHO1, which are involved in root-to-shoot Pi transport. Our findings indicate a new aspect of the interaction between S and P by listing the increased Pi accumulation as part of −S responses and by highlighting the effects of −S on Pi uptake, transport, and homeostasis. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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17 pages, 4155 KiB  
Article
A Non-Invasive Tool for Real-Time Measurement of Sulfate in Living Cells
by Urooj Fatima, Mohammad K. Okla, Mohd Mohsin, Ruphi Naz, Walid Soufan, Abdullah A. Al-Ghamdi and Altaf Ahmad
Int. J. Mol. Sci. 2020, 21(7), 2572; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21072572 - 07 Apr 2020
Cited by 4 | Viewed by 2310
Abstract
Sulfur (S) is an essential element for all forms of life. It is involved in numerous essential processes because S is considered as the primary source of one of the essential amino acids, methionine, which plays an important role in biological events. For [...] Read more.
Sulfur (S) is an essential element for all forms of life. It is involved in numerous essential processes because S is considered as the primary source of one of the essential amino acids, methionine, which plays an important role in biological events. For the control and regulation of sulfate in a metabolic network through fluxomics, a non-invasive tool is highly desirable that opens the door to monitor the level of the sulfate in real time and space in living cells without fractionation of the cells or tissue. Here, we engineered a FRET (fluorescence resonance energy transfer) based sensor for sulfate, which is genetically-encoded and named as FLIP-SP (Fluorescent indicator protein for sulfate). The FLIP-SP can measure the level of the sulfate in live cells. This sensor was constructed by the fusion of fluorescent proteins at the N- and C-terminus of sulfate binding protein (sbp). The FLIP-SP is highly specific to sulfate, and showed pH stability. Real-time monitoring of the level of sulfate in prokaryotic and eukaryotic cells showed sensor bio-compatibility with living cells. We expect that this sulfate sensor offers a valuable strategy in the understanding of the regulation of the flux of sulfate in the metabolic network. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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16 pages, 2220 KiB  
Article
Arbuscular Mycorrhizal Symbiosis Mitigates Iron (Fe)-Deficiency Retardation in Alfalfa (Medicago sativa L.) Through the Enhancement of Fe Accumulation and Sulfur-Assisted Antioxidant Defense
by Md. Atikur Rahman, Monika Parvin, Urmi Das, Esrat Jahan Ela, Sang-Hoon Lee, Ki-Won Lee and Ahmad Humayan Kabir
Int. J. Mol. Sci. 2020, 21(6), 2219; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21062219 - 23 Mar 2020
Cited by 26 | Viewed by 4466
Abstract
Iron (Fe)-deficiency is one of the major constraints affecting growth, yield and nutritional quality in plants. This study was performed to elucidate how arbuscular mycorrhizal fungi (AMF) alleviate Fe-deficiency retardation in alfalfa (Medicago sativa L.). AMF supplementation improved plant biomass, chlorophyll score, [...] Read more.
Iron (Fe)-deficiency is one of the major constraints affecting growth, yield and nutritional quality in plants. This study was performed to elucidate how arbuscular mycorrhizal fungi (AMF) alleviate Fe-deficiency retardation in alfalfa (Medicago sativa L.). AMF supplementation improved plant biomass, chlorophyll score, Fv/Fm (quantum efficiency of photosystem II), and Pi_ABS (photosynthesis performance index), and reduced cell death, electrolyte leakage, and hydrogen peroxide accumulation in alfalfa. Moreover, AMF enhanced ferric chelate reductase activity as well as Fe, Zn, S and P in alfalfa under Fe-deficiency. Although Fe-transporters (MsIRT1 and MsNramp1) did not induce in root but MsFRO1 significantly induced by AMF under Fe deficiency in roots, suggesting that AMF-mediated Fe enhancement is related to the bioavailability of Fe at rhizosphere/root apoplast rather than the upregulation of Fe transporters under Fe deficiency in alfalfa. Several S-transporters (MsSULTR1;1, MsSULTR1;2, MsSULTR1;3, and MsSULTR3;1) markedly increased following AMF supplementation with or without Fe-deficiency alfalfa. Our study further suggests that Fe uptake system is independently influenced by AMF regardless of the S status in alfalfa. However, the increase of S in alfalfa is correlated with the elevation of GR and S-metabolites (glutathione and cysteine) associated with antioxidant defense under Fe deficiency. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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Review

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20 pages, 2994 KiB  
Review
The Sulphur Response in Wheat Grain and Its Implications for Acrylamide Formation and Food Safety
by Sarah Raffan, Joseph Oddy and Nigel G. Halford
Int. J. Mol. Sci. 2020, 21(11), 3876; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21113876 - 29 May 2020
Cited by 17 | Viewed by 4815
Abstract
Free (soluble, non-protein) asparagine concentration can increase many-fold in wheat grain in response to sulphur deficiency. This exacerbates a major food safety and regulatory compliance problem for the food industry because free asparagine may be converted to the carcinogenic contaminant, acrylamide, during baking [...] Read more.
Free (soluble, non-protein) asparagine concentration can increase many-fold in wheat grain in response to sulphur deficiency. This exacerbates a major food safety and regulatory compliance problem for the food industry because free asparagine may be converted to the carcinogenic contaminant, acrylamide, during baking and processing. Here, we describe the predominant route for the conversion of asparagine to acrylamide in the Maillard reaction. The effect of sulphur deficiency and its interaction with nitrogen availability is reviewed, and we reiterate our advice that sulphur should be applied to wheat being grown for human consumption at a rate of 20 kg per hectare. We describe the genetic control of free asparagine accumulation, including genes that encode metabolic enzymes (asparagine synthetase, glutamine synthetase, glutamate synthetase, and asparaginase), regulatory protein kinases (sucrose nonfermenting-1 (SNF1)-related protein kinase-1 (SnRK1) and general control nonderepressible-2 (GCN2)), and basic leucine zipper (bZIP) transcription factors, and how this genetic control responds to sulphur, highlighting the importance of asparagine synthetase-2 (ASN2) expression in the embryo. We show that expression of glutamate-cysteine ligase is reduced in response to sulphur deficiency, probably compromising glutathione synthesis. Finally, we describe unexpected effects of sulphur deficiency on carbon metabolism in the endosperm, with large increases in expression of sucrose synthase-2 (SuSy2) and starch synthases. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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13 pages, 5261 KiB  
Review
Biosynthesis of Sulfur-Containing Small Biomolecules in Plants
by Yumi Nakai and Akiko Maruyama-Nakashita
Int. J. Mol. Sci. 2020, 21(10), 3470; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21103470 - 14 May 2020
Cited by 26 | Viewed by 3775
Abstract
Sulfur is an essential element required for plant growth. It can be found as a thiol group of proteins or non-protein molecules, and as various sulfur-containing small biomolecules, including iron-sulfur (Fe/S) clusters, molybdenum cofactor (Moco), and sulfur-modified nucleotides. Thiol-mediated redox regulation has been [...] Read more.
Sulfur is an essential element required for plant growth. It can be found as a thiol group of proteins or non-protein molecules, and as various sulfur-containing small biomolecules, including iron-sulfur (Fe/S) clusters, molybdenum cofactor (Moco), and sulfur-modified nucleotides. Thiol-mediated redox regulation has been well investigated, whereas biosynthesis pathways of the sulfur-containing small biomolecules have not yet been clearly described. In order to understand overall sulfur transfer processes in plant cells, it is important to elucidate the relationships among various sulfur delivery pathways as well as to investigate their interactions. In this review, we summarize the information from recent studies on the biosynthesis pathways of several sulfur-containing small biomolecules and the proteins participating in these processes. In addition, we show characteristic features of gene expression in Arabidopsis at the early stage of sulfate depletion from the medium, and we provide insights into sulfur transfer processes in plant cells. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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30 pages, 2879 KiB  
Review
Regulation of Iron Homeostasis and Use in Chloroplasts
by Gretchen E. Kroh and Marinus Pilon
Int. J. Mol. Sci. 2020, 21(9), 3395; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21093395 - 11 May 2020
Cited by 84 | Viewed by 6937
Abstract
Iron (Fe) is essential for life because of its role in protein cofactors. Photosynthesis, in particular photosynthetic electron transport, has a very high demand for Fe cofactors. Fe is commonly limiting in the environment, and therefore photosynthetic organisms must acclimate to Fe availability [...] Read more.
Iron (Fe) is essential for life because of its role in protein cofactors. Photosynthesis, in particular photosynthetic electron transport, has a very high demand for Fe cofactors. Fe is commonly limiting in the environment, and therefore photosynthetic organisms must acclimate to Fe availability and avoid stress associated with Fe deficiency. In plants, adjustment of metabolism, of Fe utilization, and gene expression, is especially important in the chloroplasts during Fe limitation. In this review, we discuss Fe use, Fe transport, and mechanisms of acclimation to Fe limitation in photosynthetic lineages with a focus on the photosynthetic electron transport chain. We compare Fe homeostasis in Cyanobacteria, the evolutionary ancestors of chloroplasts, with Fe homeostasis in green algae and in land plants in order to provide a deeper understanding of how chloroplasts and photosynthesis may cope with Fe limitation. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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27 pages, 1960 KiB  
Review
Potential Implications of Interactions between Fe and S on Cereal Fe Biofortification
by Yuta Kawakami and Navreet K. Bhullar
Int. J. Mol. Sci. 2020, 21(8), 2827; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21082827 - 18 Apr 2020
Cited by 10 | Viewed by 4038
Abstract
Iron (Fe) and sulfur (S) are two essential elements for plants, whose interrelation is indispensable for numerous physiological processes. In particular, Fe homeostasis in cereal species is profoundly connected to S nutrition because phytosiderophores, which are the metal chelators required for Fe uptake [...] Read more.
Iron (Fe) and sulfur (S) are two essential elements for plants, whose interrelation is indispensable for numerous physiological processes. In particular, Fe homeostasis in cereal species is profoundly connected to S nutrition because phytosiderophores, which are the metal chelators required for Fe uptake and translocation in cereals, are derived from a S-containing amino acid, methionine. To date, various biotechnological cereal Fe biofortification strategies involving modulation of genes underlying Fe homeostasis have been reported. Meanwhile, the resultant Fe-biofortified crops have been minimally characterized from the perspective of interaction between Fe and S, in spite of the significance of the crosstalk between the two elements in cereals. Here, we intend to highlight the relevance of Fe and S interrelation in cereal Fe homeostasis and illustrate the potential implications it has to offer for future cereal Fe biofortification studies. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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22 pages, 1519 KiB  
Review
The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants
by Anna Wawrzyńska and Agnieszka Sirko
Int. J. Mol. Sci. 2020, 21(8), 2771; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21082771 - 16 Apr 2020
Cited by 12 | Viewed by 3885
Abstract
Plants are able to synthesize all essential metabolites from minerals, water, and light to complete their life cycle. This plasticity comes at a high energy cost, and therefore, plants need to tightly allocate resources in order to control their economy. Being sessile, plants [...] Read more.
Plants are able to synthesize all essential metabolites from minerals, water, and light to complete their life cycle. This plasticity comes at a high energy cost, and therefore, plants need to tightly allocate resources in order to control their economy. Being sessile, plants can only adapt to fluctuating environmental conditions, relying on quality control mechanisms. The remodeling of cellular components plays a crucial role, not only in response to stress, but also in normal plant development. Dynamic protein turnover is ensured through regulated protein synthesis and degradation processes. To effectively target a wide range of proteins for degradation, plants utilize two mechanistically-distinct, but largely complementary systems: the 26S proteasome and the autophagy. As both proteasomal- and autophagy-mediated protein degradation use ubiquitin as an essential signal of substrate recognition, they share ubiquitin conjugation machinery and downstream ubiquitin recognition modules. Recent progress has been made in understanding the cellular homeostasis of iron and sulfur metabolisms individually, and growing evidence indicates that complex crosstalk exists between iron and sulfur networks. In this review, we highlight the latest publications elucidating the role of selective protein degradation in the control of iron and sulfur metabolism during plant development, as well as environmental stresses. Full article
(This article belongs to the Special Issue Iron and Sulfur in Plants)
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