ZRT‐IRT‐Like PROTEIN 6 expression perturbs local ion homeostasis in flowers and leads to anther indehiscence and male sterility

Abstract

Metallic micronutrients are essential throughout the plant life cycle. Maintaining metal homeostasis in plant tissues requires a highly complex and finely tuned network controlling metal uptake, transport, distribution and storage. Zinc and cadmium hyperaccumulation, such as observed in the model plant Arabidopsis halleri, represents an extreme evolution of this network. Here, non‐ectopic overexpression of the A. halleri ZIP6 (AhZIP6) gene, encoding a zinc and cadmium influx transporter, in Arabidopsis thaliana enabled examining the importance of zinc for flower development and reproduction. We show that AhZIP6 expression in flowers leads to male sterility resulting from anther indehiscence in a dose‐dependent manner. The sterility phenotype is associated to delayed tapetum degradation and endothecium collapse, as well as increased magnesium and potassium accumulation and higher expression of the MHX gene in stamens. It is rescued by the co‐expression of the zinc efflux transporter AhHMA4, linking the sterility phenotype to zinc homeostasis. Altogether, our results confirm that AhZIP6 is able to transport zinc in planta and highlight the importance of fine‐tuning zinc homeostasis in reproductive organs. The study illustrates how the characterization of metal hyperaccumulation mechanisms can reveal key nodes and processes in the metal homeostasis network.

Reduced expression of bZIP19 and bZIP23 increases zinc and cadmium accumulation in Arabidopsis halleri

“…Finally, several ZIP ( Zinc‐regulated transporter, Iron‐regulated transporter‐like Proteins ) genes were suggested to contribute to enhanced zinc uptake by roots, zinc radial transport and zinc distribution in shoots (Krämer et al, 2007; Lin et al, 2009; Talke et al, 2006). However, with the exception of AhZIP6 (Spielmann et al, 2020; Spielmann, Detry, et al, 2022), experimental evidence for their exact roles in metal hyperaccumulation and tolerance is still lacking.…”