The limited exclusion and efficient translocation mediated by organic acids contribute to rare earth element hyperaccumulation in Phytolacca americana.

ABSTRACT

Organic acids play an important role in metal tolerance, uptake, and translocation in hyperaccumulators. Phytolacca americana is a rare earth element (REE) hyperaccumulator, but the underlying mechanisms on REE tolerance and accumulation mediated by organic acids are poorly understood. Here, we reported for the first time the strategy of P. americana to enhance REE tolerance and accumulation through organic acids from root external secretion to internal biosynthesis. Different from the exclusion of heavy metal by organic acid in the typical plants, the results showed that oxalate secretion (0.3-0.6 µmol h-1 g-1 root DW) induced by yttrium (Y) could not prevent Y from entering the roots, resulting in excess Y uptake by P. americana. Yttrium stress also stimulated the accumulation of malate and citrate by 1.4- and 2.0-folds in the root cortex. Exogenous malate and citrate promoted the redistribution of Y from the root cell walls to the shoot by 30% and 21%, respectively. Based on comparative transcriptome analysis, 6-fold up-regulation was observed in PaNIP1;2, whose homology AtNIP1;2 is responsible for the transport of Al-malate in Arabidopsis. These results suggested that the promoted formation of Y-malate complexes within the roots potentially accelerated the transport of Y from P. americana roots to shoots through PaNIP1;2. Our study revealed the potential mechanism of organic acids in the external exclusion and internal detoxification and translocation of REE in P. americana roots, which provided a basis for improving the efficiency of REE phytoextraction.