Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency

New Phytologist

Volumn 201, Issue 1, 2014, Pages 155-167

  Fourcroy, Pierre ^a   Sisó Terraza, Patricia ^b   Sudre, Damien ^a   Savirón, María ^c   Reyt, Guilhem ^a   Gaymard, Frédéric ^a   Abadía, Anunciación ^b   Abadia, Javier ^b   Álvarez Fernández, Ana ^b   Briat, Jean François ^a  

^a CNRS   (France)

^b CSIC   (Spain)

^c UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

ABC transporter; Coumarins; Iron (Fe) nutrition; Phenolic compounds; Root secretion

Indexed keywords

BIOACCUMULATION; FUNCTIONAL ROLE; GENE EXPRESSION; IRON; MUTATION; NUTRITIONAL STATUS; PHENOLIC COMPOUND; PHYTOCHEMISTRY; ROOT SYSTEM; SECRETION;

ARABIDOPSIS;

ABC TRANSPORTER; ARABIDOPSIS PROTEIN; COUMARIN DERIVATIVE; IRON; PDR9 PROTEIN, ARABIDOPSIS; SCOPOLETIN;

ADAPTATION; ARABIDOPSIS; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IRON (FE) NUTRITION; METABOLISM; MUTATION; PHENOLIC COMPOUNDS; PHYSIOLOGICAL STRESS; PLANT GENE; PLANT ROOT; ROOT SECRETION; TANDEM MASS SPECTROMETRY; TRANSPORT AT THE CELLULAR LEVEL; UPREGULATION;

ABC TRANSPORTER; COUMARINS; IRON (FE) NUTRITION; PHENOLIC COMPOUNDS; ROOT SECRETION;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; IRON; METABOLIC NETWORKS AND PATHWAYS; MUTATION; PLANT ROOTS; SCOPOLETIN; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; UP-REGULATION;

EID: 84888307631     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12471     Document Type: Article

References (43)

1. Bashir K, Ishimaru Y, Shimo H, Kakei Y, Senoura T, Takahashi R, Sato Y, Sato Y, Uozumi N, Nakanishi H et al. 2011. Rice phenolics efflux transporter 2 (PEZ2) plays an important role in solubilizing apoplasmic iron. Soil Science and Plant Nutrition 57: 803-812.
2. Bristow AWT. 2006. Accurate mass measurement for the determination of elemental formula-a tutorial. Mass Spectrometry Reviews 25: 99-111.
3. Brown JC, Ambler JE. 1973. "Reductants" released by roots of Fe-deficient soybeans. Agronomy Journal 65: 311-314.
4. 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.
5. Crosby DG, Berthold RV. 1962. Fluorescence spectra of some simple coumarins. Analytical Biochemistry 4: 349-357.
6. 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.
7. Do CT, Pollet B, Thévenin J, Sibout R, Denoue D, Barrière Y, Lapierre C, Jouanin L. 2007. Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignins, flavonoids and synapoyl malate biosynthesis in Arabidopsis. Planta 226: 1117-1129.
8. Donnini S, De Nisi P, Gabotti D, Tato L, Zocchi G. 2012. Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability. Plant, Cell & Environment 35: 1171-1184.
9. Ducos E, Fraysse S, Boutry M. 2005. NtPDR3, an iron-deficiency inducible ABC transporter in Nicotiana tabacum. FEBS Letters 579: 6791-6795.
10. Eide D, Broderius M, Fett J, 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.
11. Gnonlonfin GJB, Sanni A, Brimer L. 2012. Review scopoletin - a coumarin phytoalexin with medicinal properties. Critical Reviews in Plant Sciences 31: 47-56.
12. 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.
13. 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.
14. 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. Journal of Biological Chemistry 286: 24 649-24 655.
15. Ito H, Gray WM. 2006. A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiology 142: 63-74.
16. Jin CW, He YF, Tang CX, Wu P, Zheng SJ. 2006. Mechanisms of microbially enhanced Fe acquisition in red clover (Trifolium pratense L.). Plant, Cell & Environment 29: 888-897.
17. Jin CW, You GY, He YF, Tang C, 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.
18. Kai K, Mizutani M, Kawamura N, Yamamoto R, Tamai M, Yamaguchi H, Sakata K, Shimizu B. 2008. Scopoletin is biosynthesized via orthohydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant Journal 55: 989-999.
19. Kai K, Shimizu B, Mizutani M, Watanabe K, Sakata K. 2006. Accumulation of coumarins in Arabidopsis thaliana. Phytochemistry 67: 379-386.
20. Lan P, Li W, Wen TN, Shiau JY, Wu YC, Lin W, Schmidt W. 2011. iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Physiology 155: 821-834.
21. Lindsay WL, Schwab AP. 1982. The chemistry of iron in soils and its availability to plants. Journal of Plant Nutrition 5: 821-840.
22. 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: 885-898.
23. Mladenka P, Macáková K, Zatloukalová L, Reháková Z, Singh BK, Prasad AK, Parmar VS, Jahodár L, Hrdina R, Saso L. 2010. In vitro interactions of coumarins with iron. Biochimie 92: 1108-1114.
24. Morrissey J, Guerinot ML. 2009. Iron uptake and transport in plants: the good, the bad, and the ionome. Chemical Reviews 109: 4553-4567.
25. 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. Journal of Biological Chemistry 286: 5446-5454.
26. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694-697.
27. 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 62: 1473-1485.
28. Rodríguez-Celma J, Vázquez-Reina S, Orduna J, Abadía A, Abadía J, Álvarez-Fernández A, López-Millán AF. 2011. Characterization of flavins in roots of Fe-deficient strategy I plants, with a focus on Medicago truncatula. Plant & Cell Physiology 52: 2173-2189.
29. Römheld V, Marschner H. 1983. Mechanism of iron uptake by peanut plants I. Fe reduction, chelate splitting, and release of phenolics. Plant Physiology 71: 949-954.
30. Ruzicka K, Strader LC, Bailly A, Yang H, Blakeslee J, Langowski L, Nejedlá E, Fujita H, Itoh H, Syono K et al. 2010. Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proceedings of the National Academy of Sciences, USA 107: 10749-10753.
31. Santi S, Schmidt W. 2009. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytologist 183: 1072-1084.
32. Schmidt W. 1999. Mechanisms and regulation of reduction-based iron uptake in plants. New Phytologist 141: 1-26.
33. Strader LC, Bartel B. 2009. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21: 1992-2007.
34. Strader LC, Monroe-Augustus M, Rogers KC, Lin GL, Bartel B. 2008. Arabidopsis iba response5 suppressors separate responses to various hormones. Genetics 180: 2019-2031.
35. 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: 20958-20965.
36. Terry N. 1980. Limiting factors in photosynthesis: I. Use of iron stress to control photochemical capacity in vivo. Plant Physiology 65: 114-120.
37. Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E et al. 2008. Plant ABC proteins- a unified nomenclature and updated inventory. Trends in Plant Science 13: 151-159.
38. Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223-1233.
39. Vose PB. 1982. Iron nutrition in plants: a world overview. Journal of Plant Nutrition 5: 233-249.
40. Walker TS, Harsh HP, Halligan KM, Stermitz FR, Vivanco JM. 2003. Metabolic profiling of root exudates of Arabidopsis thaliana. Journal of Agricultural and Food Chemistry 51: 2548-2554.
41. Yang TJ, Lin WD, Schmidt W. 2010. Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiology 152: 2130-2141.
42. Yi Y, Guerinot ML. 1996. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant Journal 10: 835-844.
43. Yoshino M, Murakami K. 1998. Interaction of iron with polyphenolic compounds: application to antioxidant characterization. Analytical Biochemistry 257: 40-44.