title: OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds.
abstract: Plants and seeds are the main dietary sources of zinc, iron, manganese, and copper, but are also the main entry point for toxic elements such as cadmium into the food chain. We report here that an Arabidopsis oligopeptide transporter mutant, opt3-2, over-accumulates cadmium (Cd) in seeds and roots but, unexpectedly, under-accumulates Cd in leaves. The cadmium distribution in opt3-2 differs from iron, zinc, and manganese, suggesting a metal-specific mechanism for metal partitioning within the plant. The opt3-2 mutant constitutively up-regulates the Fe/Zn/Cd transporter IRT1 and FRO2 in roots, indicative of an iron-deficiency response. No genetic mutants that impair the shoot-to-root signaling of iron status in leaves have been identified. Interestingly, shoot-specific expression of OPT3 rescues the Cd sensitivity and complements the aberrant expression of IRT1 in opt3-2 roots, suggesting that OPT3 is required to relay the iron status from leaves to roots. OPT3 expression was found in the vasculature with preferential expression in the phloem at the plasma membrane. Using radioisotope experiments, we found that mobilization of Fe from leaves is severely affected in opt3-2, suggesting that Fe mobilization out of leaves is required for proper trace-metal homeostasis. When expressed in yeast, OPT3 does not localize to the plasma membrane, precluding the identification of the OPT3 substrate. Our in planta results show that OPT3 is important for leaf phloem-loading of iron and plays a key role regulating Fe, Zn, and Cd distribution within the plant. Furthermore, ferric chelate reductase activity analyses provide evidence that iron is not the sole signal transferred from leaves to roots in leaf iron status signaling.
authors.affiliation: Division of Biological Sciences, Cell and Developmental Biology Section and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093, USA; Division of Plant Sciences, C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA. Electronic address: mendozacozatld@missouri.edu.
authors.forename: David G
authors.initials: DG
authors.lastname: Mendoza-Cózatl
authors.affiliation: Division of Biological Sciences, Cell and Developmental Biology Section and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093, USA; Department of Chemistry, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, Fujian, 361005, China.
authors.forename: Qingqing
authors.initials: Q
authors.lastname: Xie
authors.affiliation: Division of Biological Sciences, Cell and Developmental Biology Section and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093, USA.
authors.forename: Garo Z
authors.initials: GZ
authors.lastname: Akmakjian
authors.affiliation: Division of Biological Sciences, Cell and Developmental Biology Section and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093, USA.
authors.forename: Timothy O
authors.initials: TO
authors.lastname: Jobe
authors.affiliation: Division of Plant Sciences, C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA; Present address: Laboratory for Infectious Disease Research, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Ami
authors.initials: A
authors.lastname: Patel
authors.affiliation: Division of Plant Sciences, C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Minviluz G
authors.initials: MG
authors.lastname: Stacey
authors.affiliation: Department of Chemistry, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Lihui
authors.initials: L
authors.lastname: Song
authors.affiliation: Department of Chemistry, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Dustin Wayne
authors.initials: DW
authors.lastname: Demoin
authors.affiliation: Department of Chemistry, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Silvia S
authors.initials: SS
authors.lastname: Jurisson
authors.affiliation: Division of Plant Sciences, C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA; Department of Biochemistry, C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Gary
authors.initials: G
authors.lastname: Stacey
authors.affiliation: Division of Biological Sciences, Cell and Developmental Biology Section and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093, USA. Electronic address: jischroeder@ucsd.edu.
authors.forename: Julian I
authors.initials: JI
authors.lastname: Schroeder
mesh_terms: D017360:Arabidopsis / Q000166:cytology* / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002104:Cadmium / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D007501:Iron / Q000378:metabolism*; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism*; D009928:Organ Specificity; D052585:Phloem / Q000378:metabolism; D018515:Plant Leaves / Q000378:metabolism; D018517:Plant Roots / Q000378:metabolism; D012639:Seeds / Q000378:metabolism; D015398:Signal Transduction
chemical_list: D029681:Arabidopsis Proteins; D026901:Membrane Transport Proteins; C509148:OPT3 protein, Arabidopsis; D002104:Cadmium; D007501:Iron
keywords: ionomics.; iron deficiency; metal homeostasis; phloem transport; seed loading