The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains
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Rice OsYSL9 is a novel transporter for Fe(II)-nicotianamine and Fe(III)-deoxymugineic acid that is responsible for internal iron transport, especially from endosperm to embryo in developing seeds.
Metal chelators are essential for safe and efficient metal translocation in plants. Graminaceous plants utilize specific ferric iron chelators, mugineic acid family phytosiderophores, to take up sparingly soluble iron from the soil. Yellow Stripe 1-Like (YSL) family transporters are responsible for transport of metal-phytosiderophores and structurally similar metal-nicotianamine complexes. Among the rice YSL family members (OsYSL) whose functions have not yet been clarified, OsYSL9 belongs to an uncharacterized subgroup containing highly conserved homologs in graminaceous species. In the present report, we showed that OsYSL9 localizes mainly to the plasma membrane and transports both iron(II)-nicotianamine and iron(III)-deoxymugineic acid into the cell. Expression of OsYSL9 was induced in the roots but repressed in the nonjuvenile leaves in response to iron deficiency. In iron-deficient roots, OsYSL9 was induced in the vascular cylinder but not in epidermal cells. Although OsYSL9-knockdown plants did not show a growth defect under iron-sufficient conditions, these plants were more sensitive to iron deficiency in the nonjuvenile stage compared with non-transgenic plants. At the grain-filling stage, OsYSL9 expression was strongly and transiently induced in the scutellum of the embryo and in endosperm cells surrounding the embryo. The iron concentration was decreased in embryos of OsYSL9-knockdown plants but was increased in residual parts of brown seeds. These results suggested that OsYSL9 is involved in iron translocation within plant parts and particularly iron translocation from endosperm to embryo in developing seeds.
KeywordsIron Metal homeostasis Mugineic acid family phytosiderophores Nicotianamine Rice (Oryza sativa L.) Yellow Stripe 1-Like (YSL) transporter
We thank Dr. Nicolaus von Wirén (Leibniz Institute of Plant Genetics and Crop Plant Research) for kindly providing plasmids pDR195 and pDR196-ZmYS1, Dr. David J. Eide (Department of Nutritional Sciences, University of Wisconsin-Madison) for kindly providing yeast strain fet3fet4, Dr. Hiroyuki Watanabe (Hasegawa Kouryou) for kindly providing chemically synthesized NA, and Dr. Kosuke Namba (Tokushima University) for kindly providing chemically synthesized DMA. We also thank Ms. Hiroko Hori (Ishikawa Prefectural University) for assistance with the rice culture and analysis. This research was supported by the Japan Science and Technology Agency program ALCA (to N.K.N.), and JSPS KAKENHI Grant Number 16H04891 (to N.K.N.).
NKN and HN designed the research. TS, ES and TK performed the experiments with assistance from MT, MSA and HM. TS and ES analyzed the data. TS and TK wrote the paper.
- Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2009) OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol 70:681–692CrossRefPubMedPubMedCentralGoogle Scholar
- Chu HH, Chiecko J, Punshon T, Lanzirotti A, Lahner B, Salt DE, Walker EL (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 Physiol 154:197–210CrossRefPubMedPubMedCentralGoogle Scholar
- Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK (2008) Identification and localisation of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol 66:193–203Google Scholar
- Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (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. J Biol Chem 284:3470–3479CrossRefPubMedGoogle Scholar
- Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic press, LondonGoogle Scholar
- Matsuo T, Hoshikawa K (1993) Science of the rice plant. vol 1, morphology. Food and Agriculture Policy Research Center, TokyoGoogle Scholar
- Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol 28:1081–1092Google Scholar
- Waters BM, Chu HH, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (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 Physiol 141:1446–1458CrossRefPubMedPubMedCentralGoogle Scholar
- World Health Organization (WHO) (2002) World health report reducing risks, promoting healthy life. WHO, GenevaGoogle Scholar
- Yordem BK, Conte SS, Ma JF, Yokosho K, Vasques KA, Gopalsamy SN, Walker EL (2011) Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of Yellow Stripe-Like (YSL) transporters. Ann Bot 108:821–833CrossRefPubMedPubMedCentralGoogle Scholar