ZIP10 governs Zn influx into the cytoplasm from the endoplasmic reticulum and maintains Zn homeostasis in rice

Zn is an essential micronutrient for all organisms. Understanding how Zn homeostasis is controlled in plants is crucial for agriculture and human health. In the present study, we characterized a transporter in rice (Oryza sativa), ZRT/IRT-LIKE PROTEIN10 (OsZIP10), which is primarily expressed in the roots and localized in the endoplasmic reticulum (ER) membrane. OsZIP10 transports Zn from the ER lumen into the cytoplasm and facilitates the radial delivery of Zn via the symplastic pathway in rice roots. Notably, both OsZIP10 knockout mutants and overexpression lines enhanced Zn accumulation by upregulating Zn uptake in roots and the root-to-shoot transfer of Zn, albeit through different mechanisms. Overexpression of OsZIP10 triggered an unfolded protein response and induced the expression of the ER stress-responsive transcription factor BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR74 (bZIP74), producing an unconventional alternatively spliced isoform. This isoform of OsbZIP74 then activated the expression of ZRT/IRT-LIKE PROTEIN7 (OsZIP7) and ZRT/IRT-LIKE PROTEIN9 (OsZIP9), enhancing Zn uptake and translocation. Through a distinctive mechanism, the knockout of OsZIP10 promotes the translocation of BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR50 (bZIP50) from the cytosol to the nucleus, where it activates the expression of OsZIP7 and OsZIP9. Our findings fill a gap in the understanding of Zn transfer in rice roots and establish two distinct signaling pathways linking Zn homeostasis control in the ER with the regulation of Zn uptake, transport, and accumulation.