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P 1B -ATPases are decisive for metal accumulation phenotypes, but mechanisms of their regulation are only partially understood. Here, we studied the Cd/Zn transporting ATPases NcHMA3 and NcHMA4 from  Noccaea caerulescens  as well as AhHMA3 and AhHMA4 from  Arabidopsis halleri . Protein biochemistry was analyzed on HMA4 purified from roots of  N. caerulescens  in active state. Metal titration of NcHMA4 protein with an electrochromic dye as charge indicator suggested that HMA4 reaches maximal ATPase activity when all internal high-affinity Cd 2+  binding sites are occupied. Although HMA4 was reported to be mainly responsible for xylem loading of heavy metals for root to shoot transport, the current study revealed high expression of NcHMA4 in shoots as well. Further, there were additional 20 and 40 kD fragments at replete Zn 2+  and toxic Cd 2+ , but not at deficient Zn 2+  concentrations. Altogether, the protein level expression analysis suggested a more multifunctional role of NcHMA4 than previously assumed. Organ-level transcription analysis through quantitative PCR of mRNA in  N. caerulescens  and  A. halleri  confirmed the strong shoot expression of both  NcHMA4  and  AhHMA4 . Further, in shoots  NcHMA4  was more abundant in 10 μM Zn 2+  and  AhHMA4  in Zn 2+  deficiency. In roots,  NcHMA4  was up-regulated in response to deficient Zn 2+  when compared to replete Zn 2+  and toxic Cd 2+  treatment. In both species,  HMA3  was much more expressed in shoots than in roots, and  HMA3  transcript levels remained rather constant regardless of Zn 2+  supply, but were up-regulated by 10 μM Cd 2+ . Analysis of cellular expression by quantitative mRNA  in situ  hybridisation showed that in  A. halleri , both  HMA3  and  HMA4  mRNA levels were highest in the mesophyll, while in  N. caerulescens  they were highest in the bundle sheath of the vein. This is likely related to the different final storage sites for hyperaccumulated metals in both species: epidermis in  N. caerulescens , mesophyll in  A. halleri .

frontiers in plant science

Protein Biochemistry and Expression Regulation of Cadmium/Zinc Pumping ATPases in the Hyperaccumulator Plants Arabidopsis halleri and Noccaea caerulescens