The Chloroplast Permease PIC1 Regulates Plant Growth and Development by Directing Homeostasis and Transport of Iron  

Abstract

The membrane-spanning protein PIC1 (for permease in chloroplasts 1) in Arabidopsis (Arabidopsis thaliana) was previously described to mediate iron transport across the inner envelope membrane of chloroplasts. The albino phenotype of pic1 knockout mutants was reminiscent of iron-deficiency symptoms and characterized by severely impaired plastid development and plant growth. In addition, plants lacking PIC1 showed a striking increase in chloroplast ferritin clusters, which function in protection from oxidative stress by sequestering highly reactive free iron in their spherical protein shell. In contrast, PIC1-overexpressing lines (PIC1ox) in this study rather resembled ferritin loss-of-function plants. PIC1ox plants suffered from oxidative stress and leaf chlorosis, most likely originating from iron overload in chloroplasts. Later during growth, plants were characterized by reduced biomass as well as severely defective flower and seed development. As a result of PIC1 protein increase in the inner envelope membrane of plastids, flower tissue showed elevated levels of iron, while the content of other transition metals (copper, zinc, manganese) remained unchanged. Seeds, however, specifically revealed iron deficiency, suggesting that PIC1 overexpression sequestered iron in flower plastids, thereby becoming unavailable for seed iron loading. In addition, expression of genes associated with metal transport and homeostasis as well as photosynthesis was deregulated in PIC1ox plants. Thus, PIC1 function in plastid iron transport is closely linked to ferritin and plastid iron homeostasis. In consequence, PIC1 is crucial for balancing plant iron metabolism in general, thereby regulating plant growth and in particular fruit development.

The Arabidopsis YELLOW STRIPE LIKE4 and 6 Transporters Control Iron Release from the Chloroplast

“…Until now, the molecular mechanisms by which iron is transported into and out of the chloroplast remained elusive. Candidates for Fe import into the chloroplast include the permease PIC1, which might translocate proteins that are required for iron transport in the chloroplast (Duy et al, 2007(Duy et al, , 2011, the transporter MAR1/IREG3, which might transport an iron chelate or its ligand alone (Conte et al, 2009), or the ABC NAP14, which could be part of an iron transport complex (Shimoni-Shor et al, 2010). Our data provide strong evidence that the YSL4 and YSL6 transporters contribute to the export of iron from the chloroplast.…”

“…However, there is no evidence from direct measurement of chloroplastic Fe uptake to support a role for PIC in Fe uptake in the chloroplast. PIC1 was reported to interact with a member of the Ni 2+ -Co 2+ transporters family, referred to as NiCo, which together with PIC1, is hypothesized to act as a complex to import Fe into the chloroplast (Duy et al, 2011). Unlike FRO7, whose expression is limited to young green tissues, PIC1 expression is ubiquitous, indicating that these two genes do not participate in the same pathway of Fe entry.…”

Tobacco PIC1 Mediates Iron Transport and Regulates Chloroplast Development

“…All of these phenotypes are consistent with a defect in iron transport (Duy et al 2007). AtPIC1 overexpression causes oxidative stress and leaf chlorosis, which are likely caused by excessive iron accumulation in chloroplasts (Duy et al 2011). …”

A rapid and efficient method to study the function of crop plant transporters in Arabidopsis

“…For example, the natural resistance-associated macrophage proteins (NRAMP) family of proteins has been suggested to localize to plasma membrane or vacuolar membrane and contribute to iron uptake from soil and translocation from the root to shoot (Ishimaru et al 2012;Lanquar et al 2005). At the cellular level, iron transporters have also been identified to transport Fe into different organelles for functioning or storage, like the mitochondrial iron transporter MIT1 and the permease PIC1 in chloroplasts (Bashir et al 2011a;Bashir et al 2011b;Duy et al 2011;Duy et al 2007). The vacuole, serving as the major storage organelle inside the cell, has its own iron transporter: VIT1, which is conserved in multiple organisms (Kim et al 2006;Li et al 2001;Momonoi et al 2009;Zhang et al 2012).…”