Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil

Plant, Cell and Environment

Volumn 36, Issue 10, 2013, Pages 1888-1902

  Xiong, Hongchun ^a   Kakei, Yusuke ^b   Kobayashi, Takanori ^b,c   Guo, Xiaotong ^a   Nakazono, Mikio ^b,d   Takahashi, Hirokazu ^b,d   Nakanishi, Hiromi ^b   Shen, Hongyun ^a   Zhang, Fusuo ^a   Nishizawa, Naoko K ^b,c   Zuo, Yuanmei ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF TOKYO   (Japan)

^c ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

Iron transporter; Peanut maize intercropping; Phytosiderophores; YSL

Indexed keywords

AGRICULTURAL ECOSYSTEM; CALCAREOUS SOIL; INTERCROPPING; MAIZE; NUTRITION;

ARACHIS HYPOGAEA; TRITICUM AESTIVUM; ZEA MAYS;

2' DEOXYMUGINEIC ACID; 2'-DEOXYMUGINEIC ACID; AZETIDINE 2 CARBOXYLIC ACID; DRUG DERIVATIVE; IRON; SIDEROPHORE;

AGRICULTURE; ARTICLE; DRUG EFFECT; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROPONICS; IN SITU HYBRIDIZATION; IRON TRANSPORTER; LIQUID CHROMATOGRAPHY; MAIZE; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PEANUT; PEANUT/MAIZE INTERCROPPING; PHYTOSIDEROPHORES; PLANT GENE; PLANT ROOT; SACCHAROMYCES CEREVISIAE; SOIL; YSL;

IRON TRANSPORTER; PEANUT/MAIZE INTERCROPPING; PHYTOSIDEROPHORES; YSL;

AGRICULTURE; ARACHIS HYPOGAEA; AZETIDINECARBOXYLIC ACID; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; HYDROPONICS; IN SITU HYBRIDIZATION; IRON; MOLECULAR SEQUENCE DATA; MUTATION; PLANT ROOTS; SACCHAROMYCES CEREVISIAE; SIDEROPHORES; SOIL; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; ZEA MAYS;

EID: 84883554471     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12097     Document Type: Article

References (72)

1. Abadía J., Vázquez S., Rellán-Álvarez R., El-Jendoubi H., Abadía A., Álvarez-Fernández A. & López-Millán A.F. (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiology and Biochemistry 49, 471-482.
2. Aoyama T., Kobayashi T., Takahashi M., Nagasaka S., Usuda K., Kakei Y., Ishimaru Y., Nakanishi H., Mori S. & Nishizawa N.K. (2009) OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Molecular Biology 70, 681-692.
3. 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 and Cell Physiology 52, 1931-1940.
4. Awad F., Römheld V. & Marschner H. (1988) Mobilization of ferric iron from a calcareous soil by plant-borne chelators (Phytosiderophores). Journal of Plant Nutrition 11, 701-713.
5. Bashir K., Inoue H., Nagasaka S., Takahashi M., Nakanishi H., Mori S. & Nishizawa N.K. (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. Journal of Biological Chemistry 281, 32395-32402.
6. Brown J.C., Jolley V.D. & Mellytle C. (1991) Comparative evaluation of iron solubilizing substances (phytosiderophores) released by oats and corn: iron-efficient and iron-inefficient plants. Plant and Soil 130, 157-163.
7. 59Fe-uptake in citrus. Plant and Soil 287, 223-233.
8. Chu H.H., Chiecko J., Punshon T., Lanzirotti A., Lahner B., Salt D.E. & Walker E.L. (2010) Successful reproduction requires the function of Arabidopsis yellow stripe-like1 and yellow stripe-like3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiology 154, 197-210.
9. Connolly E.L., Fett J.P. & Guerinot M.L. (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. The Plant Cell 14, 1347-1357.
10. Curie C., Panaviene Z., Loulergue C., Dellaporta S.L., Briat J.F. & Walker E.L. (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346-349.
11. DiDonato R.J., Jr Roberts L.A., Sanderson T., Eisley R.B. & Walker E.L. (2004) Arabidopsis yellow stripe-like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. The Plant Journal 39, 403-414.
12. Ding H., Duan L., Wu H., Yang R., Ling H., Li W.X. & Zhang F. (2009) Regulation of AhFRO1, an Fe(III)-chelate reductase of peanut, during iron deficiency stress and intercropping with maize. Physiologia Plantarum 136, 274-283.
13. Ding H., Duan L., Li J., Yan H., Zhao M., Zhang F. & Li W.X. (2010) Cloning and functional analysis of the peanut iron transporter AhIRT1 during iron deficiency stress and intercropping with maize. Journal of Plant Physiology 167, 996-1002.
14. Eide D., Broderius M., Fett J. & Guerinot M.L. (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences of the United States of America 93, 5624-5628.
15. Gendre D., Czernic P., Conejero G., Pianelli K., Briat J.F., Lebrun M. & Mari S. (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. The Plant Journal 49, 1-15.
16. Gietz R.D. & Schiestl R.H. (1995) Transforming yeast with DNA. Method in Molecular and Cellular Biology 5, 255-269.
17. Guerinot M.L. & Yi Y. (1994) Iron: nutritious, noxious, and not readily available. Plant Physiology 104, 815-820.
18. Gunes A., Bagci E.G. & Inal A. (2007a) Interspecific facilitative root interactions and rhizosphere effects on phosphorus and iron nutrition between mixed grown chickpea and barley. Journal of Plant Nutrition 30, 1455-1469.
19. Gunes A., Inal A., Adak M.S., Alpaslan M., Bagci E.G., Erol T. & Pilbeam D.J. (2007b) Mineral nutrition of wheat, chickpea and lentil as affected by mixed cropping and soil moisture. Nutrient Cycling in Agroecosystems 78, 83-96.
20. Hall T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95-98.
21. Henriques R., Jásik J., Klein M., Martinoia E., Feller U., Schell J., Pais M.S. & Koncz C. (2002) Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Molecular Biology 50, 587-597.
22. Higuchi K., Suzuki K., Nakanishi H., Yamaguchi H., Nishizawa N.K. & Mori S. (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of photosiderophores. Plant Physiology 119, 471-479.
23. Higuchi K., Watanabe S., Takahashi M., Kawasaki S., Nakanishi H., Nishizawa N.K. & Mori S. (2001) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. The Plant Journal 25, 159-167.
24. Hopkinsa B.G., Jolleya V.D. & Brown J.C. (1992) Plant utilization of iron solubilized by oat phytosiderophore. Journal of Plant Nutrition 15, 1599-1612.
25. Inal A. & Gunes A. (2008) Interspecific root interactions and rhizosphere effects on salt ions and nutrient uptake between mixed grown peanut/maize and peanut/barley in original saline-sodic-boron toxic soil. Journal of Plant Physiology 165, 490-503.
26. Inal A., Gunes A., Zhang F. & Cakmak I. (2007) Peanut/maize intercropping induced changes in rhizosphere and nutrient concentrations in shoots. Plant Physiology and Biochemistry 45, 350-356.
27. Inoue H., Kobayashi T., Nozoye T., Takahashi M., Kakei Y., Suzuki K., Nakazono M., Nakanishi H., Mori S. & Nishizawa N.K. (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. Journal of Biological Chemistry 284, 3470-3479.
28. Ishimaru Y., Kim S., Tsukamoto T., etal. (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proceedings of the National Academy of Sciences of the United States of America 104, 7373-7378.
29. Kakei Y., Yamaguchi I., Kobayashi T., Takahashi M., Nakanishi H., Yamakawa T. & Nishizawa N.K. (2009) A highly sensitive, quick and simple quantification method for nicotianamine and 2′-deoxymugineic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants. Plant and Cell Physiology 50, 1988-1993.
30. Kakei Y., Ishimaru Y., Kobayshi T., Yamakawa T., Nakanishi H. & Nishizawa N.K. (2012) OsYSL16 plays a role in the allocation of iron. Plant Molecular Biology 79, 583-594.
31. Kamal K., Hagagg L. & Awad F. (2000) Improved Fe and Zn acquisition by guava seedlings grown in calcareous soils intercropped with graminaceous species. Journal of Plant Nutrition 23, 2071-2080.
32. Kawai S., Takagi S. & Sato Y. (1988) Mugineic acid-family phytosiderophores in root-secretions of barley, corn and sorghum varieties. Journal of Plant Nutrition 11, 633-642.
33. Kobayashi T., Suzuki M., Inoue H., Itai R.N., Takahashi M., Nakanishi H., Mori S. & Nishizawa N.K. (2005) Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. Journal of Experimental Botany 56, 1305-1316.
34. Kobayashi T., Nakanishi H. & Nishizawa N.K. (2010) Recent insights into iron homeostasis and their application in graminaceous crops. Proceedings of the Japan Academy 86, 900-913.
35. Lanfranchi S., Basso B. & Soave C. (2002) The yellow stripe 3 mutant of maize is defective in phytosiderophore secretion. Maydica 47, 181-184.
36. Le Jean M., Schikora A., Mari S., Briat J.F. & Curie C. (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. The Plant Journal 44, 769-782.
37. Lee S., Chiecko J.C., Kim S.A., Walker E.L., Lee Y., Guerinot M.L. & An G. (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiology 150, 786-800.
38. Luo M., Dang P., Bausher M.G., Holbrook C.C., Lee R.D., Lynch R.E. & Guo B.Z. (2005) Identification of transcripts involved in resistance responses to leaf spot disease caused by cercosporidium personatum in peanut (Arachis hypogaea). Phytopathology 95, 381-387.
39. Marschner H. & Römheld V. (1994) Strategies of plants for acquisition of iron. Plant and Soil 165, 261-274.
40. Marschner H., Römheld V. & Kissel M. (1986) Different strategies in higher plants in mobilization and uptake of iron. Journal of Plant Nutrition 9, 695-713.
41. Marschner H., Treeby M. & Römheld V. (1989) Role of root-induced changes in the rhizosphere for iron acquisition in higher-plants. Zeitschrift für Pflanzenernährung und Bodenkunde 152, 197-204.
42. Mori S. & Nishizawa N.K. (1987) Methionine as a dominant precursor of phytosiderophore in graminaceae plant. Plant and Cell Physiology 28, 1081-1092.
43. Murata Y., Ma J.F., Yamaji N., Ueno D., Nomoto K. & Iwashita T. (2006) A specific transporter for iron(III)-phytosiderophore in barley roots. The Plant Journal 46, 563-572.
44. Nozoye T., Nagasaka S., Kobayashi T., Takahashi M., Sato Y., Sato Y., Uozumi N., Nakanishi H. & Nishizawa N.K. (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry 286, 5446-5454.
45. Oldenburg K.R., Vo K.T., Michaelis S. & Paddon C. (1997) Recombination mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Research 25, 451-452.
46. Robinson N.J., Procter C.M., Connolly E.L. & Guerinot M.L. (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397, 694-697.
47. Römheld V. (1991) The role of phytosiderophores in acquisition of iron and othermicronutrients in graminaceous species: an ecological approach. Plant and Soil 130, 127-134.
48. III reduction, chelate splitting and release of phenolics. Plant Physiology 71, 949-954.
49. Römheld V. & Marschner H. (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiology 80, 175-180.
50. 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. Journal of Biological Chemistry 279, 9091-9096.
51. Schaaf G., Schikora A., Häberle J., Vert G., Ludewig U., Briat J.F., Curie C. & von Wirén N. (2005) A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant and Cell Physiology 46, 762-774.
52. Shojima S., Nishizawa N.K. & Mori S. (1989) Establishment of cell-free system for the biosynthesis of nicotianamine. Plant and Cell Physiology 30, 673-677.
53. Shojima S., Nishizawa N.K., Fushiya S., Nozoe S., Irifune T. & Mori S. (1990) Biosynthesis of phytosiderophores. Plant Physiology 93, 1497-1503.
54. Suzuki M., Takahashi M., Tsukamoto T., etal. (2006) Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. The Plant Journal 48, 85-97.
55. Takagi S. (1976) Naturally occurring iron-chelating compounds in oat- and rice-root washing. I. Activity measurement and preliminary characterization. Soil Science and Plant Nutrition 22, 423-433.
56. Takagi S., Kamei S. & Yu M.H. (1988) Efficiency of iron extraction from soil by mugineic acid family phytosiderophores. Journal of Plant Nutrition 11, 643-651.
57. Takahashi H., Kamakura H., Sato Y., Shiono K., Abiko T., Tsutsumi N., Nagamura Y., Nishizawa N. & Nakazono M. (2010) A method for obtaining high quality RNA from paraffin sections of plant tissues by laser microdissection. Journal of Plant Research 123, 807-813.
58. Takahashi M., Yamaguchi H., Nakanishi H., Shioiri T., Nishizawa N.K. & Mori S. (1999) Cloning Two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiology 121, 947-956.
59. 2+ estimation to resolve iron chlorosis in plants. Journal of Plant Nutrition 7, 81-90.
60. Treeby M., Marschner H. & Römheld V. (1989) Mobilization of iron and other micronutrient cations from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant and Soil 114, 217-226.
61. Vansuyt G., Robin A., Briat J.F., Curie C. & Lemanceau P. (2007) Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Molecular Plant-Microbe Interactions 20, 441-447.
62. Varotto C., Maiwald D., Pesaresi P., Jahns P., Salamini F. & Leister D. (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. The Plant Journal 31, 589-599.
63. Vert G., Grotz N., Dédaldéchamp F., Gaymard F., Guerinot M.L., Briat J.F. & Curie C. (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell 14, 1223-1233.
64. Von Wirén N., Mori S., Marschner H. & Römheld V. (1994) Iron inefficiency in maize mutant ys1 (Zea mays L. cv yellow-stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiology 106, 71-77.
65. Wada Y., Yamaguchi I., Takahashi M., Nakanishi H., Mori S. & Nishizawa N.K. (2007) Highly sensitive quantitative analysis of nicotianamine using LC/ESI-TOF-MS with an internal standard. Bioscience Biotechnology and Biochemistry 71, 435-441.
66. Waters B.M., Chu H.H., Didonato R.J., Roberts L.A., Eisley R.B., Lahner B., Salt D.E. & Walker E.L. (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 Physiology 141, 1446-1458.
67. Weber G., von Wirén N. & Hayen H. (2008) Investigation of ascorbate-mediated iron release from ferric phytosiderophores in the presence of nicotianamine. Biometals 21, 503-513.
68. Yuan Y., Wu H., Wang N., Li J., Zhao W., Du J., Wang D. & Ling H.Q. (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Research 18, 385-397.
69. Zuo Y. & Zhang F. (2008) Effect of peanut mixed cropping with gramineous species on micronutrient concentrations and iron chlorosis of peanut plants grown in a calcareous soil. Plant and Soil 306, 23-36.
70. Zuo Y. & Zhang F. (2009) Iron and zinc biofortification strategies in dicot plants by intercropping with gramineous species. A review. Agronomy for Sustainable Development 29, 63-71.
71. Zuo Y., Zhang F., Li X. & Cao Y. (2000) Studies on the improvement in iron nutrition of peanut by intercropping with maize on a calcareous soil. Plant and Soil 220, 13-25.
72. Zuo Y., Li X., Cao Y., Zhang F. & Christie P. (2003) Iron nutrition of peanut enhanced by mixed cropping with maize: possible role of root morphology and rhizosphere microflora. Journal of Plant Nutrition 26, 2093-2110.