MsNRAMP2 Enhances Tolerance to Iron Excess Stress in Nicotiana tabacum and MsMYB Binds to Its Promoter

Iron(Fe) is a trace metal element necessary for plant growth, but excess iron is harmful to plants. Natural resistance-associated macrophage proteins (NRAMPs) are important for divalent metal transport in plants. In this study, we isolated the MsNRAMP2 (MN_547960) gene from alfalfa, the perennial legume forage. The expression of MsNRAMP2 is specifically induced by iron excess. Overexpression of MsNRAMP2 conferred transgenic tobacco tolerance to iron excess, while it conferred yeast sensitivity to excess iron. Together with the MsNRAMP2 gene, MsMYB (MN_547959) expression is induced by excess iron. Y1H indicated that the MsMYB protein could bind to the “CTGTTG” cis element of the MsNRAMP2 promoter. The results indicated that MsNRAMP2 has a function in iron transport and its expression might be regulated by MsMYB. The excess iron tolerance ability enhancement of MsNRAMP2 may be involved in iron transport, sequestration, or redistribution.

[1]  M. Hasanuzzaman,et al.  Silencing of PpNRAMP5 improves manganese toxicity tolerance in peach (Prunus persica) seedlings. , 2023, Journal of hazardous materials.

[2]  R. Xu,et al.  In situ mapping of ion distribution profiles and gene expression reveals interactions between hypoxia and Mn2+/Fe2+ availability in barley roots. , 2023, Plant science : an international journal of experimental plant biology.

[3]  Y. S. Shivay,et al.  Agronomic biofortification of forage crops with Zn and Cu for enhancing nutritive potential- A systematic review. , 2022, Journal of the science of food and agriculture.

[4]  Lixing Yuan,et al.  Tonoplast-localized transporter ZmNRAMP2 confers root-to-shoot translocation of manganese in maize. , 2022, Plant physiology.

[5]  F. Pál-Fám,et al.  Literature Review on the Effects of Heavy Metal Stress and Alleviating Possibilities through Exogenously Applied Agents in Alfalfa (Medicago sativa L.) , 2022, Plants.

[6]  Yan Yu,et al.  ZmNRAMP4 Enhances the Tolerance to Aluminum Stress in Arabidopsis thaliana , 2022, International journal of molecular sciences.

[7]  K. Kozak,et al.  Regulation and Function of Metal Uptake Transporter NtNRAMP3 in Tobacco , 2022, Frontiers in Plant Science.

[8]  L. Dirick,et al.  NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis. , 2022, The Plant journal : for cell and molecular biology.

[9]  Jingzi Beiyuan,et al.  Phytoremediation of potentially toxic elements (PTEs) contaminated soils using alfalfa (Medicago sativa L.): A comprehensive review. , 2022, Chemosphere.

[10]  N. Chen,et al.  The NtNRAMP1 transporter is involved in cadmium and iron transport in tobacco (Nicotiana tabacum). , 2022, Plant physiology and biochemistry : PPB.

[11]  B. Liu,et al.  Identification of Malus halliana R2R3-MYB gene family under iron deficiency stress and functional characteristics of MhR2R3-MYB4 in Arabidopsis thaliana. , 2021, Plant biology.

[12]  Michael J. Haydon,et al.  Root-to-shoot iron partitioning in Arabidopsis requires IRON-REGULATED TRANSPORTER1 (IRT1) protein but not its iron(II) transport function. , 2021, The Plant journal : for cell and molecular biology.

[13]  Fu Chen,et al.  A study on the contamination assessment, health risk and mobility of two heavy metals in the soil-plants-ruminants system of a typical agricultural region in the semi arid environment , 2021, Environmental Science and Pollution Research.

[14]  Huayong Zhang,et al.  Metal speciation distribution of anaerobic fermentation with alfalfa grass harvested from abandoned iron mine and the influence of metals addition , 2021, Process Safety and Environmental Protection.

[15]  A. Kozovits,et al.  Evaluation of metal accumulation in the forage grass Brachiaria decumbens Stapf grown in contaminated soils with iron tailings , 2021, Integrated environmental assessment and management.

[16]  G. Kirk,et al.  Below-ground plant-soil interactions affecting adaptations of rice to iron toxicity. , 2021, Plant, cell & environment.

[17]  K. Wu,et al.  Restriction of Iron Loading into Developing Seeds by A YABBY Transcription Factor Safeguards Successful Reproduction in Arabidopsis. , 2021, Molecular plant.

[18]  Jingjun Li,et al.  The Tonoplast-Localized Transporter OsNRAMP2 is involved in Fe Homeostasis and affects Seed Germination in rice. , 2021, Journal of experimental botany.

[19]  A. Bozzi,et al.  Molecular mechanism of Nramp-family transition metal transport. , 2021, Journal of molecular biology.

[20]  William J. Astle,et al.  A genome-wide meta-analysis yields 46 new loci associating with biomarkers of iron homeostasis , 2021, Communications Biology.

[21]  J. Gong,et al.  Iron deficiency triggered transcriptome changes in bread wheat , 2020, Computational and structural biotechnology journal.

[22]  J. Medina,et al.  Arabidopsis thaliana transcription factors MYB28 AND MYB29 shape ammonium stress responses by regulating fe homeostasis. , 2020, The New phytologist.

[23]  H. Masuda,et al.  How Does Rice Defend Against Excess Iron?: Physiological and Molecular Mechanisms , 2020, Frontiers in Plant Science.

[24]  V. H. Cruz,et al.  Response of soybean to soil waterlogging associated with iron excess in the reproductive stage , 2020, Physiology and Molecular Biology of Plants.

[25]  F. Zhao,et al.  OsNRAMP1 contributes to cadmium and manganese uptake in rice. , 2020, Plant, cell & environment.

[26]  A. Bozzi,et al.  Transmembrane helix 6b links proton and metal release pathways and drives conformational change in an Nramp-family transition metal transporter , 2019, The Journal of Biological Chemistry.

[27]  Lu Zheng,et al.  The Intracellular Transporter AtNRAMP6 Is Involved in Fe Homeostasis in Arabidopsis , 2019, Front. Plant Sci..

[28]  K. Ahmad,et al.  Health risk assessment through determining bioaccumulation of iron in forages grown in soil irrigated with city effluent , 2019, Environmental Science and Pollution Research.

[29]  F. Gaymard,et al.  The Transcriptional Control of Iron Homeostasis in Plants: A Tale of bHLH Transcription Factors? , 2019, Front. Plant Sci..

[30]  Elizabeth L. Mann,et al.  Different iron storage strategies among bloom-forming diatoms , 2018, Proceedings of the National Academy of Sciences.

[31]  Xing Fan,et al.  Cloning and Characterization of TpNRAMP3, a Metal Transporter From Polish Wheat (Triticum polonicum L.) , 2018, Front. Plant Sci..

[32]  A. Bozzi,et al.  Proton co-transport and voltage dependence enforce unidirectional metal transport in an Nramp transporter , 2018, bioRxiv.

[33]  Y. Hao,et al.  MdMYB58 Modulates Fe Homeostasis by Directly Binding to the MdMATE43 Promoter in Plants , 2018, Plant & cell physiology.

[34]  Xing Fan,et al.  Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants , 2018, Planta.

[35]  L. Dirick,et al.  Intracellular Distribution of Manganese by the Trans-Golgi Network Transporter NRAMP2 Is Critical for Photosynthesis and Cellular Redox Homeostasis , 2017, Plant Cell.

[36]  E. Lombi,et al.  Effects of changes in leaf properties mediated by methyl jasmonate (MeJA) on foliar absorption of Zn, Mn and Fe , 2017, Annals of botany.

[37]  T. Walk,et al.  Genome-Wide Identification and Expression Analysis of NRAMP Family Genes in Soybean (Glycine Max L.) , 2017, Front. Plant Sci..

[38]  J. Ariño,et al.  Two NRAMP6 Isoforms Function as Iron and Manganese Transporters and Contribute to Disease Resistance in Rice. , 2017, Molecular plant-microbe interactions : MPMI.

[39]  C. Curie,et al.  The high-affinity metal Transporters NRAMP1 and IRT1 Team up to Take up Iron under Sufficient Metal Provision , 2016, Scientific Reports.

[40]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[41]  H. Gawrońska,et al.  Vegetable sprouts enriched with iron: Effects on yield, ROS generation and antioxidative system , 2016 .

[42]  J. Schroeder,et al.  Mechanisms of abscisic acid-mediated control of stomatal aperture. , 2015, Current opinion in plant biology.

[43]  C. Pieterse,et al.  Rhizobacterial volatiles and photosynthesis‐related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron‐deficiency responses , 2015, The Plant journal : for cell and molecular biology.

[44]  S. Bozzaro,et al.  Dictyostelium Nramp1, which is structurally and functionally similar to mammalian DMT1 transporter, mediates phagosomal iron efflux , 2015, Journal of Cell Science.

[45]  S. Thomine,et al.  Bypassing Iron Storage in Endodermal Vacuoles Rescues the Iron Mobilization Defect in the natural resistance associated-macrophage protein3natural resistance associated-macrophage protein4 Double Mutant1[OPEN] , 2015, Plant Physiology.

[46]  M. M. Lucas,et al.  Medicago truncatula Natural Resistance-Associated Macrophage Protein1 Is Required for Iron Uptake by Rhizobia-Infected Nodule Cells1[OPEN] , 2015, Plant Physiology.

[47]  R. Dutzler,et al.  Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport , 2014, Nature Structural &Molecular Biology.

[48]  C. Pieterse,et al.  β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. , 2014, The New phytologist.

[49]  C. Colombo,et al.  Induction of ferritin synthesis by water deficit and iron excess in common bean (Phaseolus vulgaris L.) , 2014, Molecular Biology Reports.

[50]  J. Xia,et al.  A node-based switch for preferential distribution of manganese in rice , 2013, Nature Communications.

[51]  Haizhen Ma,et al.  Responses of seedling growth and antioxidant activity to excess iron and copper in Triticum aestivum L. , 2012, Ecotoxicology and environmental safety.

[52]  Y. Zuo,et al.  AhNRAMP1 iron transporter is involved in iron acquisition in peanut , 2012, Journal of experimental botany.

[53]  E. Braga,et al.  Responses to excess iron in sweet potato: impacts on growth, enzyme activities, mineral concentrations, and anatomy , 2012, Acta Physiologiae Plantarum.

[54]  R. Takahashi,et al.  Characterizing the role of rice NRAMP5 in Manganese, Iron and Cadmium Transport , 2012, Scientific Reports.

[55]  J. Peters,et al.  Excess iron-induced changes in the photosynthetic characteristics of sweet potato. , 2011, Journal of plant physiology.

[56]  E. Zabaleta,et al.  Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. , 2011, Plant science : an international journal of experimental plant biology.

[57]  Wolfgang Busch,et al.  The bHLH Transcription Factor POPEYE Regulates Response to Iron Deficiency in Arabidopsis Roots[W][OA] , 2010, Plant Cell.

[58]  Magali Schnell Ramos,et al.  Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency1[W] , 2010, Plant Physiology.

[59]  C. Curie,et al.  The NRAMP6 metal transporter contributes to cadmium toxicity. , 2009, The Biochemical journal.

[60]  Zhenhai Han,et al.  An MYB transcription factor from Malus xiaojinensis has a potential role in iron nutrition. , 2008, Journal of integrative plant biology.

[61]  H. Ling,et al.  Transgenic expression of DwMYB2 impairs iron transport from root to shoot in Arabidopsis thaliana , 2006, Cell Research.

[62]  Mark G. M. Aarts,et al.  Large Expression Differences in Genes for Iron and Zinc Homeostasis, Stress Response, and Lignin Biosynthesis Distinguish Roots of Arabidopsis thaliana and the Related Metal Hyperaccumulator Thlaspi caerulescens1[W] , 2006, Plant Physiology.

[63]  N. Nelson,et al.  The NRAMP family of metal-ion transporters. , 2006, Biochimica et biophysica acta.

[64]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[65]  S. Mori,et al.  Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. , 2006, The Plant journal : for cell and molecular biology.

[66]  W. Köster,et al.  Divalent metal transport in the green microalga Chlamydomonas reinhardtii is mediated by a protein similar to prokaryotic Nramp homologues , 2005, Biometals.

[67]  E. Esmans,et al.  Metabolic Fate of Jasmonates in Tobacco Bright Yellow-2 Cells1 , 2004, Plant Physiology.

[68]  M. Ganal,et al.  Differential Regulation of nramp and irt Metal Transporter Genes in Wild Type and Iron Uptake Mutants of Tomato* , 2003, Journal of Biological Chemistry.

[69]  Ji-Yeun Lee,et al.  Photodynamic Effect of Iron Excess on Photosystem II Function in Pea Plants¶ , 2002 .

[70]  J. Ecker,et al.  Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. , 2000, The Biochemical journal.

[71]  C. Winterbourn.  Toxicity of iron and hydrogen peroxide: the Fenton reaction. , 1995, Toxicology letters.

[72]  M. Guerinot,et al.  Iron: Nutritious, Noxious, and Not Readily Available , 1994, Plant physiology.

[73]  D. Gomez-Casati,et al.  Advances in Iron Retrograde Signaling Mechanisms and Uptake Regulation in Photosynthetic Organisms. , 2023, Methods in molecular biology.

[74]  OUP accepted manuscript , 2022, The Plant Cell.

[75]  Chao-Feng Huang,et al.  NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. , 2018, The New phytologist.

[76]  P. Trivedi,et al.  Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. , 2014, Plant, cell & environment.

[77]  Zhou Da-mai.  Analysis and Evaluation of Soil Available Iron Content in Gaobeidian City of Hebei Province , 2013 .

[78]  J. Markovic,et al.  Alfalfa-most important perennial forage legume in animal husbandry , 2009 .

[79]  A. Ranieri,et al.  Iron deficiency differently affects peroxidase isoforms in sunflower. , 2001, Journal of experimental botany.