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Root vacuolar sequestration is one of the best-conserved plant strategies to cope with heavy metal toxicity. Here we report that zinc (Zn) tolerance in  Arabidopsis  requires the action of a novel Major Facilitator Superfamily (MFS) transporter. We show that ZIF2 (Zinc-Induced Facilitator 2) localises primarily at the tonoplast of root cortical cells and is a functional transporter able to mediate Zn efflux when heterologously expressed in yeast. By affecting plant tissue partitioning of the metal ion, loss of  ZIF2  function exacerbates plant sensitivity to excess Zn, while its overexpression enhances Zn tolerance. The  ZIF2  gene is Zn-induced and an intron retention event in its 5′UTR generates two splice variants ( ZIF2.1  and  ZIF2.2 ) encoding the same protein. Importantly, high Zn favours production of the longer  ZIF2.2  transcript, which compared to  ZIF2.1  confers greater Zn tolerance to transgenic plants by promoting higher root Zn immobilization. We show that the retained intron in the  ZIF2  5′UTR enhances translation in a Zn-responsive manner, markedly promoting ZIF2 protein expression under excess Zn. Moreover, Zn regulation of translation driven by the  ZIF2.2  5′UTR depends largely on a predicted stable stem loop immediately upstream of the start codon that is lost in the  ZIF2.1  5′UTR. Collectively, our findings indicate that alternative splicing controls the levels of a Zn-responsive mRNA variant of the ZIF2 transporter to enhance plant tolerance to the metal ion.

Intron Retention in the 5′UTR of the Novel ZIF2 Transporter Enhances Translation to Promote Zinc Tolerance in Arabidopsis