OsHMA3, a P_1B‐type of ATPase affects root‐to‐shoot cadmium translocation in rice by mediating efflux into vacuoles

Abstract

Summary• The cadmium (Cd) over-accumulating rice (Oryza sativa) cv Cho-Ko-Koku was previously shown to have an enhanced rate of root-to-shoot Cd translocation. This trait is controlled by a single recessive allele located at qCdT7.• In this study, using positional cloning and transgenic strategies, heavy metal ATPase 3 (OsHMA3) was identified as the gene that controls root-to-shoot Cd translocation rates. The subcellular localization and Cd-transporting activity of the gene products were also investigated.• The allele of OsHMA3 that confers high root-to-shoot Cd translocation rates (OsHMA3mc) encodes a defective P 1B -ATPase transporter. OsHMA3 fused to green fluorescent protein was localized to vacuolar membranes in plants and yeast. An OsHMA3 transgene complemented Cd sensitivity in a yeast mutant that lacks the ability to transport Cd into vacuoles. By contrast, OsHMA3mc did not complement the Cd sensitivity of this yeast mutant, indicating that the OsHMA3mc transport function was lost.• We propose that the root cell cytoplasm of Cd-overaccumulating rice plants has more Cd available for loading into the xylem as a result of the lack of OsHMA3-mediated transportation of Cd to the vacuoles. This defect results in Cd translocation to the shoots in higher concentrations. These data demonstrate the importance of vacuolar sequestration for Cd accumulation in rice.

Detection of a QTL for accumulating Cd in rice that enables efficient Cd phytoextraction from soil

“…QTL analyses, including ours, identified major QTLs responsible for the high-Cd trait of these three cultivars in almost identical regions on chromosome 7 (Tezuka et al 2010, Ueno et al 2009). Very recently, it has been revealed that OsHMA3, a P 1B -type ATPase, is encoded by a gene within the QTL region on chromosome 7 and plays an important role in controlling shoot Cd accumulation in rice (Miyadate et al 2011, Ueno et al 2010. Functional assays by heterologous expression of OsHMA3 in yeast showed that low-Cd cultivars contain a functional version of this gene, which is involved in Cd storage in root vacuoles.…”

Heavy Metals in Crop Plants: Transport and Redistribution Processes on the Whole Plant Level

“…Good evidence was presented for the involvement of Ni-histidine complexes in the vacuolar compartmentation of Ni and as a consequence in the retention of this heavy metal in roots [59]. A heavy metal ATPase was suggested to be involved in Cd accumulation in vacuoles of root cells causing Cd retention in roots and decreasing the transport to the shoot [66].…”

“…After the release into the root xylem, free or chelated ions flow with the xylem sap upwards (Figure 2). Important for the concentration of heavy metals in the transpiration stream are xylem loading in the roots, interactions with cell walls during acropetal transport and selective removal from the xylem sap [65,66,68,69]. If there would be no further redistribution, the heavy metals would accumulate primarily in photosynthetically active (transpiring) leaves.…”

A Member of the Heavy Metal P-Type ATPase OsHMA5 Is Involved in Xylem Loading of Copper in Rice

“…Among rice P-type ATPases characterized, OsHMA2 transports Zn and Cd (Satoh-Nagasawa et al, 2012;Takahashi et al, 2012;Yamaji et al, 2013), OsHMA3 is involved in Cd accumulation (Ueno et al, 2010;Miyadate et al, 2011), and OsHMA9 is responsible for the transport of Zn, Cu, Pb, and Cd (Lee et al, 2007). Knockout of OsHMA5 only resulted in altered Cu concentration, but not other metals, including Zn, Fe, and Mn (Fig.…”

“…Furthermore, OsHMA2 at the node is required for preferential distribution of Zn to young leaves and panicles (Yamaji et al, 2013). OsHMA3 is localized to the tonoplast of the root cells and responsible for the sequestration of Cd into the vacuoles (Ueno et al, 2010;Miyadate et al, 2011). On the other hand, OsHMA9 was mainly expressed in vascular tissues, including the xylem and phloem (Lee et al, 2007).…”