The genetic basis of natural variation for iron homeostasis in the maize IBM population

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Benke, Andreas ^a   Urbany, Claude ^a   Marsian, Johanna ^a   Shi, Rongli ^b   Wirén, Nicolaus V ^b   Stich, Benjamin ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ZEA MAYS;

IRON; VEGETABLE PROTEIN;

ARTICLE; GENETICS; MAIZE; METABOLISM; PLANT LEAF; QUANTITATIVE TRAIT LOCUS;

IRON; PLANT LEAVES; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI; ZEA MAYS;

EID: 84892162754     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-12     Document Type: Article

References (62)

1. Marschner H. Mineral Nutrition of Higher Plants (Second Edition) 1995, UK: Elsevier.
2. Hergert GW, Nordquist PT, Petersen JL, Skates BA. Fertilizer and crop management practices for improving maize yields on high pH soils. J Plant Nutr 1996, 19:1223-1233.
3. Nordquist PT, Hergert GW, Skates BA, Petersen JL. Genetic improvement of corn for tolerance to high pH soils. J Plant Nutr 1996, 19:1309-1317.
4. Hansen NC, Hopkins BG, Ellsworth JW, Jolley VD. Iron nutrition in field crops. Iron Nutrition in Plants and Rhizospheric Microorganisms 2006, 23-59. Netherlands: Springer, Barton LL, Abadia J.
5. Bashir K, Ishimaru Y, Nishizawa NK. Iron uptake and loading into rice grains. Rice 2010, 3:122-130.
6. Godsey CB, Schmidt JP, Schlegel AJ, Taylor RK, Thompson CR, Gehl RJ. Correcting iron deficiency in corn with seed row-applied iron sulfate. Agron J 2003, 95:160-166.
7. Kobayashi T, Nishizawa NK. Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 2012, 63:131-152. 10.1146/annurev-arplant-042811-105522, 22404471.
8. Römheld V, Marschner H. Mobilization of iron in the rhizosphere of different plant species. Advances in Plant Nutrition 1986, 155-204. New York: Praeger Scientific, Tinker B, Läuchli A.
9. Römheld V, Marschner H. Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores. Plant Soil 1990, 123:147-153.
10. Bernards ML, Von Jolley D, Stevens WB, Hergert GW. Phytosiderophore release from nodal, primary, and complete root systems in maize. Plant Soil 2002, 241:105-113.
11. Kobayashi T, Itai RN, Aung MS, Senoura T, Nakanishi H, Nishizawa NK. The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. Plant J 2012, 69:81-91. 10.1111/j.1365-313X.2011.04772.x, 21880076.
12. Higuchi K, Nakanishi H, Suzuki K, Nishizawa NK, Mori S. Presence of nicotianamine synthase isozymes and their homologues in the root of graminaceous plants. Soil Sci Plant Nutr 1999, 45:681-691.
13. Nagasaka S, Takahashi M, Nakanishi-Itai R, Bashir K, Nakanishi H, Mori S, Nishizawa N. Time course analysis of gene expression over 24 hours in Fe-deficient barley roots. Plant Mol Biol 2009, 69:621-631. 10.1007/s11103-008-9443-0, 19089316.
14. Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK. Identification and localisation of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol 2008, 66:193-203. 10.1007/s11103-007-9262-8, 18034312.
15. Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 2006, 281:32395-32402. 10.1074/jbc.M604133200, 16926158.
16. Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 2011, 286:5446-5454. 10.1074/jbc.M110.180026, 3037657, 21156806.
17. Giehl RF, Meda AR, von Wirén N. Moving up, down, and everywhere: signaling of micronutrients in plants. Curr Opin Plant Biol 2009, 12:320-327. 10.1016/j.pbi.2009.04.006, 19481496.
18. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL. Maizeyellow stripe1 encodes a membrane protein directly involved in FeIII uptake. Nature 2001, 409:346-349. 10.1038/35053080, 11201743.
19. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 2004, 279:9091-9096. 10.1074/jbc.M311799200, 14699112.
20. Astolfi S, Zuchi S, Hubberten HM, Pinton R, Hoefgen R. Supply of sulphur to S-deficient young barley seedlings restores their capability to cope with iron shortage. J Exp Bot 2010, 61:799-806. 10.1093/jxb/erp346, 2814111, 20018904.
21. von Wirén N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC. Nicotianamine chelates both Fe(III) and Fe(II) implications for metal transport in plants. Plant Physiol 1999, 119:1107-1114. 10.1104/pp.119.3.1107, 32093, 10069850.
22. Kim SA, Punshon T, Lanzirotti A, Li A, Alonso JM, Ecker JR, Kaplan J, Guerinot ML. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 2006, 314:1295-1298. 10.1126/science.1132563, 17082420.
23. Lanquar V, Leliévre F, Bolte S, Hamés C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H, Thomine S. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO Journal 2005, 24:4041-4051. 10.1038/sj.emboj.7600864, 1356305, 16270029.
24. Kobayashi Y, Koyama H. QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol 2002, 43:1526-1533. 10.1093/pcp/pcf174, 12514250.
25. Salt DE, Baxter I, Lahner B. Ionomics and the study of the plant ionome. Annu Rev Plant Biol 2008, 59:709-733. 10.1146/annurev.arplant.59.032607.092942, 18251712.
26. Mitchell-Olds T, Pedersen D. The molecular basis of quantitative genetic variation in central and secondary metabolism in Arabidopsis. Genetics 1998, 149:739-747. 1460200, 9611188.
27. Zhang N, Gibon Y, Gur A, Chen C, Lepak N, Höhne M, Zhang Z, Kroon D, Tschoep H, Stitt M, Buckler E. Fine quantitative trait loci mapping of carbon and nitrogen metabolism enzyme activities and seedling biomass in the maize IBM mapping population. Plant Physiol 2010, 154(4):1753-1765. 10.1104/pp.110.165787, 2996021, 20971858.
28. Thoiron S, Pascal N, Briat JF. Impact of iron deficiency and iron re-supply during the early stages of vegetative development in maize (Zea mays L.). Plant Cell Environ 1997, 20:1051-1060.
29. Lung'aho MG, Mwaniki AM, Szalma SJ, Hart JJ, Rutzke MA, Kochian LV, Glahn RP, Hoekenga OA. Genetic and physiological analysis of iron biofortification in Maize Kernels. PLoS ONE 2011, 6:e20429. 10.1371/journal.pone.0020429, 3110754, 21687662.
30. Xue D, Chen M, Zhang G. Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 2009, 165:587-596.
31. Römheld V. The chlorosis paradox: Fe inactivation as a secondary event in chlorotic leaves of grapevine. J Plant Nutr 2000, 23:1629-1643.
32. Duy D, Stübe R, Wanner G, Philippar K. The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 2011, 155:1709-1722. 10.1104/pp.110.170233, 3091129, 21343424.
33. Briat JF, Lobréaux S, Grignon N, Vansuyt G. Regulation of plant ferritin synthesis: How and why. Cell Mol Life Sci 1999, 56:155-166. 10.1007/s000180050014, 11213255.
34. Zhang C, Römheld V, Marschner H. Retranslocation of iron from primary leaves of bean plants grown under iron deficiency. J Plant Physiol 1995, 146:268-272.
35. Tognetti VB, Zurbriggen MD, Morandi EN, Fillat MF, Valle EM, Hajirezaei MR, Carrillo N. Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin. Proc Natl Acad Sci USA 2007, 104:11495-11500. 10.1073/pnas.0704553104, 2040926, 17592141.
36. Hase T, Kimata Y, Yonekura K, Matsumura T, Sakakibara H. Molecular cloning and differential expression of the maize ferredoxin gene family. Plant Physiol 1991, 96:77-83. 10.1104/pp.96.1.77, 1080715, 16668188.
37. Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS. Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 2009, 284:25867-25878. 10.1074/jbc.M109.023622, 2757988, 19586916.
38. von Wirén N, Mori S, Marschner H, Römheld V. Iron inefficiency in maize mutant ys1 (Zea mays L. cv Yellow Stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol 1994, 106:71-77. 159500, 12232304.
39. Meda AR, Scheuermann EB, Prechsl UE, Erenoglu B, Schaaf G, Hayen H, Weber G, von Wirén N. Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiol 2007, 143:1761-1773. 10.1104/pp.106.094474, 1851820, 17337530.
40. Hanikenne M, Krämer U, Demoulin V, Baurain D. A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol 2005, 137:428-446. 10.1104/pp.104.054189, 1065346, 15710683.
41. Talke IN, Hanikenne M, Krämer U. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 2006, 142:148-167. 10.1104/pp.105.076232, 1557598, 16844841.
42. Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK. Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiol 2003, 132:1989-1997. 10.1104/pp.102.019869, 181284, 12913155.
43. Ling HQ, Koch G, Bäumlein H, Ganal MW. Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 1999, 96:7098-7103. 10.1073/pnas.96.12.7098, 22069, 10359845.
44. Marschner H, Römheld V, Cakmak I. Root-induced changes of nutrient availability in the rhizosphere. Plant Nutr 1987, 10:1175-1184.
45. Yehuda Z, Shenker M, Römheld V, Marschner H, Hadar Y, Chen Y. The role of ligand exchange in the uptake of iron from microbial siderophores by gramineous plants. Plant Physiol 1996, 112:1273-1280. 158055, 12226445.
46. Kobayashi T, Itai RN, Ogo Y, Kakei Y, Nakanishi H, Takahashi M, Nishizawa NK. The rice transcription factor IDEF1 is essential for the early response to iron deficiency, and induces vegetative expression of late embryogenesis abundant genes. Plant J 2009, 60:948-961. 10.1111/j.1365-313X.2009.04015.x, 19737364.
47. Lee M, Sharopova N, Beavis WD, Grant D, Katt M, Blair D, Hallauer A. Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population. Plant Mol Biol 2002, 48:453-461. 10.1023/A:1014893521186, 11999829.
48. von Wirén N, Marschner H, Römheld V. Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiol 1996, 111:1119-1125. 160987, 12226351.
49. Shi R, Weber G, Köster J, Reza-Hajirezaei M, Zou C, Zhang F, von Wirén N. Senescence-induced iron mobilization in source leaves of barley (Hordeum vulgare) plants. New Phytol 2012, 195:372-383. 10.1111/j.1469-8137.2012.04165.x, 22591276.
50. Gilmour AR, Gogel BJ, Cullis BR, Thompson R. ASReml User Guide Release 2.0 2006, Hemel Hempstead: VSN International Ltd.
51. Chakravarti IM, Laha RG, Roy J. Handbook of Methods of Applied Statistics,. Volume I 1967, New York, London, and Sydney: John Wiley and Sons.
52. Whittaker J. Graphical Models in Applied Multivariate Statistics 1990, Chichester: John Wiley.
53. Butts CT. Network: a package for managing relational data in R. J Stat Softw 2007, 24:1-36.
54. Dufour P, Johnsson C, Antoine-Michard S, Cheng R, Murigneux A, Beckert M. Segregation distortion at marker loci: variation during microspore embryogenesis in maize. Theor Appl Genet 2001, 102:993-1001.
55. Sen S, Churchill GA. A statistical framework for quantitative trait mapping. Genetics 2001, 159:371-387. 1461799, 11560912.
56. Schwarz G. Estimating the dimension of a model. Ann Stat 1978, 6:461-464.
57. Jansen RC. A general Monte Carlo method for mapping multiple quantitative trait loci. Genetics 1996, 142:305-311. 1206959, 8770607.
58. Broman KW, Sen S. A Guide to QTL Mapping with R/qtl. Statistics for Biology and Health 2009, New York: Springer.
59. Carson ML, Stuber CW, Senior ML. Quantitative trait loci conditioning resistance to phaeosphaeria leaf spot of maize caused by Phaeosphaeria maydis. Plant Dis 2005, 89:571-574.
60. Churchill GA, Doerge RW. Empirical threshold values for quantitative trait mapping. Genetics 1994, 138:963-971. 1206241, 7851788.
61. Sen S. Confidence intervals for gene location - The effect of model misspecification and smoothing. PhD thesis, Department of Statistics, University of Chicago 1998.
62. R Core Team R: A Language and Environment for Statistical Computing 2012, Vienna: R Foundation for Statistical Computing, R Core Team.