The role of transition metal homeostasis in plant seed development

Current Opinion in Plant Biology

Volumn 14, Issue 3, 2011, Pages 318-324

  Walker, Elsbeth L ^a   Waters, Brian M ^b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZETIDINE 2 CARBOXYLIC ACID; CARRIER PROTEIN; DRUG DERIVATIVE; IRON; METAL; NICOTIANAMINE; TRANSITION ELEMENT; VEGETABLE PROTEIN; ZINC;

GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HUMAN; METABOLISM; PLANT; PLANT SEED; REPRODUCTION; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

AZETIDINECARBOXYLIC ACID; BIOLOGICAL TRANSPORT; HOMEOSTASIS; HUMANS; IRON; MEMBRANE TRANSPORT PROTEINS; METALS; PLANT PROTEINS; PLANTS; REPRODUCTION; SEEDS; TRANSITION ELEMENTS; ZINC;

EID: 79957686123     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2011.03.025     Document Type: Review

References (65)

1. Yu H.J., Hogan P., Sundaresan V. Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol 2005, 139:1853-1869.
2. Steffen J.G., Kang I.H., Macfarlane J., Drews G.N. Identification of genes expressed in the Arabidopsis female gametophyte. Plant J 2007, 51:281-292.
3. Kerim T., Imin N., Weinman J.J., Rolfe B.G. Proteome analysis of male gametophyte development in rice anthers. Proteomics 2003, 3:738-751.
4. Noir S., Brautigam A., Colby T., Schmidt J., Panstruga R. A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem Biophys Res Commun 2005, 337:1257-1266.
5. Sheoran I., Sproule K., Olson D., Ross A., Sawhney V. Proteome profile and functional classification of proteins in Arabidopsis thaliana (Landsberg erecta) mature pollen. Sex Plant Reprod 2006, 19:185-196.
6. Johnston A.J., Meier P., Gheyselinck J., Wuest S.E., Federer M., Schlagenhauf E., Becker J.D., Grossniklaus U. Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol 2007, 8:R204.
7. Agrawal G.K., Hajduch M., Graham K., Thelen J.J. In-depth investigation of the soybean seed-filling proteome and comparison with a parallel study of rapeseed. Plant Physiol 2008, 148:504-518.
8. Hajduch M., Hearne L.B., Miernyk J.A., Casteel J.E., Joshi T., Agrawal G.K., Song Z., Zhou M., Xu D., Thelen J.J. Systems analysis of seed filling in Arabidopsis: using general linear modeling to assess concordance of transcript and protein expression. Plant Physiol 2010, 152:2078-2087.
9. Ravet K., Touraine B., Boucherez J., Briat J., Gaymard F., Cellier F. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 2009, 57:400-412.
10. Waters B.M., Chu H.H., Didonato R.J., Roberts L.A., Eisley R.B., Lahner B., Salt D.E., Walker E.L. 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 Physiol 2006, 141:1446-1458.
11. Stacey M.G., Koh S., Becker J., Stacey G. AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. Plant Cell 2002, 14:2799-2811.
12. Stacey M.G., Patel A., McClain W.E., Mathieu M., Remley M., Rogers E.E., Gassmann W., Blevins D.G., Stacey G. The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 2008, 146:589-601.
13. Hussain D., Haydon M.J., Wang Y., Wong E., Sherson S.M., Young J., Camakaris J., Harper J.F., Cobbett C.S. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 2004, 16:1327-1339.
14. Barneix A.J. Physiology and biochemistry of source-regulated protein accumulation in the wheat grain. J Plant Physiol 2007, 164:581-590.
15. Hopkins M., Taylor C., Liu Z., Ma F., McNamara L., Wang T.W., Thompson J.E. Regulation and execution of molecular disassembly and catabolism during senescence. New Phytol 2007, 175:201-214.
16. Himelblau E., Amasino R.M. Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 2001, 158:1317-1323.
17. Joppa L.R., Du C.H., Hart G.E., Hareland G.A. Mapping gene(s) for grain protein in tetraploid wheat (Triticum turgidum L.) using a population of recombinant inbred chromosome lines. Crop Sci 1997, 37:1586-1589.
18. Olmos S., Distelfeld A., Chicaiza O., Schlatter A.R., Fahima T., Echenique V., Dubcovsky J. Precise mapping of a locus affecting grain protein content in durum wheat. Theor Appl Genet 2003, 107:1243-1251.
19. Uauy C., Distelfeld A., Fahima T., Blechl A., Dubcovsky J. A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 2006, 314:1298-1301.
20. Cakmak I., Torun A., Millet E., Feldman M., Fahima T., Korol A., Nevo E., Braun H.J., Ozkan H. Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Sci Plant Nutr 2004, 50:1047-1054.
21. Distelfeld A., Cakmak I., Peleg Z., Ozturk L., Yazici A.M., Budak H., Saranga Y., Fahima T. Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiol Plant 2007, 129:635-643.
22. Uauy C., Brevis J.C., Dubcovsky J. The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 2006, 57:2785-2794.
23. Waters B.M., Uauy C., Dubcovsky J., Grusak M.A. Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J Exp Bot 2009, 60:4263-4274.
24. Stephan U.W., Grun M. Physiological disorders of the nicotianamine-auxothroph tomato mutant chloronerva at different levels of iron nutrition. II. Iron deficiency response and heavy metal metabolism. Biochem Physiol Pflanzen 1989, 185:189-200.
25. Pich A., Scholz G. Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J Exp Bot 1996, 47:41-47.
26. Schmidke I., Stephan U.W. Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings. Physiol Plant 1995, 95:147-153.
27. Rellan-Alvarez R., Abadia J., Alvarez-Fernandez A. Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 2008, 22:1553-1562.
28. Ling H.Q., Koch G., Baumlein H., Ganal M.W. 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.
29. Herbik A., Koch G., Mock H.P., Dushkov D., Czihal A., Thielmann J., Stephan U.W., Baumlein H. Isolation, characterization and cDNA cloning of nicotianamine synthase from barley. A key enzyme for iron homeostasis in plants. Eur J Biochem 1999, 265:231-239.
30. Higuchi K., Suzuki K., Nakanishi H., Yamaguchi H., Nishizawa N.K., Mori S. Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 1999, 119:471-480.
31. Scholz G., Becker R., Pich A., Stephan U.W. Nicotianamine-a common constitutent of strategies I and II of iron acquisition by plants: a review. J Plant Nutr 1992, 15:1647-1665.
32. Stephan U.W., Schmidke I., Stephan V.W., Scholz G. The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 1996, 9:84-90.
33. Scholz G., Schlesier G., Seifert K. Effect of nicotianamine on iron uptake by the tomato mutant 'chloronerva'. Physiol Plant 1985, 63:99-104.
34. Pich A., Scholz G., Stephan U.W. Iron-dependent changes of heavy metals, nicotianamine, and citrate in different plant organs and in the xylem exudate of two tomato genotypes. Nicotianamine as possible copper translocator. Plant Soil 1994, 165:189-196.
35. Klatte M., Schuler M., Wirtz M., Fink-Straube C., Hell R., Bauer P. The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 2009, 150:257-271.
36. Anderegg G., Ripperger H. Correlation between metal complex formation and biological activity of nicotianamine analogues. J Chem Soc Chem Commun 1989, 10:647-650.
37. von Wiren N., Klair S., Bansal S., Briat J.-F., Khodr H., Shioiri T., Leigh R.A., Hider R.C. Nicotianamine chelates both Fe[III] and Fe[II]. Implications for metal transport in plants. Plant Physiol 1999, 119:1107-1114.
38. Lee S., Jeon U.S., Lee S.J., Kim Y.K., Persson D.P., Husted S., Schjorring J.K., Kakei Y., Masuda H., Nishizawa N.K., et al. Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 2009, 106:22014-22019.
39. Higuchi K., Tani M., Nakanishi H., Yoshiwara T., Goto F., Nishizawa N.K., Mori S. The expression of a barley HvNAS1 nicotianamine synthase gene promoter-gus fusion gene in transgenic tobacco is induced by Fe-deficiency in roots. Biosci Biotechnol Biochem 2001, 65:1692-1696.
40. Masuda H., Usuda K., Kobayashi T., Ishimaru Y., Kakei Y., Takahashi M., Higuchi K., Nakanishi H., Mori S., Nishizawa N.K. Overexpression of the barley Nicotianamine Synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2009, 2:155-166.
41. Waters B.M., Grusak M.A. Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol 2008, 177:389-405.
42. Chu H.H., Chiecko J., Punshon T., Lanzirotti A., Lahner B., Salt D.E., Walker E.L. Successful reproduction requires the function of Arabidopsis YELLOW STRIPE-LIKE1 and YELLOW STRIPE-LIKE3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol 2010, 154:197-210.
43. Koike S., Inoue H., Mizuno D., Takahashi M., Nakanishi H., Mori S., Nishizawa N.K. OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 2004, 39:415-424.
44. Ishimaru Y., Masuda H., Bashir K., Inoue H., Tsukamoto T., Takahashi M., Nakanishi H., Aoki N., Hirose T., Ohsugi R., et al. Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 2010, 62:379-390.
45. Long T.A., Tsukagoshi H., Busch W., Lahner B., Salt D.E., Benfey P.N. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 2010, 22:2219-2236.
46. Bogs J., Bourbouloux A., Cagnac O., Wachter A., Rausch T., Delrot S. Functional characterization and expression analysis of a glutathione transporter, BjGT1, from Brassica juncea: evidence for regulation by heavy metal exposure. Plant Cell Environ 2003, 26:1703-1711.
47. Pike S., Patel A., Stacey G., Gassmann W. Arabidopsis OPT6 is an oligopeptide transporter with exceptionally broad substrate specificity. Plant Cell Physiol 2009, 50:1923-1932.
48. Vasconcelos M.W., Li G.W., Lubkowitz M.A., Grusak M.A. Characterization of the PT clade of oligopeptide transporters in rice. Plant Gen 2008, 1:77-88.
49. Ozturk L., Yazici M.A., Yucel C., Torun A., Cekic C., Bagci A., Ozkan H., Braun H.J., Sayers Z., Cakmak I. Concentration and localization of zinc during seed development and germination in wheat. Physiol Plant 2006, 128:144-152.
50. Cakmak I., Kalayci M., Kaya Y., Torun A.A., Aydin N., Wang Y., Arisoy Z., Erdem H., Yazici A., Gokmen O., et al. Biofortification and localization of zinc in wheat grain. J Agric Food Chem 2010, 58:9092-9102.
51. Lombi E., Smith E., Hansen T.H., Paterson D., de Jonge M.D., Howard D.L., Persson D.P., Husted S., Ryan C., Schjoerring J.K. Megapixel imaging of (micro)nutrients in mature barley grains. J Exp Bot 2011, 62:273-282.
52. Wang Y.X., Specht A., Horst W.J. Stable isotope labelling and zinc distribution in grains studied by laser ablation ICP-MS in an ear culture system reveals zinc transport barriers during grain filling in wheat. New Phytol 2011, 189:428-437.
53. Kim S.A., Punshon T., Lanzirotti A., Li L., Alonso J.M., Ecker J.R., Kaplan J., Guerinot M.L. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 2006, 314:1295-1298.
54. Roschzttardtz H., Conejero G., Curie C., Mari S. Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol 2009, 151:1329-1338.
55. Lanquar V., Lelievre F., Bolte S., Hames C., Alcon C., Neumann D., Vansuyt G., Curie C., Schroder A., Kramer U., et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 2005, 24:4041-4051.
56. Ravet K., Touraine B., Kim S.A., Cellier F., Thomine S., Guerinot M.L., Briat J.F., Gaymard F. Post-translational regulation of AtFER2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Mol Plant 2009, 2:1095-1106.
57. Marentes E., Grusak M.A. Iron transport and storage within the seed coat and embryo of developing seeds of pea (Pisum sativum L.). Seed Sci Res 1998, 8:367-375.
58. Cvitanich C., Przybylowicz W.J., Urbanski D.F., Jurkiewicz A.M., Mesjasz-Przybylowicz J., Blair M.W., Astudillo C., Jensen E.O., Stougaard J. Iron and ferritin accumulate in separate cellular locations in Phaseolus seeds. BMC Plant Biol 2010, 10:14.
59. Lobreaux S., Briat J.F. Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J 1991, 274(Pt 2):601-606.
60. Stadler R., Lauterbach C., Sauer N. Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 2005, 139:701-712.
61. Thorne J.H. Phloem unloading of C-assimilates and N-assimilates in developing seeds. Annu Rev Plant Physiol Plant Mol Biol 1985, 36:317-343.
62. Zhang W.H., Zhou Y.C., Dibley K.E., Tyerman S.D., Furbank R.T., Patrick J.W. Nutrient loading of developing seeds. Funct Plant Biol 2007, 34:314-331.
63. Tauris B., Borg S., Gregersen P.L., Holm P.B. A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J Exp Bot 2009, 60:1333-1347.
64. Hill J. The remobilization of nutrients from leaves. J Plant Nutr 1980, 2:407-444.
65. Grusak M.A. Iron transport to developing ovules of pisum sativum (I. Seed import characteristics and phloem iron-loading capacity of source regions). Plant Physiol 1994, 104:649-655.