A loss‐of‐function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars

Abstract

Excessive cadmium (Cd) accumulation in rice poses a risk to food safety. OsHMA3 plays an important role in restricting Cd translocation from roots to shoots. A non-functional allele of OsHMA3 has been reported in some Indica rice cultivars with high Cd accumulation, but it is not known if OsHMA3 allelic variation is associated with Cd accumulation in Japonica cultivars. In this study, we identified a Japonica cultivar with consistently high Cd accumulation in shoots and grain in both field and greenhouse experiments. The cultivar possesses an OsHMA3 allele with a predicted amino acid mutation at the 380(th) position from Ser to Arg. The haplotype had no Cd transport activity when the gene was expressed in yeast, and the allele did not complement a known nonfunctional allele of OsHMA3 in F1 test. The allele is present only in temperate Japonica cultivars among diversity panels of 1483 rice cultivars. Different cultivars possessing this allele showed greatly increased root-to-shoot Cd translocation and a shift in root Cd speciation from Cd-S to Cd-O bonding determined by synchrotron X-ray absorption spectroscopy. Our study has identified a new loss-of-function allele of OsHMA3 in Japonica rice cultivars leading to high Cd accumulation in shoots and grain.

Comparative transcriptome combined with morpho‐physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes

“…Yan et al . found a loss‐of‐function allele of OsHMA3 with a predicted amino acid mutation from Ser to Arg at the 380th position, which was associated with high‐Cd accumulation in shoots and grain of a Japonica rice cultivar (Yan et al ., ).…”

Genotypic and Environmental Variations in Grain Cadmium and Arsenic Concentrations Among a Panel of High Yielding Rice Cultivars

“…This gene encodes a Cd transporter localized on the tonoplast functioning to sequester Cd in the vacuoles of root cells, thus limiting Cd translocation to the shoots and grain (Ueno et al 2010; Miyadate et al 2011). Several loss-of-function alleles of OsHMA3 have been identified in a number of Indica (Ueno et al 2010; Miyadate et al 2011) and Japonica (Yan et al, 2016) cultivars, leading to high accumulation of Cd in rice grain. However, these loss-of-function alleles are rare among collections of rice cultivars and germplasm (Yan et al 2016).…”

“…Several loss-of-function alleles of OsHMA3 have been identified in a number of Indica (Ueno et al 2010; Miyadate et al 2011) and Japonica (Yan et al, 2016) cultivars, leading to high accumulation of Cd in rice grain. However, these loss-of-function alleles are rare among collections of rice cultivars and germplasm (Yan et al 2016). It is possible that other functional alleles of OsHMA3 may vary in the functionality by exhibiting different transport activities for Cd.…”

“…There are large genotypic variations among both Japonica and Indica cultivars (Ueno et al, 2009). Pinson et al (2015) and Yan et al (2016) showed that some Japonica cultivars can accumulate high Cd concentrations. Therefore, depending on the cultivars tested, Japonica cultivars as a group may not always show a significant lower Cd accumulation than the Indica group.…”

SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola

“…Mills et al, ). AtHMA3 and OsHMA3 of rice ( Oryza sativa ) mainly localize to the vacuolar membrane of root cells and transport Cd and excess Zn into the vacuoles for detoxification (Chao et al, ; Gravot et al, ; Miyadate, Adachi, Hiraizumi, Tezuka, & Nakazawa, ; Ueno et al, ; Yan et al, ). In the hyperaccumulator, AhHMA4 is a key gene responsible for the remarkable ability of A. halleri to hyperaccumulate Zn in the shoots, and functions by partitioning Zn/Cd into the xylem vessels for root to shoot translocation (Courbot et al, ; Hanikenne et al, ).…”