Abstract
Agriculture and plant science face a formidable challenge in feeding the world’s expanding population in a sustainable, sufficient, and nutrient-rich manner. The mineral micronutrient composition of food crops merits special consideration. Globally, cultivated soil and plant micronutrient deficits have negative impacts on crop yield, plant nutritional value, human health and well-being. This article reviews the present knowledge on iron (Fe) uptake, transport, subcellular translocation, and its regulation at the molecular level mainly on Oryza sativa and Arabidopsis thaliana, which typically represent graminaceous and non-graminaceous plants, respectively. This study emphasizes the recent advancements in various approaches, including high-throughput technologies (NGS, proteomics, ionomics) and genetic engineering such as CRISPR/Cas for Fe biofortification in crop plants and their subsequent impact on human health. The aforementioned information can be applied to elevate the Fe content in model plants along with various fruit and vegetable crops. This might be helpful for nutritious food production for large human population in the world to achieve one of the most important Sustainable Development Goals (SDGs) for nutrition security.
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References
Alka, Jangra Siddhant, Chaturvedi Naveen, Kumar Hardeep, Singh Vishal, Sharma Manisha, Thakur Siddharth, Tiwari Vinod, Chhokar Polyamines: The Gleam of Next-Generation Plant Growth Regulators for Growth Development Stress Mitigation and Hormonal Crosstalk in Plants?A Systematic Review. Journal of Plant Growth Regulation https://doi.org/10.1007/s00344-022-10846-4
Asmamaw M, Zawdie B (2021) Mechanism and applications of CRISPR/Cas-9-Mediated genome editing. Biol : targets therapy 15:353–361. https://doi.org/10.2147/btt.S326422
Assunção AGL, Cakmak I, Clemens S, González-Guerrero M, Nawrocki A, Thomine S (2022) Micronutrient homeostasis in plants for more sustainable agriculture and healthier human nutrition. Journal of experimental botany 73 (6):1789–1799. https://doi.org/10.1093/jxb/erac014
Awasthi P, Khan S, Lakhani H, Chaturvedi S, Kaur N, Singh J, Kesarwani A.K. and Tiwari S (2022) Transgene-free genome editing supports the role of carotenoid cleavage dioxygenase 4 as a negative regulator of β-carotene in banana. Journal of Experimental Botany, 73(11), pp.3401–3416
Bandyopadhyay T, Prasad M (2021) IRONing out stress problems in crops: a homeostatic perspective. Physiol Plant 171(4):559–577. https://doi.org/10.1111/ppl.13184
Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 281(43):32395–32402. https://doi.org/10.1074/jbc.M604133200
Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8(1):e1002446. https://doi.org/10.1371/journal.pgen.1002446
Carbonero P, Iglesias-Fernández R, Vicente-Carbajosa J (2017) The AFL subfamily of B3 transcription factors: evolution and function in angiosperm seeds. J Exp Bot 68(4):871–880. https://doi.org/10.1093/jxb/erw458
Carey-Fung O, Beasley JT, Johnson AAT (2021) Annotation and molecular characterisation of the TaIRO3 and TaHRZ Iron Homeostasis genes in Bread Wheat (Triticum aestivum L.). Genes 12(5). https://doi.org/10.3390/genes12050653
Carey-Fung O, O’Brien M, Beasley JT, Johnson AAT (2022) A model to incorporate the bHLH transcription factor OsIRO3 within the Rice Iron Homeostasis Regulatory Network. Int J Mol Sci 23(3). https://doi.org/10.3390/ijms23031635
Chaturvedi S, Chaudhary R, Tiwari S (2021) Contribution of crop biofortification in mitigating vitamin deficiency globally. Genome Engineering for Crop Improvement, pp 112–130
Chaturvedi S, Khan S, Bhunia RK, Kaur K, Tiwari S (2022) Metabolic engineering in food crops to enhance ascorbic acid production: crop biofortification perspectives for human health. Physiology and Molecular Biology of Plants, pp 1–14
Che J, Yamaji N, Ma JF (2021) Role of a vacuolar iron transporter OsVIT2 in the distribution of iron to rice grains. New Phytol 230(3):1049–1062. https://doi.org/10.1111/nph.17219
Chen L, Ding C, Zhao X, Xu J, Mohammad AA, Wang S, Ding Y (2015) Differential regulation of proteins in rice (Oryza sativa L.) under iron deficiency. Plant Cell Rep 34(1):83–96. https://doi.org/10.1007/s00299-014-1689-1
Chennakesavulu K, Singh H, Trivedi PK, Jain M, Yadav SR (2022) State-of-the-art in CRISPR Technology and Engineering Drought, Salinity, and Thermo-tolerant crop plants. Plant Cell Rep 41(3):815–831. https://doi.org/10.1007/s00299-021-02681-w
Chou SJ, Wang C, Sintupisut N, Niou ZX, Lin CH, Li KC, Yeang CH (2016) Analysis of spatial-temporal gene expression patterns reveals dynamics and regionalization in developing mouse brain. Sci Rep 6:19274. https://doi.org/10.1038/srep19274
Coleto I, Bejarano I, Marín-Peña AJ, Medina J, Rioja C, Burow M, Marino D (2021) Arabidopsis thaliana transcription factors MYB28 and MYB29 shape ammonium stress responses by regulating Fe homeostasis. New Phytol 229(2):1021–1035. https://doi.org/10.1111/nph.16918
Connorton JM, Balk J, Rodríguez-Celma J (2017) Iron homeostasis in plants - a brief overview. Metallomics 9(7):813–823. https://doi.org/10.1039/c7mt00136c
Cui Y, Chen CL, Cui M, Zhou WJ, Wu HL, Ling HQ (2018) Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA Inhibition of Iron Uptake in Arabidopsis. Mol Plant 11(9):1166–1183. https://doi.org/10.1016/j.molp.2018.06.005
Deng W, Zhang K, Busov V, Wei H (2017) Recursive random forest algorithm for constructing multilayered hierarchical gene regulatory networks that govern biological pathways. PLoS ONE 12(2):e0171532. https://doi.org/10.1371/journal.pone.0171532
Donnini S, Prinsi B, Negri AS, Vigani G, Espen L, Zocchi G (2010) Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots. BMC Plant Biol 10:268. https://doi.org/10.1186/1471-2229-10-268
Duy D, Stübe R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155(4):1709–1722. https://doi.org/10.1104/PP.110.170233
Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7):397–405. https://doi.org/10.1016/j.tibtech.2013.04.004
Gao F, Robe K, Dubos C (2020) Further insights into the role of bHLH121 in the regulation of iron homeostasis in Arabidopsis thaliana. Plant Signal Behav 15(10):1795582. https://doi.org/10.1080/15592324.2020.1795582
Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C (2019) The Transcriptional Control of Iron Homeostasis in plants: a tale of bHLH transcription factors? Front Plant Sci 10:6. https://doi.org/10.3389/fpls.2019.00006
Grant-Grant S, Schaffhauser M, Baeza-Gonzalez P, Gao F, Conéjéro G, Vidal EA, Gaymard F, Dubos C, Curie C, Roschzttardtz H (2022) B3 transcription factors determine Iron distribution and FERRITIN gene expression in embryo but do not control total seed Iron content. Front Plant Sci 13:870078. https://doi.org/10.3389/fpls.2022.870078
Grillet L, Lan P, Li W, Mokkapati G, Schmidt W (2018) IRON MAN is a ubiquitous family of peptides that control iron transport in plants. Nat plants 4(11):953–963. https://doi.org/10.1038/s41477-018-0266-y
Gutierrez-Carbonell E, Lattanzio G, Albacete A, Rios JJ, Kehr J, Abadía A, Grusak MA, Abadía J, López-Millán AF (2015) Effects of Fe deficiency on the protein profile of Brassica napus phloem sap. Proteomics 15(22):3835–3853. https://doi.org/10.1002/pmic.201400464
Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20(5):735–747. https://doi.org/10.1093/molbev/msg088
Hintze KJ, Theil EC (2006) Cellular regulation and molecular interactions of the ferritins. Cell Mol life Sci : CMLS 63(5):591–600. https://doi.org/10.1007/s00018-005-5285-y
Hirayama T, Lei GJ, Yamaji N, Nakagawa N, Ma JF (2018) The putative peptide gene FEP1 regulates Iron Deficiency response in Arabidopsis. Plant Cell Physiol 59(9):1739–1752. https://doi.org/10.1093/pcp/pcy145
Hirschi KD (2003) Strike while the ionome is hot: making the most of plant genomic advances. Trends Biotechnol 21(12):520–521. https://doi.org/10.1016/j.tibtech.2003.09.013
Huang XY, Salt DE (2016) Plant Ionomics: from elemental profiling to Environmental Adaptation. Mol Plant 9(6):787–797. https://doi.org/10.1016/j.molp.2016.05.003
Ibrahim S, Saleem B, Rehman N, Zafar SA, Naeem MK, Khan MR (2022) CRISPR/Cas9 mediated disruption of Inositol Pentakisphosphate 2-Kinase 1 (TaIPK1) reduces phytic acid and improves iron and zinc accumulation in wheat grains. J Adv Res 37:33–41. https://doi.org/10.1016/j.jare.2021.07.006
Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284(6):3470–3479. https://doi.org/10.1074/jbc.M806042200
Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286(28):24649–24655. https://doi.org/10.1074/jbc.M111.221168
Jean-Baptiste K, McFaline-Figueroa JL, Alexandre CM, Dorrity MW, Saunders L, Bubb KL, Trapnell C, Fields S, Queitsch C, Cuperus JT (2019) Dynamics of Gene expression in single Root cells of Arabidopsis thaliana. Plant Cell 31(5):993–1011. https://doi.org/10.1105/tpc.18.00785
Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci USA 105(30):10619–10624. https://doi.org/10.1073/pnas.0708367105
Jin F, Frohman C, Thannhauser TW, Welch RM, Glahn RP (2009) Effects of ascorbic acid, phytic acid and tannic acid on iron bioavailability from reconstituted ferritin measured by an in vitro digestion-Caco-2 cell model. Br J Nutr 101(7):972–981. https://doi.org/10.1017/s0007114508055621
Kaur K, Awasthi P, Tiwari S (2021) Comparative transcriptome analysis of unripe and ripe banana (cv. Nendran) unraveling genes involved in ripening and other related processes. PLoS ONE 16(7):e0254709. https://doi.org/10.1371/journal.pone.0254709
Kaur N, Alok A, Shivani, Kumar P, Kaur N, Awasthi P, Chaturvedi S, Pandey P, Pandey A, Pandey AK, Tiwari S (2020) CRISPR/Cas9 directed editing of lycopene epsilon-cyclase modulates metabolic flux for β-carotene biosynthesis in banana fruit. Metab Eng 59:76–86. https://doi.org/10.1016/j.ymben.2020.01.008
Kawakami Y, Gruissem W, Bhullar NK (2022) Novel rice iron biofortification approaches using expression of ZmYS1 and OsTOM1 controlled by tissue-specific promoters. J Exp Bot 73(16):5440–5459. https://doi.org/10.1093/jxb/erac214
Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581(12):2273–2280. https://doi.org/10.1016/j.febslet.2007.04.043
Kobayashi T, Nozoye T, Nishizawa NK (2019a) Iron transport and its regulation in plants. Free Radic Biol Med 133:11–20. https://doi.org/10.1016/j.freeradbiomed.2018.10.439
Kobayashi T, Ozu A, Kobayashi S, An G, Jeon JS, Nishizawa NK (2019b) OsbHLH058 and OsbHLH059 transcription factors positively regulate iron deficiency responses in rice. Plant Mol Biol 101(4–5):471–486. https://doi.org/10.1007/s11103-019-00917-8
Kobayashi T, Nagano A, J and, Nishizawa NK (2021) Iron deficiency-inducible peptide-coding genes OsIMA1 and OsIMA2 positively regulate a major pathway of iron uptake and translocation in rice. J Exp Bot 72(6):2196–2211. https://doi.org/10.1093/JXB/ERAA546
Kolbert Z, Cuypers A, Verbruggen N (2022) Essential trace metals: micronutrients with large impact. J Exp Bot 73(6):1685–1687. https://doi.org/10.1093/jxb/erac025
Kumar SB, Arnipalli SR, Mehta P, Carrau S, Ziouzenkova O (2022) Iron Deficiency Anemia: Efficacy and Limitations of Nutritional and Comprehensive Mitigation Strategies. Nutrients 14(14). https://doi.org/10.3390/NU14142976
Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, McIntyre L, Schroeder JI, Salt DE (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21(10):1215–1221. https://doi.org/10.1038/nbt865
Lan P, Li W, Wen TN, Schmidt W (2012) Quantitative phosphoproteome profiling of iron-deficient Arabidopsis roots. Plant Physiol 159(1):403–417. https://doi.org/10.1104/pp.112.193987
Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24(23):4041–4051. https://doi.org/10.1038/sj.emboj.7600864
Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150(2):786–800. https://doi.org/10.1104/pp.109.135418
Lei R, Li Y, Cai Y, Li C, Pu M, Lu C, Yang Y, Liang G (2020) bHLH121 functions as a direct link that facilitates the activation of FIT by bHLH IVc transcription factors for maintaining Fe Homeostasis in Arabidopsis. Mol Plant 13(4):634–649. https://doi.org/10.1016/j.molp.2020.01.006
Li C, Li Y, Xu P, Liang G (2022a) OsIRO3 negatively regulates Fe homeostasis by repressing the expression of OsIRO2. The Plant journal : for cell and molecular biology. https://doi.org/10.1111/tpj.15864
Li H-L, Chen X-X, Ji X-L, Qiao Z-W, Liu R-X, Wang X-F, Ge H-J, You C-XJE, Botany E (2022b) BTB protein MdBT2 negatively regulates iron homeostasis by interacting with MdNAC1 in apple. 195:104778
Li L, Gao W, Peng Q, Zhou B, Kong Q, Ying Y, Shou H (2018) Two soybean bHLH factors regulate response to iron deficiency. J Integr Plant Biol 60(7):608–622. https://doi.org/10.1111/jipb.12651
Lin L, Li Z, Wu C, Wang J, Liang D, Xia H, Deng Q (2022) Melatonin promotes iron uptake and accumulation in peach. Sci Hort 306:111481
Li S, Song Z, Liu X, Zhou X, Yang W, Chen J, Chen R (2022c) Mediation of Zinc and Iron Accumulation in Maize by ZmIRT2, a Novel Iron-Regulated transporter. Plant Cell Physiol 63(4):521–534. https://doi.org/10.1093/pcp/pcab177
Li W, Lan P (2017) The understanding of the Plant Iron Deficiency responses in Strategy I plants and the role of Ethylene in this process by omic approaches. Front Plant Sci 8:40. https://doi.org/10.3389/fpls.2017.00040
Li Y, Lu C, Li K, Lei CY, Pu RH, Zhao MN, Peng JH, Ping F, Wang HQ, Liang D G (2021) IRON MAN interacts with BRUTUS to maintain iron homeostasis in Arabidopsis. Proc Natl Acad Sci USA 118(39). https://doi.org/10.1073/PNAS.2109063118
Li YY, Sui XY, Yang JS, Xiang XH, Li ZQ, Wang YY, Zhou ZC, Hu RS, Liu D (2020) A novel bHLH transcription factor, NtbHLH1, modulates iron homeostasis in tobacco (Nicotiana tabacum L.). Biochemical and biophysical research communications 522. 233–239. https://doi.org/10.1016/j.bbrc.2019.11.063. 1
Li Z, Phillip D, Neuhäuser B, Schulze WX, Ludewig U (2015) Protein Dynamics in Young Maize Root Hairs in response to macro- and Micronutrient Deprivation. J Proteome Res 14(8):3362–3371. https://doi.org/10.1021/acs.jproteome.5b00399
Liang G, Zhang H, Li X, Ai Q, Yu D (2017) bHLH transcription factor bHLH115 regulates iron homeostasis in Arabidopsis thaliana. J Exp Bot 68(7):1743–1755. https://doi.org/10.1093/jxb/erx043
Liang G, Zhang H, Li Y, Pu M, Yang Y, Li C, Lu C, Xu P, Yu D (2020) Oryza sativa FER-LIKE FE DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (OsFIT/OsbHLH156) interacts with OsIRO2 to regulate iron homeostasis. J Integr Plant Biol 62(5):668–689. https://doi.org/10.1111/jipb.12933
Liang G (2022) Iron uptake, signaling, and sensing in plants. Plant Commun 3(5). https://doi.org/10.1016/J.XPLC.2022.100349
Liberal Â, Pinela J, Vívar-Quintana AM, Ferreira I, Barros L (2020) Fighting Iron-Deficiency Anemia: innovations in Food Fortificants and Biofortification strategies. Foods (Basel Switzerland) 9(12). https://doi.org/10.3390/foods9121871
Lichtblau DM, Schwarz B, Baby D, Endres C, Sieberg C, Bauer P (2022) The Iron Deficiency-Regulated small protein effector FEP3/IRON MAN1 modulates Interaction of BRUTUS-LIKE1 with bHLH subgroup IVc and POPEYE transcription factors. Front Plant Sci 13:930049. https://doi.org/10.3389/fpls.2022.930049
Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99(21):13938–13943. https://doi.org/10.1073/pnas.212448699
Liu W, Karemera NJU, Wu T, Yang Y, Zhang X, Xu X, Wang Y, Han Z (2017a) The ethylene response factor AtERF4 negatively regulates the iron deficiency response in Arabidopsis thaliana. PLoS ONE 12(10):e0186580. https://doi.org/10.1371/journal.pone.0186580
Lockhart J (2020) Personal trainer: bHLH121 functions Upstream of a Transcriptional Network of Heavy Lifters involved in Balancing Iron levels. Plant Cell 32(2):293–294. https://doi.org/10.1105/tpc.19.00918
Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22(7):2219–2236. https://doi.org/10.1105/tpc.110.074096
López-Millán AF, Grusak MA, Abadía A, Abadía J (2013) Iron deficiency in plants: an insight from proteomic approaches. Front Plant Sci 4:254. https://doi.org/10.3389/fpls.2013.00254
López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166(4):375–384. https://doi.org/10.1016/j.jplph.2008.06.011
Mahawar L, Ramasamy KP, Pandey A, Prasad SM (2022) Iron deficiency in plants: an update on homeostasis and its regulation by nitric oxide and phytohormones. Plant Growth Regulation, pp 1–17
Mai HJ, Pateyron S, Bauer P (2016) Iron homeostasis in Arabidopsis thaliana: transcriptomic analyses reveal novel FIT-regulated genes, iron deficiency marker genes and functional gene networks. BMC Plant Biol 16(1):211. https://doi.org/10.1186/s12870-016-0899-9
Mansour D, Hofmann A, Gemzell-Danielsson K (2021) A review of clinical guidelines on the management of Iron Deficiency and Iron-Deficiency Anemia in women with heavy menstrual bleeding. Adv therapy 38(1):201–225. https://doi.org/10.1007/s12325-020-01564-y
Marchi G, Busti F, Lira Zidanes A, Castagna A, Girelli D (2019) Aceruloplasminemia: a severe neurodegenerative disorder deserving an early diagnosis. Front NeuroSci 13:325. https://doi.org/10.3389/fnins.2019.00325
Martín-Barranco A, Spielmann J, Dubeaux G, Vert G, Zelazny E (2020) Dynamic control of the High-Affinity Iron Uptake Complex in Root epidermal cells. Plant Physiol 184(3):1236–1250. https://doi.org/10.1104/PP.20.00234
Maurer F, Naranjo Arcos MA, Bauer P (2014) Responses of a triple mutant defective in three iron deficiency-induced Basic Helix-Loop-Helix genes of the subgroup ib(2) to iron deficiency and salicylic acid. PLoS ONE 9(6):e99234. https://doi.org/10.1371/journal.pone.0099234
Meisrimler CN, Planchon S, Renaut J, Sergeant K, Lüthje S (2011) Alteration of plasma membrane-bound redox systems of iron deficient pea roots by chitosan. J Proteom 74(8):1437–1449. https://doi.org/10.1016/j.jprot.2011.01.012
Mergner J, Frejno M, Messerer M, Lang D, Samaras P, Wilhelm M, Mayer KFX, Schwechheimer C, Kuster B (2020) Proteomic and transcriptomic profiling of aerial organ development in Arabidopsis. Sci data 7(1):334. https://doi.org/10.1038/s41597-020-00678-w
Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147(3):969–977. https://doi.org/10.1104/pp.108.118232
Morrissey J, Baxter IR, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21(10):3326–3338. https://doi.org/10.1105/tpc.109.069401
Nagamine A, Ezura H (2022) Genome editing for improving Crop Nutrition. Front genome editing 4:850104. https://doi.org/10.3389/fgeed.2022.850104
Nelms B, Walbot V (2019) Defining the developmental program leading to meiosis in maize. Sci (New York NY) 364(6435):52–56. https://doi.org/10.1126/science.aav6428
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286(7):5446–5454. https://doi.org/10.1074/jbc.M110.180026
Ogo Y, Itai RN, Nakanishi H, Inoue H, Kobayashi T, Suzuki M, Takahashi M, Mori S, Nishizawa NK (2006) Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J Exp Bot 57(11):2867–2878. https://doi.org/10.1093/jxb/erl054
Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23(4):482–487. https://doi.org/10.1038/nbt1082
Pérez-Massot E, Banakar R, Gómez-Galera S, Zorrilla-López U, Sanahuja G, Arjó G, Miralpeix B, Vamvaka E, Farré G, Rivera SM, Dashevskaya S, Berman J, Sabalza M, Yuan D, Bai C, Bassie L, Twyman RM, Capell T, Christou P, Zhu C (2013) The contribution of transgenic plants to better health through improved nutrition: opportunities and constraints. Genes & nutrition 8(1):29–41. https://doi.org/10.1007/s12263-012-0315-5
Piskin E, Cianciosi D, Gulec S, Tomas M, Capanoglu E (2022) Iron absorption: factors, Limitations, and improvement methods. ACS omega 7(24):20441–20456. https://doi.org/10.1021/acsomega.2c01833
Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57(3):400–412. https://doi.org/10.1111/j.1365-313X.2008.03698.x
Rellán-Alvarez R, Giner-Martínez-Sierra J, Orduna J, Orera I, Rodríguez-Castrillón JA, García-Alonso JI, Abadía J, Alvarez-Fernández A (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51(1):91–102. https://doi.org/10.1093/pcp/pcp170
Robe K, Izquierdo E, Vignols F, Rouached H, Dubos C (2021) The Coumarins: secondary metabolites playing a primary role in Plant Nutrition and Health. Trends Plant Sci 26(3):248–259. https://doi.org/10.1016/J.TPLANTS.2020.10.008
Rodríguez-Celma J, Chou H, Kobayashi T, Long TA, Balk J (2019a) Hemerythrin E3 ubiquitin ligases as negative regulators of Iron homeostasis in plants. Front Plant Sci 10:98. https://doi.org/10.3389/fpls.2019.00098
Rodríguez-Celma J, Lattanzio G, Villarroya D, Gutierrez-Carbonell E, Ceballos-Laita L, Rencoret J, Gutiérrez A, Del Río JC, Grusak MA, Abadía A, Abadía J, López-Millán AF (2016) Effects of Fe deficiency on the protein profiles and lignin composition of stem tissues from Medicago truncatula in absence or presence of calcium carbonate. J Proteom 140:1–12. https://doi.org/10.1016/j.jprot.2016.03.017
Rodríguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W (2013) The transcriptional response of Arabidopsis leaves to Fe deficiency. Front Plant Sci 4:276. https://doi.org/10.3389/fpls.2013.00276
Saito A, Iino T, Sonoike K, Miwa E, Higuchi K (2010) Remodeling of the major light-harvesting antenna protein of PSII protects the young leaves of barley (Hordeum vulgare L.) from photoinhibition under prolonged iron deficiency. Plant Cell Physiol 51(12):2013–2030. https://doi.org/10.1093/pcp/pcq160
Samson K, Fischer LI, Roche JAJ M L (2022) Iron Status, Anemia, and Iron Interventions and their Associations with cognitive and academic performance in adolescents. Syst Rev Nutrients 14(1). https://doi.org/10.3390/NU14010224
Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54(4):608–620. https://doi.org/10.1111/j.1365-313X.2008.03461.x
Scheepers M, Spielmann J, Boulanger M, Carnol M, Bosman B, De Pauw E, Goormaghtigh E, Motte P, Hanikenne M (2020) Intertwined metal homeostasis, oxidative and biotic stress responses in the Arabidopsis frd3 mutant. The Plant Journal: For Cell and Molecular Biology 102(1):34–52. https://doi.org/10.1111/TPJ.14610
Schwarz B, Azodi CB, Shiu SH, Bauer P (2020) Putative cis-Regulatory Elements Predict Iron Deficiency responses in Arabidopsis roots. Plant Physiol 182(3):1420–1439. https://doi.org/10.1104/pp.19.00760
Schwarz B, Bauer P (2020) FIT, a regulatory hub for iron deficiency and stress signaling in roots, and FIT-dependent and -independent gene signatures. J Exp Bot 71(5):1694–1705. https://doi.org/10.1093/jxb/eraa012
Shahzad R, Jamil S, Ahmad S, Nisar A, Khan S, Amina Z, Kanwal S, Aslam HMU, Gill RA, Zhou W (2021) Biofortification of Cereals and Pulses using new breeding techniques: current and future perspectives. Front Nutr 8:721728. https://doi.org/10.3389/fnut.2021.721728
Skolmowska D, Głąbska D, Kołota A, Guzek D (2022) Effectiveness of Dietary Interventions to treat Iron-Deficiency Anemia in Women: a systematic review of Randomized controlled trials. Nutrients 14(13). https://doi.org/10.3390/nu14132724
Sperotto RA, Boff T, Duarte GL, Santos LS, Grusak MA, Fett JP (2010) Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains. J Plant Physiol 167(17):1500–1506. https://doi.org/10.1016/j.jplph.2010.05.003
Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139(2):701–712. https://doi.org/10.1104/pp.105.065607
Sun L, Wei YQ, Wu KH, Yan JY, Xu JN, Wu YR, Li GX, Xu JM, Harberd NP, Ding ZJ, Zheng SJ (2021a) Restriction of iron loading into developing seeds by a YABBY transcription factor safeguards successful reproduction in Arabidopsis. Mol Plant 14(10):1624–1639. https://doi.org/10.1016/j.molp.2021.06.005
Sun SK, Xu X, Tang Z, Tang Z, Huang XY, Wirtz M, Hell R, Zhao FJ (2021b) A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain. Nat Commun 12(1):1392. https://doi.org/10.1038/s41467-021-21282-5
Sun Y, Li J, Xia L (2016) Precise Genome Modification via Sequence-Specific Nucleases-Mediated Gene Targeting for Crop Improvement. Frontiers in plant science 7:1928. doi:https://doi.org/10.3389/fpls.2016.01928
Swamy BPM, Marathi B, Ribeiro-Barros AIF, Calayugan MIC, Ricachenevsky FK (2021) Iron Biofortification in Rice: an update on quantitative trait loci and candidate genes. Front Plant Sci 12:647341. https://doi.org/10.3389/fpls.2021.647341
Tanabe N, Noshi M, Mori D, Nozawa K, Tamoi M, Shigeoka S (2019) The basic helix-loop-helix transcription factor, bHLH11 functions in the iron-uptake system in Arabidopsis thaliana. J Plant Res 132(1):93–105. https://doi.org/10.1007/s10265-018-1068-z
Uygun S, Seddon AE, Azodi CB, Shiu SH (2017) Predictive models of spatial transcriptional response to high salinity. Plant Physiol 174(1):450–464. https://doi.org/10.1104/pp.16.01828
Vélez-Bermúdez IC, Schmidt W (2022) How plants recalibrate Cellular Iron Homeostasis. Plant Cell Physiol 36(2):154–162. https://doi.org/10.1093/PCP/PCAB166
Wang L, Ying Y, Narsai R, Ye L, Zheng L, Tian J, Whelan J, Shou H (2013a) Identification of OsbHLH133 as a regulator of iron distribution between roots and shoots in Oryza sativa. Plant Cell Environ 36(1):224–236. https://doi.org/10.1111/j.1365-3040.2012.02569.x
Wang M, Gong J, Bhullar NK (2020a) Iron deficiency triggered transcriptome changes in bread wheat. Comput Struct Biotechnol J 18:2709–2722. https://doi.org/10.1016/j.csbj.2020.09.009
Wang S, Li L, Ying Y, Wang J, Shao JF, Yamaji N, Whelan J, Ma JF, Shou H (2020b) A transcription factor OsbHLH156 regulates strategy II iron acquisition through localising IRO2 to the nucleus in rice. New Phytol 225(3):1247–1260. https://doi.org/10.1111/nph.16232
Wang Y, Huan Q, Li K, Qian W (2021) Single-cell transcriptome atlas of the leaf and root of rice seedlings. J Genet genomics = Yi chuan xue bao 48(10):881–898. https://doi.org/10.1016/j.jgg.2021.06.001
Wani SH, Gaikwad K, Razzaq A, Samantara K, Kumar M, Govindan V (2022) Improving Zinc and Iron Biofortification in Wheat through Genomics Approaches. Mol Biol Rep 49(8):8007–8023. https://doi.org/10.1007/s11033-022-07326-z
Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141(4):1446–1458. https://doi.org/10.1104/pp.106.082586
Wei L, Lee D, Law CT, Zhang MS, Shen J, Chin DW, Zhang A, Tsang FH, Wong CL, Ng IO, Wong CC, Wong CM (2019) Genome-wide CRISPR/Cas9 library screening identified PHGDH as a critical driver for Sorafenib resistance in HCC. Nat Commun 10(1):4681. https://doi.org/10.1038/s41467-019-12606-7
Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol 46(9):1505–1514. https://doi.org/10.1093/pcp/pci163
Yan JY, Li CX, Sun L, Ren JY, Li GX, Ding ZJ, Zheng SJ (2016) A WRKY transcription factor regulates Fe Translocation under Fe Deficiency. Plant Physiol 171(3):2017–2027. https://doi.org/10.1104/pp.16.00252
Yokosho K, Yamaji N, Ma JF (2016) OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. J Exp Bot 67(18):5485–5494. https://doi.org/10.1093/jxb/erw314
Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15(8):613–621. https://doi.org/10.1038/sj.cr.7290331
Zha M, Li X, Li R, Huang J, Fan J, Zhang J, Wang Y, Zhang C (2022) Overexpression of Nicotianamine synthase (AtNAS1) increases Iron Accumulation in the Tuber of Potato. Plants (Basel Switzerland) 11(20). https://doi.org/10.3390/PLANTS11202741
Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Piñeros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T, Guerinot ML, Salt DE, Kochian LV, Vatamaniuk OK (2014) OPT3 is a phloem-specific Iron transporter that is essential for systemic Iron Signaling and Redistribution of Iron and Cadmium in Arabidopsis. Plant Cell 26(5):2249–2264. https://doi.org/10.1105/tpc.114.123737
Zhang H, Li Y, Pu M, Xu P, Liang G, Yu D (2020) Oryza sativa POSITIVE REGULATOR OF IRON DEFICIENCY RESPONSE 2 (OsPRI2) and OsPRI3 are involved in the maintenance of Fe homeostasis. Plant Cell Environ 43(1):261–274. https://doi.org/10.1111/pce.13655
Zhang Y, Massel K, Godwin ID, Gao C (2018) Applications and potential of genome editing in crop improvement. Genome Biol 19(1):210. https://doi.org/10.1186/s13059-018-1586-y
Zhao Q, Ren YR, Wang QJ, Yao YX, You CX, Hao YJ (2016) Overexpression of MdbHLH104 gene enhances the tolerance to iron deficiency in apple. Plant Biotechnol J 14(7):1633–1645. https://doi.org/10.1111/pbi.12526
Zheng X, Kuijer HNJ, Al-Babili S (2021) Carotenoid biofortification of crops in the CRISPR era. Trends Biotechnol 39(9):857–860. https://doi.org/10.1016/j.tibtech.2020.12.003
Zhu XF, Wu Q, Meng YT, Tao Y, Shen RF (2020) AtHAP5A regulates iron translocation in iron-deficient Arabidopsis thaliana. J Integr Plant Biol 62(12):1910–1925. https://doi.org/10.1111/jipb.12984
Acknowledgements
The authors express their gratitude to the National Agri-Food Biotechnology Institute (NABI), Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India for the research facilities and support. S.K. is thankful to the Department of Botany, Central University of Punjab, India for Ph.D. registration. Authors would like to acknowledge DBT-eLibrary Consortium (DelCON) for providing access to online journals.
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This work was supported by National Agri-Food Biotechnology Institute (NABI), Department of Biotechnology (DBT), Ministry of Science & Technology, Government of India.
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S.T. and V.K. conceived and designed the research. S.K. and K.K. performed the literature survey. S.K, K.K. and S.T. wrote the manuscript. S.T. and V.K. contributed in editing and revision of the manuscript.
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Khan, S., Kaur, K., Kumar, V. et al. Iron transport and homeostasis in plants: current updates and applications for improving human nutrition values and sustainable agriculture. Plant Growth Regul 100, 373–390 (2023). https://doi.org/10.1007/s10725-023-00979-1
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DOI: https://doi.org/10.1007/s10725-023-00979-1