OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice

Abstract

Background Metal homeostasis is critical for plant growth, development and adaptation to environmental stresses and largely governed by a variety of metal transporters. The plant ZIP ( Z n-regulated transporter, I ron-regulated transporter-like P rotein) family proteins belong to the integral membrane transporters responsible for uptake and allocation of essential and non-essential metals. However, whether the ZIP family members mediate metal efflux and its regulatory mechanism remains unknown. Results In this report, we provided evidence that OsZIP1 is a metal-detoxified transporter through preventing excess Zn, Cu and Cd accumulation in rice. OsZIP1 is abundantly expressed in roots throughout the life span and sufficiently induced by excess Zn, Cu and Cd but not by Mn and Fe at transcriptional and translational levels. Expression of OsZIP-GFP fusion in rice protoplasts and tobacco leaves shows that OsZIP1 resides in the endoplasmic reticulum (ER) and plasma membrane (PM). The yeast ( Saccharomyces cerevisiae ) complementation test shows that expression of OsZIP1 reduced Zn accumulation. Transgenic rice overexpressing OsZIP1 grew better under excess metal stress but accumulated less of the metals in plants. In contrast, both oszip1 mutant and RNA interference (RNAi) lines accumulated more metal in roots and contributed to metal sensitive phenotypes. These results suggest OsZIP1 is able to function as a metal exporter in rice when Zn, Cu and Cd are excess in environment. We further identified the DNA methylation of histone H3K9me2 of OsZIP1 and found that OsZIP1 locus, whose transcribed regions imbed a 242 bp sequence, is demethylated, suggesting that epigenetic modification is likely associated with OsZIP1 function under Cd stress. Conclusion OsZIP1 is a transporter that is required for detoxification of excess Zn, Cu and Cd in rice. Electronic supplementary material The online version of this article (10.1186/s12870-019-1899-3) contains supplementary material, which is available to authorized users.

A high activity zinc transporter OsZIP9 mediates zinc uptake in rice

“…A branch consisting of OsZIP1 and OsZIP9 showed more specific expression in the roots. As OsZIP1 was recently shown to function as a metal efflux transporter preventing excess Zn, Cu and Cd accumulation, rather than as a Zn uptake transporter (Liu et al, 2019), we focused on the as yet uncharacterized OsZIP9 for further investigation.…”

“…Conversely, the molecular mechanism of Zn uptake was less understood. OsZIP1 had long been considered to account for the Zn uptake, but recently it was demonstrated to be responsible for the detoxification of excess Zn in roots, rather than for the uptake of Zn (Ramesh et al, 2003;Liu et al, 2019).…”

Endomembrane Reorganization Induced by Heavy Metals

“…Interestingly, Fe transporters such as IRT1 and IRT2 are able to take up Cd in both Oryza sativa and A. thaliana [32]. Other ZIP transporters may be responsible for metal distribution into cellular compartments, as AtIRT2, which is located in endo-membranes vesicles contributing to Fe transport into these compartments [33,34] and OsZIP1, showing a dual location on the plasma membrane and on the endoplasmic reticulum upon normal growth conditions and limiting Zn, Cu, and Cd accumulation in rice tissues [35].…”

Transcriptomic expression patterns of two contrasting lowland rice varieties reveal high iron stress tolerance

“…NRAMP4 is an aluminum uptake transporter (Xia, Yamaji, Kasai, & Ma, 2010). Metal transporter ZIP2 has not been functionally characterized itself, but its homolog ZIP1 has been shown to transport different metal ions (Ramesh, Shin, Eide, & Schachtman, 2003) and has later been found to act as a plasma membrane and ER-located Zn, Cu and Cd efflux transporter (Liu et al, 2019). Although ZIP1 probably does not transport Fe (Liu et al, 2019), higher expression of ZIP1 and ZIP2 in the tolerant versus the sensitive line under excess Fe suggests that they might contribute to the tolerance mechanism.…”