Cited by 859Plant Micronutrient Interactions and EffectsPlant nutrient uptake and metabolismNitrogen and Sulfur Effects on Brassica

Manganese in Plants: From Acquisition to Subcellular Allocation

Open access
Alejandro, Santiago, Höller, Stefanie, Meier, Bastian, Peiter, Edgar·2020·Frontiers in Plant Science

Abstract

Manganese (Mn) is an important micronutrient for plant growth and development and sustains metabolic roles within different plant cell compartments. The metal is an essential cofactor for the oxygen-evolving complex (OEC) of the photosynthetic machinery, catalyzing the water-splitting reaction in photosystem II (PSII). Despite the importance of Mn for photosynthesis and other processes, the physiological relevance of Mn uptake and compartmentation in plants has been underrated. The subcellular Mn homeostasis to maintain compartmented Mn-dependent metabolic processes like glycosylation, ROS scavenging, and photosynthesis is mediated by a multitude of transport proteins from diverse gene families. However, Mn homeostasis may be disturbed under suboptimal or excessive Mn availability. Mn deficiency is a serious, widespread plant nutritional disorder in dry, well-aerated and calcareous soils, as well as in soils containing high amounts of organic matter, where bio-availability of Mn can decrease far below the level that is required for normal plant growth. By contrast, Mn toxicity occurs on poorly drained and acidic soils in which high amounts of Mn are rendered available. Consequently, plants have evolved mechanisms to tightly regulate Mn uptake, trafficking, and storage. This review provides a comprehensive overview, with a focus on recent advances, on the multiple functions of transporters involved in Mn homeostasis, as well as their regulatory mechanisms in the plant's response to different conditions of Mn availability.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fpls.2020.00300

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 222

  1. Agorio A. Giraudat J. Bianchi M. W. Marion J. Espagne C. Castaings L. (2017). Phosphatidylinositol 3-phosphate–binding protein AtPH1 controls the localization of the metal transporter NRAMP1 in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114 E3354– E3363. 10.1073/pnas.1702975114 28373552 PMC5402440 · DOI
  2. Alam S. Akiha F. Kamei S. Huq S. M. I. Kawai S. (2005). Mechanism of potassium alleviation of manganese phytotoxicity in barley. J. Plant Nutr. 28 889– 901. 10.1081/pln-200055572 · DOI
  3. Alejandro S. Cailliatte R. Alcon C. Dirick L. Domergue F. Correia D. (2017). Intracellular distribution of manganese by the trans-Golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. Plant Cell 29 3068– 3084. 10.1105/tpc.17.00578 29180598 PMC5757278 · DOI
  4. Allen M. D. Kropat J. Tottey S. Del Campo J. A. Merchant S. S. (2007). Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol. 143 263– 277. 10.1104/pp.106.088609 17085511 PMC1761973 · DOI
  5. Amao Y. Ohashi A. (2008). Effect of Mn ion on the visible light induced water oxidation activity of photosynthetic organ grana from spinach. Catal. Commun. 10 217– 220. 10.1016/j.catcom.2008.08.022 · DOI
  6. Araki R. Murata J. Murata Y. (2011). A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal-phytosiderophore complexes. Plant Cell Physiol. 52 1931– 1940. 10.1093/pcp/pcr126 21937676 · DOI
  7. Baldisserotto C. Ferroni L. Anfuso E. Pagnoni A. Fasulo M. P. Pancaldi S. (2007). Responses of Trapa natans L. floating laminae to high concentrations of manganese. Protoplasma 231 65– 82. 10.1007/s00709-007-0242-2 17602280 · DOI
  8. Basu D. Tian L. Wang W. Bobbs S. Herock H. Travers A. (2015). A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. BMC Plant Biol. 15: 295. 10.1186/s12870-015-0670-7 26690932 PMC4687291 · DOI
  9. Bereczky Z. Wang H. Y. Schubert V. Ganal M. Bauer P. (2003). Differential regulation of nramp and irt metal transporter genes in wild type and iron uptake mutants of tomato. J. Biol. Chem. 278 24697– 24704. 10.1074/jbc.m301365200 12709425 · DOI
  10. Blamey F. P. C. Hernandez-Soriano M. Cheng M. Tang C. Paterson D. Lombi E. (2015). Synchrotron-based techniques shed light on mechanisms of plant sensitivity and tolerance to high manganese in the root environment. Plant Physiol. 169 2006– 2020. 10.1104/pp.15.00726 26395840 PMC4634059 · DOI
  11. Bloom A. J. (2019). Metal regulation of metabolism. Curr. Opin. Chem. Biol. 49 33– 38. 10.1016/j.cbpa.2018.09.017 30296690 · DOI
  12. Bloom A. J. Lancaster K. M. (2018). Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nat. Plants 4 414– 422. 10.1038/s41477-018-0191-0 29967515 · DOI
  13. Bondarava N. Un S. Krieger-Liszkay A. (2007). Manganese binding to the 23 kDa extrinsic protein of photosystem II. Biochim. Biophys. Acta Bioenerg. 1767 583– 588. 10.1016/j.bbabio.2007.01.001 17292849 · DOI
  14. Brandenburg F. Schoffman H. Kurz S. Krämer U. Keren N. Weber A. P. M. (2017). The Synechocystis manganese exporter Mnx is essential for manganese homeostasis in cyanobacteria. Plant Physiol. 173 1798– 1810. 10.1104/pp.16.01895 28153926 PMC5338678 · DOI
  15. Bricker T. M. Roose J. L. Fagerlund R. D. Frankel L. K. Eaton-Rye J. J. (2012). The extrinsic proteins of Photosystem II. Biochim. Biophys. Acta Bioenerg. 1817 121– 142. 21801710
  16. Broadley M. Brown P. Cakmak I. Rengel Z. Zhao F. (2012). “ Function of nutrients: micronutrients,” in Marschner’s Mineral Nutrition of Higher Plants, 3rd Edn, ed. Marschner P. (Oxford: Elsevier), 191– 249.
  17. Burnell J. N. (1988). “The biochemistry of manganese in plants,” in Manganese in Soils and Plants, eds Graham R. D. Hannam R. J. Uren N. C. (Dordrecht: Springer), 125– 137.
  18. Cailliatte R. Schikora A. Briat J.-F. Mari S. Curie C. (2010). High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22 904– 917. 10.1105/tpc.109.073023 20228245 PMC2861449 · DOI
  19. Cao F. Q. Werner A. K. Dahncke K. Romeis T. Liu L. H. Witte C. P. (2010). Identification and characterization of proteins involved in rice urea and arginine catabolism. Plant Physiol. 154 98– 108. 10.1104/pp.110.160929 20631318 PMC2938139 · DOI
  20. Cao J. (2019). Molecular evolution of the vacuolar iron transporter (VIT) family genes in 14 plant species. Genes 10: 144. 10.3390/genes10020144 30769903 PMC6409731 · DOI
  21. Castaings L. Caquot A. Loubet S. Curie C. (2016). The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci. Rep. 6 37222– 37222. 10.1038/srep37222 27849020 PMC5110964 · DOI
  22. Chen Z. Fujii Y. Yamaji N. Masuda S. Takemoto Y. Kamiya T. (2013). Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J. Exp. Bot. 64 4375– 4387. 10.1093/jxb/ert243 23963678 PMC3808320 · DOI
  23. Cheng N.-H. Pittman J. K. Shigaki T. Hirschi K. D. (2002). Characterization of CAX4, an Arabidopsis H+ /cation antiporter. Plant Physiol. 128 1245– 1254. 10.1104/pp.010857 11950973 PMC154252 · DOI
  24. Chereskin B. M. Castelfranco P. A. (1982). Effects of iron and oxygen on chlorophyll biosynthesis. Plant Physiol. 69 112– 116. 10.1104/pp.69.1.112 16662140 PMC426156 · DOI
  25. Chu H.-H. Car S. Socha A. L. Hindt M. N. Punshon T. Guerinot M. L. (2017). The Arabidopsis MTP8 transporter determines the localization of manganese and iron in seeds. Sci. Rep. 7 11024– 11024. 10.1038/s41598-017-11250-9 28887568 PMC5591227 · DOI
  26. Clairmont K. B. Hagar W. G. Davis E. A. (1986). Manganese toxicity to chlorophyll synthesis in tobacco callus. Plant Physiol. 80 291– 293. 10.1104/pp.80.1.291 16664602 PMC1075100 · DOI
  27. Collin S. Justin A. M. Cantrel C. Arondel V. Kader J. C. (1999). Identification of AtPIS, a phosphatidylinositol synthase from Arabidopsis. Eur. J. Biochem. 262 652– 658. 10.1046/j.1432-1327.1999.00378.x 10411624 · DOI
  28. Connorton J. M. Jones E. R. Rodríguez-Ramiro I. Fairweather-Tait S. Uauy C. Balk J. (2017). Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiol. 174 2434– 2444. 10.1104/pp.17.00672 28684433 PMC5543970 · DOI
  29. Connorton J. M. Webster R. E. Cheng N. Pittman J. K. (2012). Knockout of multiple Arabidopsis cation/H+ exchangers suggests isoform-specific roles in metal stress response, germination and seed mineral nutrition. PLoS One 7: e47455. 10.1371/journal.pone.0047455 23071810 PMC3470555 · DOI
  30. Cornah J. E. Roper J. M. Singh D. P. Smith A. G. (2002). Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem. J. 362 423– 432. 10.1042/bj3620423 11853551 PMC1222403 · DOI
  31. Corpas F. J. Barroso J. B. Palma J. M. Rodriguez-Ruiz M. (2017). Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol. 11 535– 542. 10.1016/j.redox.2016.12.033 28092771 PMC5238456 · DOI
  32. Curie C. Alonso J. M. Le Jean M. Ecker J. R. Briat J.-F. (2000). Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. 347: 749. 10.1042/0264-6021:3470749 10769179 PMC1221012 · DOI
  33. Delhaize E. Gruber B. D. Pittman J. K. White R. G. Leung H. Miao Y. (2007). A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J. 51 198– 210. 10.1111/j.1365-313x.2007.03138.x 17559518 · DOI
  34. Delhaize E. Kataoka T. Hebb D. M. White R. G. Ryan P. R. (2003). Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15 1131– 1142. 10.1105/tpc.009134 12724539 PMC153721 · DOI
  35. Demaegd D. Colinet A. S. Deschamps A. Morsomme P. (2014). Molecular evolution of a novel family of putative calcium transporters. PLoS One 9: e100851. 10.1371/journal.pone.0100851 24955841 PMC4067407 · DOI
  36. Demaegd D. Foulquier F. Colinet A. S. Gremillon L. Legrand D. Mariot P. (2013). Newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proc. Natl. Acad. Sci. U.S.A. 110 6859– 6864. 10.1073/pnas.1219871110 23569283 PMC3637739 · DOI
  37. Doncheva S. Poschenrieder C. Stoyanova Z. Georgieva K. Velichkova M. Barceló J. (2009). Silicon amelioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environ. Exp. Bot. 65 189– 197. 10.1016/j.envexpbot.2008.11.006 · DOI · Paper page
  38. Dou C. M. Fu X. P. Chen X. C. Shi J. Y. Chen Y. X. (2009). Accumulation and detoxification of manganese in hyperaccumulator Phytolacca americana. Plant Biol. 11 664– 670. 10.1111/j.1438-8677.2008.00163.x 19689773 · DOI
  39. Dubeaux G. Neveu J. Zelazny E. Vert G. (2018). Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. Mol. Cell 69 953– 964. 10.1016/j.molcel.2018.02.009 29547723 · DOI
  40. Dučić T. Polle A. (2007). Manganese toxicity in two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca) seedlings as affected by phosphorus supply. Funct. Plant Biol. 34 31– 40. 32689329
  41. Eckhardt U. Mas Marques A. Buckhout T. J. (2001). Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol. Biol. 45 437– 448. 11352462
  42. Edmond C. Shigaki T. Ewert S. Nelson M. D. Connorton J. M. Chalova V. (2009). Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem. J. 418 145– 154. 10.1042/BJ20081814 18950291 · DOI
  43. Egelund J. Petersen B. L. Motawia M. S. Damager I. Faik A. Olsen C. E. (2006). Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi-localized (1,3)-alpha-D-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan-II. Plant Cell 18 2593– 2607. 10.1105/tpc.105.036566 17056709 PMC1626629 · DOI
  44. Eisenhut M. Hoecker N. Schmidt S. B. Basgaran R. M. Flachbart S. Jahns P. (2018). The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis. Mol. Plant 11 955– 969. 10.1016/j.molp.2018.04.008 29734002 · DOI
  45. Emsley J. (2003). Nature’s Building Blocks: An A-Z Guide to the Elements. Oxford: Oxford University Press.
  46. Engelsma G. (1972). A possible role of divalent manganese ions in the photoinduction of phenylalanine ammonia-lyase. Plant Physiol. 50 599– 602. 10.1104/pp.50.5.599 16658225 PMC366198 · DOI
  47. Erbasol I. Bozdag G. O. Koc A. Pedas P. Karakaya H. C. (2013). Characterization of two genes encoding metal tolerance proteins from Beta vulgaris subspecies maritima that confers manganese tolerance in yeast. Biometals 26 795– 804. 10.1007/s10534-013-9658-7 23864431 · DOI
  48. Eroglu S. Giehl R. F. H. Meier B. Takahashi M. Terada Y. Ignatyev K. (2017). Metal tolerance protein 8 mediates manganese homeostasis and iron reallocation during seed development and germination. Plant Physiol. 174 1633– 1647. 10.1104/pp.16.01646 28461400 PMC5490884 · DOI
  49. Eroglu S. Meier B. von Wirén N. Peiter E. (2016). The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiol. 170 1030– 1045. 10.1104/pp.15.01194 26668333 PMC4734556 · DOI
  50. Farthing E. C. Menguer P. K. Fett J. P. Williams L. E. (2017). OsMTP11 is localised at the Golgi and contributes to Mn tolerance. Sci. Rep. 7: 15258. 10.1038/s41598-017-15324-6 29127328 PMC5681648 · DOI
  51. Farzadfar S. Zarinkamar F. Hojati M. (2017). Magnesium and manganese affect photosynthesis, essential oil composition and phenolic compounds of Tanacetum parthenium. Plant Physiol. Biochem. 112 207– 217. 10.1016/j.plaphy.2017.01.002 28092849 · DOI
  52. Fecht-Christoffers M. M. Führs H. Braun H. P. Horst W. J. (2006). The role of hydrogen peroxide-producing and hydrogen peroxide-consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiol. 140 1451– 1463. 10.1104/pp.105.070474 16489137 PMC1435823 · DOI
  53. Fernando D. R. Bakkaus E. J. Perrier N. Baker A. J. Woodrow I. E. Batianoff G. N. (2006a). Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytol. 171 751– 758. 10.1111/j.1469-8137.2006.01783.x 16918546 · DOI
  54. Fernando D. R. Batianoff G. N. Baker A. J. Woodrow I. E. (2006b). In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Environ. 29 1012– 1020. 10.1111/j.1365-3040.2006.01498.x 17087483 · DOI
  55. Fernando D. R. Lynch J. P. (2015). Manganese phytotoxicity: new light on an old problem. Annals Bot. 116 313– 319. 10.1093/aob/mcv111 26311708 PMC4549964 · DOI
  56. Fernando D. R. Mizuno T. Woodrow I. E. (2010). Characterization of foliar manganese (Mn) in Mn (hyper) accumulators using X−ray absorption spectroscopy. New Phytol. 188 1014– 1027. 10.1111/j.1469-8137.2010.03431.x 20819177 · DOI
  57. Ferrandon M. Chamel A. R. (1988). Cuticular retention, foliar absorption and translocation of Fe, Mn and Zn supplied in organic and inorganic form. J. Plant Nutr. 11 247– 263. 10.1080/01904168809363800 · DOI
  58. Frank J. Happeck R. Meier B. Hoang M. T. T. Stribny J. Hause G. (2019). Chloroplast-localized BICAT proteins shape stromal calcium signals and are required for efficient photosynthesis. New Phytol. 221 866– 880. 10.1111/nph.15407 30169890 · DOI
  59. Fu X.-Z. Zhou X. Xing F. Ling L.-L. Chun C.-P. Cao L. (2017). Genome-wide identification, cloning and functional analysis of the Zinc/Iron-Regulated Transporter-Like Protein (ZIP) gene family in trifoliate orange (Poncirus trifoliata L. Raf.). Front. Plant Sci. 8: 588. 10.3389/fpls.2017.00588 28469631 PMC5395618 · DOI
  60. Führs H. Behrens C. Gallien S. Heintz D. Van Dorsselaer A. Braun H. P. (2010). Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare). Ann. Bot. 105 1129– 1140. 10.1093/aob/mcq046 20237113 PMC2887067 · DOI
  61. Gao H. Xie W. Yang C. Xu J. Li J. Wang H. (2018). NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol. 217 179– 193. 10.1111/nph.14783 28913895 · DOI
  62. Gao Y. Q. Chen J. G. Chen Z. R. An D. Lv Q. Y. Han M. L. (2017). A new vesicle trafficking regulator CTL1 plays a crucial role in ion homeostasis. PLoS Biol. 15: e2002978. 10.1371/journal.pbio.2002978 29284002 PMC5746208 · DOI
  63. George T. S. French A. S. Brown L. K. Karley A. J. White P. J. Ramsay L. (2014). Genotypic variation in the ability of landraces and commercial cereal varieties to avoid manganese deficiency in soils with limited manganese availability: is there a role for root-exuded phytases? Physiol. Plant. 151 243– 256. 10.1111/ppl.12151 24438182 · DOI
  64. Gherardi M. J. Rengel Z. (2004). The effect of manganese supply on exudation of carboxylates by roots of lucerne (Medicago sativa). Plant Soil 260 271– 282. 10.1023/b:plso.0000030182.11473.3b · DOI
  65. Giles C. D. Brown L. K. Adu M. O. Mezeli M. M. Sandral G. A. Simpson R. J. (2017). Response-based selection of barley cultivars and legume species for complementarity: root morphology and exudation in relation to nutrient source. Plant Sci. 255 12– 28. 10.1016/j.plantsci.2016.11.002 28131338 · DOI
  66. Glynn S. E. Baker P. J. Sedelnikova S. E. Davies C. L. Eadsforth T. C. Levy C. W. (2005). Structure and mechanism of imidazoleglycerol-phosphate dehydratase. Structure 13 1809– 1817. 10.1016/j.str.2005.08.012 16338409 · DOI
  67. Goulding K. W. T. (2016). Soil acidification and the importance of liming agricultural soils with particular reference to the United Kingdom. Soil Use Manag. 32 390– 399. 10.1111/sum.12270 27708478 PMC5032897 · DOI
  68. Gregory A. L. Hurley B. A. Tran H. T. Valentine A. J. She Y. M. Knowles V. L. (2009). In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. Biochem. J. 420 57– 65. 10.1042/BJ20082397 19228119 PMC2677216 · DOI
  69. Hajiboland R. (2012). “Effect of micronutrient deficiencies on plants stress responses,” in Abiotic Stress Responses in Plants, eds Ahmad P. Prasad M. (New York, NY: Springer), 283– 329. 10.1007/978-1-4614-0634-1_16 · DOI
  70. Hansel C. M. Zeiner C. A. Santelli C. M. Webb S. M. (2012). Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proc. Natl. Acad. Sci. U.S.A. 109 12621– 12625. 10.1073/pnas.1203885109 22802654 PMC3412038 · DOI
  71. Hashimoto K. Eckert C. Anschütz U. Scholz M. Held K. Waadt R. (2012). Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. J. Biol. Chem. 287 7956– 7968. 10.1074/jbc.M111.279331 22253446 PMC3318702 · DOI
  72. Hauck M. Paul A. Gross S. Raubuch M. (2003). Manganese toxicity in epiphytic lichens: chlorophyll degradation and interaction with iron and phosphorus. Environ. Exp. Bot. 49 181– 191. 10.1016/s0098-8472(02)00069-2 · DOI
  73. Hebbern C. A. Laursen K. H. Ladegaard A. H. Schmidt S. B. Pedas P. Bruhn D. (2009). Latent manganese deficiency increases transpiration in barley (Hordeum vulgare). Physiol. Plant. 135 307– 316. 10.1111/j.1399-3054.2008.01188.x 19140891 · DOI
  74. Hebbern C. A. Pedas P. Schjoerring J. K. Knudsen L. Husted S. (2005). Genotypic differences in manganese efficiency: field experiments with winter barley (Hordeum vulgare L.). Plant Soil 272 233– 244. 10.1007/s11104-004-5048-9 · DOI
  75. Heckman J. R. Clarke B. B. Murphy J. A. (2003). Optimizing manganese fertilization for the suppression of take-all patch disease on creeping bentgrass. Crop Sci. 43 1395– 1398. 10.2135/cropsci2003.1395 · DOI
  76. Heine G. Max J. F. J. Führs H. Moran-Puente D. W. Heintz D. Horst W. J. (2011). Effect of manganese on the resistance of tomato to Pseudocercospora fuligena. J. Plant Nutr. Soil Sci. 174 827– 836. 10.1002/jpln.201000440 · DOI
  77. Henriques F. S. (2004). Reduction in chloroplast number accounts for the decrease in the photosynthetic capacity of Mn-deficient pecan leaves. Plant Sci. 166 1051– 1055. 10.1016/j.plantsci.2003.12.022 · DOI
  78. Hirschi K. D. Korenkov V. D. Wilganowski N. L. Wagner G. J. (2000). Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol. 124 125– 134. 10.1104/pp.124.1.125 10982428 PMC59128 · DOI
  79. Hoecker N. Leister D. Schneider A. (2017). Plants contain small families of UPF0016 proteins including the PHOTOSYNTHESIS AFFECTED MUTANT71 transporter. Plant Signal. Behav 12: e1278101. 10.1080/15592324.2016.1278101 28075225 PMC5351731 · DOI
  80. Hou L. Gu D. Li Y. Li J. Li J. Chen X. (2019). Phylogenetic and expression analysis of Mn-CDF transporters in pear (Pyrus bretschneideri Rehd.). Plant Mol. Biol. Report. 37 98– 110. 10.1007/s11105-019-01142-9 · DOI
  81. Hsieh M. H. Chang C. Y. Hsu S. J. Chen J. J. (2008). Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Mol. Biol. 66 663– 673. 10.1007/s11103-008-9297-5 18236010 · DOI
  82. Huang Y. L. Yang S. Long G. X. Zhao Z. K. Li X. F. Gu M. H. (2016). Manganese toxicity in sugarcane plantlets grown on acidic soils of southern China. PLoS One 11: e0148956. 10.1371/journal.pone.0148956 27023702 PMC4811547 · DOI
  83. Husted S. Laursen K. H. Hebbern C. A. Schmidt S. B. Pedas P. Haldrup A. (2009). Manganese deficiency leads to genotype-specific changes in fluorescence induction kinetics and state transitions. Plant Physiol. 150 825– 833. 10.1104/pp.108.134601 19369593 PMC2689976 · DOI
  84. Ihnatowicz A. Siwinska J. Meharg A. A. Carey M. Koornneef M. Reymond M. (2014). Conserved histidine of metal transporter AtNRAMP1 is crucial for optimal plant growth under manganese deficiency at chilling temperatures. New Phytol. 202 1173– 1183. 10.1111/nph.12737 24571269 · DOI
  85. Ishimaru Y. Masuda H. Bashir K. Inoue H. Tsukamoto T. Takahashi M. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62 379– 390. 10.1111/j.1365-313X.2010.04158.x 20128878 · DOI
  86. Ishimaru Y. Takahashi R. Bashir K. Shimo H. Senoura T. Sugimoto K. (2012). Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci. Rep. 2: 286. 10.1038/srep00286 22368778 PMC3285952 · DOI
  87. Jauregui M. A. Reisenauer H. M. (1982). Dissolution of oxides of manganese and iron by root exudate components. Soil Sci. Soc. Am. J. 46 314– 317. 10.2136/sssaj1982.03615995004600020020x · DOI
  88. Johnson N. A. Liu F. Weeks P. D. Hentzen A. E. Kruse H. P. Parker J. J. (2009). A tomato ER-type Ca2 +-ATPase, LCA1, has a low thapsigargin-sensitivity and can transport manganese. Arch. Biochem. Biophys. 481 157– 168. 10.1016/j.abb.2008.11.010 19056336 · DOI
  89. Kamer K. J. Sancak Y. Fomina Y. Meisel J. D. Chaudhuri D. Grabarek Z. (2018). MICU1 imparts the mitochondrial uniporter with the ability to discriminate between Ca2 + and Mn2 +. Proc. Natl. Acad. Sci. U.S.A. 115 E7960– E7969. 10.1073/pnas.1807811115 30082385 PMC6112746 · DOI
  90. Kamiya T. Akahori T. Ashikari M. Maeshima M. (2006). Expression of the vacuolar Ca2 +/H+ exchanger, OsCAX1a, in rice: cell and age specificity of expression, and enhancement by Ca2 +. Plant Cell Physiol. 47 96– 106. 10.1093/pcp/pci227 16275657 · DOI
  91. Kamiya T. Akahori T. Maeshima M. (2005). Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. Plant Cell Physiol. 46 1735– 1740. 10.1093/pcp/pci173 16043430 · DOI
  92. Kamrul Huda K. M. Yadav S. Akhter Banu M. S. Trivedi D. K. Tuteja N. (2013). Genome-wide analysis of plant-type II Ca2 + ATPases gene family from rice and Arabidopsis: potential role in abiotic stresses. Plant Physiol. Biochem. 65 32– 47. 10.1016/j.plaphy.2013.01.002 23416494 · DOI
  93. Khabaz-Saberi H. Setter T. L. Waters I. (2006). Waterlogging induces high to toxic concentrations of iron, aluminum, and manganese in wheat varieties on acidic soil. J. Plant Nutr. 29 899– 911. 10.1080/01904160600649161 · DOI
  94. Kim K. N. Lee J. S. Han H. Choi S. A. Go S. J. Yoon I. S. (2003). Isolation and characterization of a novel rice Ca2 +-regulated protein kinase gene involved in responses to diverse signals including cold, light, cytokinins, sugars and salts. Plant Mol. Biol. 52 1191– 1202. 10.1023/b:plan.0000004330.62660.a2 14682618 · DOI
  95. Kim S. A. Punshon T. Lanzirotti A. Li L. Alonso J. M. Ecker J. R. (2006). Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314 1295– 1298. 10.1126/science.1132563 17082420 · DOI
  96. Kirichok Y. Krapivinsky G. Clapham D. E. (2004). The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427 360– 364. 10.1038/nature02246 14737170 · DOI · Paper page
  97. Koike S. Inoue H. Mizuno D. Takahashi M. Nakanishi H. Mori S. (2004). OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39 415– 424. 10.1111/j.1365-313x.2004.02146.x 15255870 · DOI
  98. Köllner T. G. Held M. Lenk C. Hiltpold I. Turlings T. C. J. Gershenzon J. (2008). A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20 482– 494. 10.1105/tpc.107.051672 18296628 PMC2276456 · DOI
  99. Koren’kov V. Park S. Cheng N. H. Sreevidya C. Lachmansingh J. Morris J. (2007). Enhanced Cd2 +-selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225 403– 411. 10.1007/s00425-006-0352-7 16845524 · DOI
  100. Korshunova Y. O. Eide D. Clark W. G. Guerinot M. L. Pakrasi H. B. (1999). The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40 37– 44. 10394943
  101. Lambers H. Hayes P. E. Laliberté E. Oliveira R. S. Turner B. L. (2015). Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci. 20 83– 90. 10.1016/j.tplants.2014.10.007 25466977 · DOI
  102. Lane B. G. (2002). Oxalate, germins, and higher-plant pathogens. IUBMB Life 53 67– 75. 10.1080/15216540211474 12049198 · DOI
  103. Lanquar V. Lelièvre F. Barbier-Brygoo H. Thomine S. (2004). Regulation and function of AtNRAMP4 metal transporter protein. Soil Sci. Plant Nutr. 50 1141– 1150. 10.1080/00380768.2004.10408587 · DOI
  104. Lanquar V. Lelièvre F. Bolte S. Hamès C. Alcon C. Neumann D. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24 4041– 4051. 10.1038/sj.emboj.7600864 16270029 PMC1356305 · DOI
  105. Lanquar V. Schnell Ramos M. Lelièvre F. Barbier-Brygoo H. Krieger-Liszkay A. Krämer U. (2010). Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. 152 1986– 1999. 10.1104/pp.109.150946 20181755 PMC2850043 · DOI
  106. LeClere S. Tellez R. Rampey R. A. Matsuda S. P. T. Bartel B. (2002). Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J. Biol. Chem. 277 20446– 20452. 10.1074/jbc.m111955200 11923288 · DOI
  107. Lešková A. Giehl R. F. H. Hartmann A. Fargašová A. von Wirén N. (2017). Heavy metals induce iron deficiency responses at different hierarchic and regulatory levels. Plant Physiol. 174 1648– 1668. 10.1104/pp.16.01916 28500270 PMC5490887 · DOI
  108. Li C. Wang P. Menzies N. W. Lombi E. Kopittke P. M. (2017). Effects of changes in leaf properties mediated by methyl jasmonate (MeJA) on foliar absorption of Zn, Mn and Fe. Ann. Bot. 120 405– 415. 10.1093/aob/mcx063 28641371 PMC5591425 · DOI
  109. Li J. Y. Liu J. Dong D. Jia X. Mccouch S. R. Kochian L. V. (2014). Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc. Natl. Acad. Sci. U.S.A. 111 6503– 6508. 10.1073/pnas.1318975111 24728832 PMC4035919 · DOI
  110. Li L. Xu X. Chen C. Shen Z. (2016). Genome-wide characterization and expression analysis of the Germin-like protein family in rice and Arabidopsis. Int. J. Mol. Sci. 17: 1622. 10.3390/ijms17101622 27669230 PMC5085655 · DOI
  111. Li L. Yang X. (2018). The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid. Med. Cell. Longev. 2018: 7580707. 10.1155/2018/7580707 29849912 PMC5907490 · DOI
  112. Li Q. Chen L. S. Jiang H. X. Tang N. Yang L. T. Lin Z. H. (2010). Effects of manganese-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol. 10: 42. 10.1186/1471-2229-10-42 20205939 PMC2848762 · DOI
  113. Li X. Chanroj S. Wu Z. Romanowsky S. M. Harper J. F. Sze H. (2008). A distinct endosomal Ca2 +/Mn2 + pump affects root growth through the secretory process. Plant Physiol. 147 1675– 1689. 10.1104/pp.108.119909 18567829 PMC2492598 · DOI
  114. Liang F. Cunningham K. W. Harper J. F. Sze H. (1997). ECA1 complements yeast mutants defective in Ca2 + pumps and encodes an endoplasmic reticulum-type Ca2 +-ATPase in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 94 8579– 8584. 10.1073/pnas.94.16.8579 9238019 PMC23025 · DOI
  115. Lidon F. C. Barreiro M. G. Ramalho J. C. (2004). Manganese accumulation in rice: implications for photosynthetic functioning. J. Plant Physiol. 161 1235– 1244. 10.1016/j.jplph.2004.02.003 15602815 · DOI
  116. Liu J. Gao Y. Tang Y. Wang D. Chen X. Yao Y. (2019). Genome-wide identification, comprehensive gene feature, evolution, and expression analysis of plant metal tolerance proteins in tobacco under heavy metal toxicity. Front. Genet. 10: 345. 10.3389/fgene.2019.00345 31105736 PMC6491887 · DOI
  117. Long L. Persson D. P. Duan F. Jørgensen K. Yuan L. Schjoerring J. K. (2018). The iron-regulated transporter 1 plays an essential role in uptake, translocation and grain-loading of manganese, but not iron, in barley. New Phytol. 217 1640– 1653. 10.1111/nph.14930 29206303 · DOI
  118. Longnecker N. E. Graham R. D. Card G. (1991). Effects of manganese deficiency on the pattern of tillering and development of barley (Hordeum vulgare c.v. galleon). Field Crops Res. 28 85– 102. 10.1016/0378-4290(91)90076-8 · DOI
  119. López-Millán A. F. Ellis D. R. Grusak M. A. (2004). Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol. Biol. 54 583– 596. 10.1023/b:plan.0000038271.96019.aa 15316291 · DOI
  120. Lovely D. R. (1995). Microbial reduction of iron, manganese, and other metals. Adv. Agron. 54 175– 231. 10.1016/s0065-2113(08)60900-1 · DOI
  121. Ma G. Li J. Li J. Li Y. Gu D. Chen C. (2018). OsMTP11, a trans-Golgi network localized transporter, is involved in manganese tolerance in rice. Plant Sci. 274 59– 69. 10.1016/j.plantsci.2018.05.011 30080641 · DOI
  122. Martinoia E. Meyer S. De Angeli A. Nagy R. (2012). Vacuolar transporters in their physiological context. Annu. Rev. Plant Biol. 63 183– 213. 10.1146/annurev-arplant-042811-105608 22404463 · DOI
  123. Martins V. Carneiro F. Conde C. Sottomayor M. Gerós H. (2017). The grapevine VvCAX3 is a cation/H+ exchanger involved in vacuolar Ca2 + homeostasis. Planta 246 1083– 1096. 10.1007/s00425-017-2754-0 28801786 · DOI
  124. Matsushima R. Hayashi Y. Yamada K. Shimada T. Nishimura M. Hara-Nishimura I. (2003). The ER body, a novel endoplasmic reticulum-derived structure in Arabidopsis. Plant Cell Physiol. 44 661– 666. 10.1093/pcp/pcg089 12881493 · DOI
  125. McNaughton R. L. Reddi A. R. Clement M. H. S. Sharma A. Barnese K. Rosenfeld L. (2010). Probing in vivo Mn2 + speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc. Natl. Acad. Sci U.S.A. 107 15335– 15339. 10.1073/pnas.1009648107 20702768 PMC2932569 · DOI · Paper page
  126. McNear D. H. Küpper J. V. (2014). Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale. Plant Soil 377 407– 422. 10.1007/s11104-013-2003-7 · DOI
  127. Mei H. Cheng N. H. Zhao J. Park S. Escareno R. A. Pittman J. K. (2009). Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol. 183 95– 105. 10.1111/j.1469-8137.2009.02831.x 19368667 · DOI
  128. Meinhard M. Rodriguez P. L. Grill E. (2002). The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214 775– 782. 10.1007/s00425-001-0675-3 11882947 · DOI
  129. Membré N. Bernier F. Staiger D. Berna A. (2000). Arabidopsis thaliana germin-like proteins: common and specific features point to a variety of functions. Planta 211 345– 354. 10.1007/s004250000277 10987552 · DOI
  130. Meng J. G. Zhang X. D. Tan S. K. Zhao K. X. Yang Z. M. (2017). Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP1 mediated by miR167 in Brassica napus. Biometals 30 917– 931. 10.1007/s10534-017-0057-3 28993932 · DOI
  131. Migocka M. Papierniak A. Kosieradzka A. Posyniak E. Maciaszczyk-Dziubinska E. Biskup R. (2015). Cucumber metal tolerance protein CsMTP9 is a plasma membrane H+-coupled antiporter involved in the Mn2 + and Cd2 + efflux from root cells. Plant J. 84 1045– 1058. 10.1111/tpj.13056 26485215 · DOI
  132. Millaleo R. Reyes-Díaz M. Alberdi M. Ivanov A. G. Krol M. Hüner N. P. A. (2013). Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J. Exp. Bot. 64 343– 354. 10.1093/jxb/ers339 23183256 PMC3528040 · DOI
  133. Millaleo R. Reyes-Diaz M. Ivanov A. G. Mora M. L. Alberdi M. (2010). Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J. Soil Sci. Plant Nutr. 10 470– 481. 10.4067/s0718-95162010000200008 · DOI
  134. Mills R. F. Doherty M. L. Lopez-Marques R. L. Weimar T. Dupree P. Palmgren M. G. (2007). ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146 116– 128. 10.1104/pp.107.110817 18024560 PMC2230566 · DOI
  135. Milner M. J. Seamon J. Craft E. Kochian L. V. (2013). Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J. Exp. Bot. 64 369– 381. 10.1093/jxb/ers315 23264639 PMC3528025 · DOI
  136. Montanini B. Blaudez D. Jeandroz S. Sanders D. Chalot M. (2007). Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8: 107. 10.1186/1471-2164-8-107 17448255 PMC1868760 · DOI
  137. Morgan J. J. (2005). Kinetics of reaction between O2 and Mn(II) species in aqueous solutions. Geochim. Cosmochim. Acta 69 35– 48. 10.1016/j.gca.2004.06.013 · DOI
  138. Morgan P. W. Joham H. E. Amin J. V. (1966). Effect of manganese toxicity on the indoleacetic acid oxidase system of cotton. Plant Physiol. 41 718– 724. 10.1104/pp.41.4.718 16656311 PMC1086411 · DOI
  139. Morris J. Tian H. Park S. Sreevidya C. S. Ward J. M. Hirschi K. D. (2008). AtCCX3 is an Arabidopsis endomembrane H+-dependent K+ transporter. Plant Physiol. 148 1474– 1486. 10.1104/pp.108.118810 18775974 PMC2577254 · DOI
  140. Nable R. O. Houtz R. L. Cheniae G. M. (1988). Early inhibition of photosynthesis during development of Mn toxicity in tobacco. Plant Physiol. 86 1136– 1142. 10.1104/pp.86.4.1136 16666045 PMC1054641 · DOI
  141. Nevo Y. Nelson N. (2006). The NRAMP family of metal-ion transporters. Biochim. Biophys. Acta Mol. Cell Res. 1763 609– 620. 10.1016/j.bbamcr.2006.05.007 16908340 · DOI
  142. Nian L. S. (1989). Manganese induced iron chlorosis in pineapple and its control by foliar application of iron-citrate. J. Plant Nutr. Soil Sci. 152 125– 126. 10.1002/jpln.19891520122 · DOI
  143. Nowicki M. Müller F. Frentzen M. (2005). Cardiolipin synthase of Arabidopsis thaliana. FEBS Lett. 579 2161– 2165. 10.1016/j.febslet.2005.03.007 15811335 · DOI
  144. Nuruzzaman M. Lambers H. Bolland M. D. A. Veneklaas E. J. (2006). Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281 109– 120. 10.1007/s11104-005-3936-2 · DOI
  145. Ohki K. (1985). Manganese deficiency and toxicity effects on photosynthesis, chlorophyll, and transpiration in Wheat. Crop Sci. 25 187– 191. 10.2135/cropsci1985.0011183x002500010045x · DOI
  146. Önnerud H. Zhang L. Gellerstedt G. Henriksson G. (2002). Polymerization of monolignols by redox shuttle–mediated enzymatic oxidation. Plant Cell 14 1953– 1962. 10.1105/tpc.001487 12172033 PMC151476 · DOI
  147. Oomen R. J. F. J. Wu J. Lelièvre F. Blanchet S. Richaud P. Barbier-Brygoo H. (2009). Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol. 181 637– 650. 10.1111/j.1469-8137.2008.02694.x 19054339 · DOI · Paper page
  148. Panda S. Mishra A. K. Biswal U. C. (1987). Manganese induced peroxidation of thylakoid lipids and changes in chlorophyll-α fluorescence during aging of cell free chloroplasts in light. Phytochemistry 26 3217– 3219. 10.1016/s0031-9422(00)82472-3 · DOI
  149. Papadakis I. E. Giannakoula A. Therios I. N. Bosabalidis A. M. Moustakas M. Nastou A. (2007). Mn-induced changes in leaf structure and chloroplast ultrastructure of Citrus volkameriana (L.) plants. J. Plant Physiol. 164 100– 103. 10.1016/j.jplph.2006.04.011 16781796 · DOI
  150. Pedas P. Hebbern C. A. Schjoerring J. K. Holm P. E. Husted S. (2005). Differential capacity for high-affinity manganese uptake contributes to differences between barley genotypes in tolerance to low manganese availability. Plant Physiol. 139 1411– 1420. 10.1104/pp.105.067561 16244151 PMC1283776 · DOI
  151. Pedas P. Husted S. Skytte K. Schjoerring J. K. (2011). Elevated phosphorus impedes manganese acquisition by barley plants. Front. Plant Sci. 2: 37. 10.3389/fpls.2011.00037 22639592 PMC3355622 · DOI
  152. Pedas P. Stokholm M. S. Hegelund J. N. Ladegård A. H. Schjoerring J. K. Husted S. (2014). Golgi localized barley MTP8 proteins facilitate Mn transport. PLoS One 9: e113759. 10.1371/journal.pone.0113759 25486417 PMC4259309 · DOI
  153. Pedas P. Ytting C. K. Fuglsang A. T. Jahn T. P. Schjoerring J. K. Husted S. (2008). Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol. 148 455– 466. 10.1104/pp.108.118851 18614714 PMC2528110 · DOI
  154. Peiter E. Montanini B. Gobert A. Pedas P. Husted S. Maathuis F. J. M. (2007). A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc. Natl. Acad. Sci. U.S.A. 104 8532– 8537. 10.1073/pnas.0609507104 17494768 PMC1895984 · DOI · Paper page
  155. Peris-Peris C. Serra-Cardona A. Sánchez-Sanuy F. Campo S. Ariño J. San Segundo B. (2017). Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice. Mol. Plant Microbe Interact. 30 385– 398. 10.1094/MPMI-01-17-0005-R 28430017 · DOI
  156. Pittman J. K. (2005). Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol. 167 733– 742. 10.1111/j.1469-8137.2005.01453.x 16101910 · DOI
  157. Pittman J. K. Hirschi K. D. (2016). Phylogenetic analysis and protein structure modelling identifies distinct Ca2 +/cation antiporters and conservation of gene family structure within Arabidopsis and rice species. Rice 9: 3 10.1186/s12284-016-0075-8 PMC4735048 26833031 · DOI
  158. Pittman J. K. Shigaki T. Marshall J. L. Morris J. L. Cheng N. Hirschi K. D. (2004). Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol. Biol. 56 959– 971. 10.1007/s11103-004-6446-3 15821993 · DOI
  159. Pottier M. Oomen R. Picco C. Giraudat J. Scholz-Starke J. Richaud P. (2015). Identification of mutations allowing natural resistance associated macrophage proteins (NRAMP) to discriminate against cadmium. Plant J. 83 625– 637. 10.1111/tpj.12914 26088788 · DOI
  160. Reddi A. R. Jensen L. T. Naranuntarat A. Rosenfeld L. Leung E. Shah R. (2009). The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Radic. Biol. Med. 46 154– 162. 10.1016/j.freeradbiomed.2008.09.032 18973803 PMC2707084 · DOI
  161. Requena L. Bornemann S. (1999). Barley (Hordeum vulgare) oxalate oxidase is a manganese-containing enzyme. Biochem. J. 343 185– 190. 10.1042/bj3430185 10493928 PMC1220540 · DOI
  162. Robert H. S. Offringa R. (2008). Regulation of auxin transport polarity by AGC kinases. Curr. Opin. Plant Biol. 11 495– 502. 10.1016/j.pbi.2008.06.004 18640868 · DOI
  163. Rodríguez-Celma J. Tsai Y.-H. Wen T.-N. Wu Y.-C. Curie C. Schmidt W. (2016). Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots. Sci. Rep. 6 35846– 35846. 10.1038/srep35846 27804982 PMC5090222 · DOI
  164. Rohdich F. Lauw S. Kaiser J. Feicht R. Köhler P. Bacher A. (2006). Isoprenoid biosynthesis in plants - 2C-methyl-D-erythritol-4-phosphate synthase (IspC protein) of Arabidopsis thaliana. FEBS J. 273 4446– 4458. 10.1111/j.1742-4658.2006.05446.x 16972937 · DOI
  165. Rohdich F. Wungsintaweekul J. Eisenreich W. Richter G. Schuhr C. A. Hecht S. (2000). Biosynthesis of terpenoids: 4-diphosphocytidyl-2C-methyl-D-erythritol synthase of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 97 6451– 6456. 10.1073/pnas.97.12.6451 10841550 PMC18623 · DOI
  166. Sasaki A. Yamaji N. Xia J. Ma J. F. (2011). OsYSL6 is involved in the detoxification of excess manganese in rice. Plant Physiol. 157 1832– 1840. 10.1104/pp.111.186031 21969384 PMC3327210 · DOI
  167. Sasaki A. Yamaji N. Yokosho K. Ma J. F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24 2155– 2167. 10.1105/tpc.112.096925 22589467 PMC3442593 · DOI
  168. Schaaf G. Ludewig U. Erenoglu B. E. Mori S. Kitahara T. von Wirén N. (2004). ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. 279 9091– 9096. 10.1074/jbc.m311799200 14699112 · DOI
  169. Schenk G. Ge Y. Carrington L. E. Wynne C. J. Searle I. R. Carroll B. J. (1999). Binuclear metal centers in plant purple acid phosphatases: Fe-Zn in sweet potato and Fe-Zn in soybean. Arch. Biochem. Biophys. 370 183– 189. 10.1006/abbi.1999.1407 10510276 · DOI
  170. Schmidt S. B. Jensen P. E. Husted S. (2016). Manganese deficiency in plants: The impact on photosystem II. Trends Plant Sci. 21 622– 632. 10.1016/j.tplants.2016.03.001 27150384 · DOI
  171. Schneider A. Steinberger I. Herdean A. Gandini C. Eisenhut M. Kurz S. (2016). The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. Plant Cell 28 892– 910. 10.1105/tpc.15.00812 27020959 PMC4863382 · DOI
  172. Schweighofer A. Hirt H. Meskiene I. (2004). Plant PP2C phosphatases: Emerging functions in stress signaling. Trends Plant Sci. 9 236– 243. 10.1016/j.tplants.2004.03.007 15130549 · DOI
  173. Sello S. Moscatiello R. Mehlmer N. Leonardelli M. Carraretto L. Cortese E. (2018). Chloroplast Ca2 + fluxes into and across thylakoids revealed by thylakoid-targeted aequorin probes. Plant Physiol. 177 38– 51. 10.1104/pp.18.00027 29559589 PMC5933129 · DOI
  174. Shao J. F. Yamaji N. Shen R. F. Ma J. F. (2017). The key to Mn homeostasis in plants: regulation of Mn transporters. Trends Plant Sci. 22 215– 224. 10.1016/j.tplants.2016.12.005 28087151 · DOI
  175. Shigaki T. Pittman J. K. Hirschi K. D. (2003). Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J. Biol. Chem. 278 6610– 6617. 10.1074/jbc.M209952200 12496310 · DOI
  176. Socha A. L. Guerinot M. L. (2014). Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front. Plant Sci. 5: 106. 10.3389/fpls.2014.00106 24744764 PMC3978347 · DOI
  177. Sparrow L. A. Uren N. C. (2014). Manganese oxidation and reduction in soils: effects of temperature, water potential, pH and their interactions. Soil Res. 52 483– 494. 10.1071/SR13159 · DOI
  178. St.Clair S. B. Lynch J. P. (2005). Element accumulation patterns of deciduous and evergreen tree seedlings on acid soils: implications for sensitivity to manganese toxicity. Tree Physiol. 25 85– 92. 10.1093/treephys/25.1.85 15519989 · DOI
  179. Stael S. Wurzinger B. Mair A. Mehlmer N. Vothknecht U. C. Teige M. (2012). Plant organellar calcium signalling: an emerging field. J. Exp. Bot. 63 1525– 1542. 10.1093/jxb/err394 22200666 PMC3966264 · DOI
  180. Stengel A. Gügel I. L. Hilger D. Rengstl B. Jung H. Nickelsen J. (2012). Initial steps of photosystem II de novo assembly and preloading with manganese take place in biogenesis centers in Synechocystis. Plant Cell 24 660– 675. 10.1105/tpc.111.093914 22319052 PMC3315239 · DOI
  181. Stoltz E. Wallenhammar A. C. (2014). Manganese application increases winter hardiness in barley. Field Crops Res. 164 148– 153. 10.1016/j.fcr.2014.05.008 · DOI
  182. Strasser R. Bondili J. S. Vavra U. Schoberer J. Svoboda B. Glossl J. (2007). A unique β1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19 2278– 2292. 10.1105/tpc.107.052985 17630273 PMC1955701 · DOI
  183. Stumm W. Morgan J. J. (1996). Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. New York, NY: Wiley.
  184. Svedruzic D. Jonsson S. Toyota C. G. Reinhardt L. A. Ricagno S. Lindqvist Y. (2005). The enzymes of oxalate metabolism: unexpected structures and mechanisms. Arch. Biochem. Biophys. 433 176– 192. 10.1016/j.abb.2004.08.032 15581576 · DOI
  185. Szurmak B. Wysłouch-Cieszyńska A. Wszelaka-Rylik M. Bal W. Dobrzańska M. (2008). A diadenosine 5′,5″-P1P4 tetraphosphate (Ap4A) hydrolase from Arabidopsis thaliana that is activated preferentially by Mn2 + ions. Acta Biochim. Polon. 55 151– 160. 10.18388/abp.2008_3173 18345354 · DOI
  186. Takahashi S. Sakamoto A. N. Tanaka A. Shimizu K. (2007). AtREV1, a Y-family DNA polymerase in Arabidopsis, has deoxynucleotidyl transferase activity in vitro. Plant Physiol. 145 1052– 1060. 10.1104/pp.107.101980 17827267 PMC2048784 · DOI
  187. Takemoto Y. Tsunemitsu Y. Fujii-Kashino M. Mitani-Ueno N. Yamaji N. Ma J. F. (2017). The tonoplast-localized transporter MTP8.2 contributes to manganese detoxification in the shoots and roots of Oryza sativa L. Plant Cell Physiol. 58 1573– 1582. 10.1093/pcp/pcx082 28633293 · DOI
  188. Teardo E. Carraretto L. Moscatiello R. Cortese E. Vicario M. Festa M. (2019). A chloroplast-localized mitochondrial calcium uniporter transduces osmotic stress in Arabidopsis. Nat. Plants 5 581– 588. 10.1038/s41477-019-0434-8 31182842 · DOI
  189. Thomine S. Lelièvre F. Debarbieux E. Schroeder J. I. Barbier-Brygoo H. (2003). AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34 685– 695. 10.1046/j.1365-313X.2003.01760.x 12787249 · DOI
  190. Thomine S. Wang R. Ward J. M. Crawford N. M. Schroeder J. I. (2000). Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. U.S.A. 97 4991– 4996. 10.1073/pnas.97.9.4991 10781110 PMC18345 · DOI
  191. Tiwari M. Sharma D. Dwivedi S. Singh M. Tripathi R. D. Trivedi P. K. (2014). Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ. 37 140– 152. 10.1111/pce.12138 23700971 · DOI
  192. Tsukamoto T. Nakanishi H. Kiyomiya S. Watanabe S. Matsuhashi S. Nishizawa N. K. (2006). 52Mn translocation in barley monitored using a positron-emitting tracer imaging system. Soil Sci. Plant Nutr. 52 717– 725. 10.1111/j.1747-0765.2006.00096.x · DOI
  193. Tsunemitsu Y. Genga M. Okada T. Yamaji N. Ma J. F. Miyazaki A. (2018). A member of cation diffusion facilitator family, MTP11, is required for manganese tolerance and high fertility in rice. Planta 248 231– 241. 10.1007/s00425-018-2890-1 29700611 · DOI
  194. Ueno D. Sasaki A. Yamaji N. Miyaji T. Fujii Y. Takemoto Y. (2015). A polarly localized transporter for efficient manganese uptake in rice. Nat. Plants 1: 15170. 10.1038/nplants.2015.170 27251715 · DOI
  195. Ullah I. Wang Y. Eide D. J. Dunwell J. M. (2018). Evolution, and functional analysis of natural resistance-associated macrophage proteins (NRAMPs) from Theobroma cacao and their role in cadmium accumulation. Sci. Rep. 8: 14412. 10.1038/s41598-018-32819-y 30258092 PMC6158261 · DOI
  196. Venkidasamy B. Selvaraj D. Ramalingam S. (2019). Genome-wide analysis of purple acid phosphatase (PAP) family proteins in Jatropha curcas L. Int. J. Biol. Macromol. 123 648– 656. 10.1016/j.ijbiomac.2018.11.027 30414420 · DOI
  197. Wagner S. Behera S. De Bortoli S. Logan D. C. Fuchs P. Carraretto L. (2015). The EF-hand Ca2 + binding protein MICU choreographs mitochondrial Ca2 + dynamics in Arabidopsis. Plant Cell 27 3190– 3212. 10.1105/tpc.15.00509 26530087 PMC4682298 · DOI
  198. Wang C. Xu W. Jin H. Zhang T. Lai J. Zhou X. (2016). A putative chloroplast-localized Ca2 +/H+ antiporter CCHA1 is involved in calcium and pH homeostasis and required for PSII function in Arabidopsis. Mol. Plant 9 1183– 1196. 10.1016/j.molp.2016.05.015 27302341 · DOI
  199. Wang N. Qiu W. Dai J. Guo X. Lu Q. Wang T. (2019). AhNRAMP1 enhances manganese and zinc uptake in plants. Front. Plant Sci. 10: 415. 10.3389/fpls.2019.00415 31134101 PMC6514220 · DOI
  200. Wang X. Zhong F. Woo C. H. Miao Y. Grusak M. A. Zhang X. (2017). A rapid and efficient method to study the function of crop plant transporters in Arabidopsis. Protoplasma 254 737– 747. 10.1007/s00709-016-0987-6 27240439 · DOI

200 of 222 shown

Cited by

Sorted by citations

Authors
Alejandro, S., Höller, S., Meier, B., & Peiter, E.
Affiliations
Martin Luther University Halle-Wittenberg (DE)
Corresponding author
  • Alejandro, Santiago
  • Peiter, Edgar
Venue
Frontiers in Plant Science
Published
2020-03-26
Volume
11
Pages
300-300
ISSN
1664-462X (ISSN-L)
OpenAlex
W3013601849
Cited by
859
References
4
Citations by year
2026: 146 · 2025: 181 · 2024: 146 · 2023: 160 · 2022: 127 · 2021: 88 · 2020: 11
FWCI
8.16
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Digitalen Hochschulbibliothek Sachsen-Anhalt (Universitäts- und Landesbibliothek Sachsen-Anhalt) (cc-by)
Funders
  • Deutsche Forschungsgemeinschaft
  • European Regional Development Fund (ZS/2016/06/79740)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nitrogen and Sulfur Effects on Brassica
Keywords
manganese, manganese transporter, manganese deficiency, manganese toxicity, photosystem II, oxygen-evolving complex, manganese uptake, reactive oxygen species scavenging, glycosylation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review