Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms

New Phytologist

Volumn 209, Issue 2, 2016, Pages 733-745

  Sisó Terraza, Patricia ^a   Rios, Juan J ^a   Abadía, Javier ^a   Abadía, Anunciación ^a   Álvarez Fernández, Ana ^a  

^a CSIC   (Spain)

Author keywords

Beta vulgaris; Dicotyledoneous plants; Flavins; Iron acquisition; Iron deficiency; Iron nutrition; Redox shuttle; Root secretion

Indexed keywords

CHELATE; DICOTYLEDON; ENZYME ACTIVITY; GRASS; IRON; NUTRITION; OXIDE; PIGMENT; REDOX CONDITIONS; REDUCTION; ROOT SYSTEM; SECRETION; SOLUBILIZATION;

BETA VULGARIS; POACEAE;

FERRIC ION; FERRIC OXIDE; IRON; METAL; NICOTINAMIDE ADENINE DINUCLEOTIDE; RIBOFLAVIN DERIVATIVE;

BEET; DRUG EFFECTS; METABOLISM; PLANT LEAF; PLANT ROOT; SOLUBILITY;

BETA VULGARIS; FERRIC COMPOUNDS; FLAVINS; IRON; METALS; NAD; PLANT LEAVES; PLANT ROOTS; SOLUBILITY;

EID: 84955210690     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13633     Document Type: Article

References (57)

1. Andaluz S, Rodríguez-Celma J, Abadía A, Abadía J, López-Millán AF. 2009. Time course induction of several key enzymes in Medicago truncatula roots in response to Fe deficiency. Plant Physiology and Biochemistry 47: 1082-1088.
2. Balasubramanian R, Levinson BT, Rosenzweig AC. 2010. Secretion of flavins by three species of methanotrophic bacteria. Applied and Environmental Microbiology 76: 7356-7358.
3. Bienfait HF, Bino RJ, Vanderbliek AM, Duivenvoorden JF, Fontaine JM. 1983. Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris. Physiologia Plantarum 59: 196-202.
4. Briat JF, Dubos C, Gaymard F. 2015. Iron nutrition, biomass production, and plant product quality. Trends in Plant Science 20: 33-40.
5. Brutinel ED, Gralnick JA. 2012. Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Applied Microbiology and Biotechnology 93: 41-48.
6. von Canstein H, Ogawa J, Shimizu S, Lloyd JR. 2008. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Applied and Environmental Microbiology 74: 615-623.
7. Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L. 2010. Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil 329: 1-25.
8. Crossley RA, Gaskin DJH, Holmes K, Mulholland F, Wells JM, Kelly DJ, van Vliet AHM, Walton NJ. 2007. Riboflavin biosynthesis is associated with assimilatory ferric reduction and iron acquisition by Campylobacter jejuni. Applied and Environmental Microbiology 73: 7819-7825.
9. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL. 2001. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409: 346-349.
10. 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 Biology 10: 268.
11. Eide D, Broderius M, Fett J, Guerinot ML. 1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences, USA 93: 5624-5628.
12. Fassbinder F, Kist M, Bereswill S. 2000. Structural and functional analysis of the riboflavin synthesis genes encoding GTP cyclohydrolase II (ribA), DHBP synthase (ribBA), riboflavin synthase (ribC), and riboflavin deaminase/reductase (ribD) from Helicobacter pylori strain P1. FEMS Microbiology Letters 191: 191-197.
13. Fodor F, Gáspár L, Morales F, Gogorcena Y, Lucena JJ, Cseh E, Kröpfl K, Abadía J, Sárvári E. 2005. Effects of two iron sources on iron and cadmium allocation in poplar (Populus alba) plants exposed to cadmium. Tree Physiology 25: 1173-1180.
14. Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadía J, Álvarez-Fernández A, Briat JF. 2014. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytologist 201: 155-167.
15. Fuller SJ, McMillan DGG, Renz MB, Schmidt M, Burke IT, Stewart DI. 2014. Extracellular electron transport-mediated Fe(III) reduction by a community of alkaliphilic bacteria that use flavins as electron shuttles. Applied and Environmental Microbiology 80: 128-137.
16. González-Vallejo EB, Susín S, Abadía A, Abadía J. 1998. Changes in sugar beet leaf plasma membrane Fe(III)-chelate reductase activities mediated by Fe-deficiency, assay buffer composition, anaerobiosis and the presence of flavins. Protoplasma 205: 163-168.
17. Hemmerich P, Spence J. 1966. Interaction of flavin with the Mo (V, VI)- and Fe (II, III)-redox systems. Slater EC, ed. Flavins and flavoproteins. Amsterdam, the Netherlands: B. B. A. Library, Elsevier, 82-98.
18. Higa A, Mori Y, Kitamura Y. 2010. Iron deficiency induces changes in riboflavin secretion and the mitochondrial electron transport chain in hairy roots of Hyoscyamus albus. Journal of Plant Physiology 167: 870-878.
19. Jin CW, You GY, He YF, Tang CX, Wu P, Zheng SJ. 2007. Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiology 144: 278-285.
20. Jordan CM, Wakeman RJ, Devay JE. 1992. Toxicity of free riboflavin and methionine-riboflavin solutions to Phytophthora infestans and the reduction of potato late blight disease. Canadian Journal of Microbiology 38: 1108-1111.
21. Kobayashi T, Nishizawa NK, Mori S. 2006. Molecular analysis of iron-deficient graminaceous plants. Barton LL, Abadía J, eds. Iron nutrition in plants and rhizospheric microorganisms. Dordrecht, the Netherlands: Springer, 395-435.
22. Kotloski NJ, Gralnick JA. 2013. Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. MBio 4: 4.
23. Lindsay WL. 1995. Chemical reactions in soils that affect iron availability to plants. A quantative approach. Abadía J, ed. Iron nutrition in soils and plants. Dordrecht, the Netherlands: Kluwer Academic, 7-14.
24. López-Millán AF, Grusak MA, Abadía A, Abadía J. 2013. Iron deficiency in plants: an insight from proteomic approaches. Frontiers in Plant Science 4: 7.
25. López-Millán AF, Morales F, Andaluz S, Gogorcena Y, Abadía A, De Las Rivas J, Abadía J. 2000. Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiology 124: 885-897.
26. López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J. 2001. Iron resupply-mediated deactivation of Fe-deficiency stress responses in roots of sugar beet. Australian Journal of Plant Physiology 28: 171-180.
27. López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J. 2009. Metabolic responses in iron deficient tomato plants. Journal of Plant Physiology 166: 375-384.
28. Madigan M, Martinko J, Parker J. 2003. Brock biology of microorganisms. Upper Saddle River, NJ, USA: Prentice Hall/Pearson Education.
29. nd edn. New York, NY, USA: Academic Press.
30. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. 2008. Shewanella secretes flavins that mediate extracellular electron transfer. Proceedings of the National Academy of Sciences, USA 105: 3968-3973.
31. Mehta-Kolte MG, Bond DR. 2012. Geothrix fermentans secretes two different redox-active compounds to utilize electron acceptors across a wide range of redox potentials. Applied and Environmental Microbiology 78: 6987-6995.
32. Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S. 2014. Rhizospheric organic compounds in the soil-microorganism-plant system: their role in iron availability. European Journal of Soil Science 65: 629-642.
33. Müller F, Hemmerich P, Ehrenberg A. 1968. Light absorption of flavosemiquinone. European Journal of Biochemistry 5: 158-164.
34. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AGM, Martin WF. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiology and Molecular Biology Reviews 76: 444-495.
35. Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK. 2011. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry 286: 5446-5454.
36. Pérez-Sanz A, Lucena JJ. 1995. Synthetic ion oxides as sources of Fe in a hydroponic culture of sunflower. Abadía J, ed. Iron nutrition in soils and plants. Dordrecht, the Netherlands: Kluwer Academic, 241-246.
37. Rellán-Álvarez R, Andaluz S, Rodríguez-Celma J, Wohlgemuth G, Zocchi G, Álvarez-Fernández A, Fiehn O, López-Millán AF, Abadía J. 2010. Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biology 10: 15.
38. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694-697.
39. Rodríguez-Celma J, Lattanzio G, Grusak MA, Abadía A, Abadía J, López-Millán AF. 2011a. Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin biosynthesis. Journal of Proteome Research 10: 2590-2601.
40. Rodríguez-Celma J, Lin WD, Fu GM, Abadía J, López-Millán AF, Schmidt W. 2013. Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiology 162: 1473-1485.
41. Rodríguez-Celma J, Vázquez-Reina S, Orduna J, Abadía A, Abadía J, Álvarez-Fernández A, López-Millán AF. 2011b. Characterization of flavins in roots of Fe-deficient Strategy I plants, with a focus on Medicago truncatula. Plant and Cell Physiology 52: 2173-2189.
42. Römheld V. 1991. The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant and Soil 130: 127-134.
43. Römheld V, Marschner H. 1986. Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiology 80: 175-180.
44. 2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytologist 187: 145-158.
45. Schmid NB, Giehl RFH, Doll S, Mock HP, Strehmel N, Scheel D, Kong XL, Hider RC, von Wirén N. 2014. Feruloyl-CoA 6'-hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiology 164: 160-172.
46. Schmidt H, Gunther C, Weber M, Sporlein C, Loscher S, Bottcher C, Schobert R, Clemens S. 2014. Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS One 9: 11.
47. Senda T, Senda M, Kimura S, Ishida T. 2009. Redox control of protein conformation in flavoproteins. Antioxidants & Redox Signaling 11: 1741-1766.
48. Shi Z, Zachara JM, Shi L, Wang ZM, Moore DA, Kennedy DW, Fredrickson JK. 2012. Redox reactions of reduced flavin mononucleotide (FMN), riboflavin (RBF), and anthraquinone-2, 6-disulfonate (AQDS) with ferrihydrite and lepidocrocite. Environmental Science & Technology 46: 11 644-11 652.
49. Shi Z, Zachara JM, Wang ZM, Shi L, Fredrickson JK. 2013. Reductive dissolution of goethite and hematite by reduced flavins. Geochimica Et Cosmochimica Acta 121: 139-154.
50. Susín S, Abadía A, González-Reyes JA, Lucena JJ, Abadía J. 1996. The pH requirement for in vivo activiy of the iron-deficiency-induced "Turbo" ferric chelate reductase: a comparison of the iron-deficiency-induced iron reductase activities of intact plants and isolated plasma membrane fractions in sugar beet (Beta vulgaris). Plant Physiology 110: 111-123.
51. Susín S, Abián J, Peleato ML, Sánchez-Baeza F, Abadía A, Gelpí E, Abadía J. 1994. Flavin excretion from roots of iron-deficient sugar beet (Beta vulgaris L.). Planta 193: 514-519.
52. Susín S, Abián J, Sánchez-Baeza F, Peleato ML, Abadía A, Gelpí E, Abadía J. 1993. Riboflavin 3'- and 5'-sulfate, two novel flavins accumulating in the roots of iron-deficient sugar-beet (Beta vulgaris). Journal of Biological Chemistry 268: 20 958-20 965.
53. Vigani G. 2012. Discovering the role of mitochondria in the iron deficiency-induced metabolic responses of plants. Journal of Plant Physiology 169: 1-11.
54. Vigani G, Zocchi G. 2010. Effect of Fe deficiency on mitochondrial alternative NAD(P)H dehydrogenases in cucumber roots. Journal of Plant Physiology 167: 666-669.
55. Welkie GW. 2000. Taxonomic distribution of dicotyledonous species capable of root excretion of riboflavin under iron deficiency. Journal of Plant Nutrition 23: 1819-1831.
56. Wu S, Xiao Y, Wang L, Zheng Y, Chang KL, Zheng ZY, Yang ZH, Varcoe JR, Zhao F. 2014. Extracellular electron transfer mediated by flavins in gram-positive Bacillus sp WS-XY1 and yeast Pichia stipitis. Electrochimica Acta 146: 564-567.
57. Zocchi G. 2006. Metabolic changes in iron-stressed dicotyledonous plants. Barton LL, Abadía J, eds. Iron nutrition in plants and rhizospheric microorganisms. Dordrecht, the Netherlands: Springer, 359-370.