HMA1 and PAA1, two chloroplast-envelope PIB-ATPases, play distinct roles in chloroplast copper homeostasis

Abstract

Copper is an essential micronutrient but it is also potentially toxic as copper ions can catalyse the production of free radicals, which result in various types of cell damage. Therefore, copper homeostasis in plant and animal cells must be tightly controlled. In the chloroplast, copper import is mediated by a chloroplast-envelope PIB-type ATPase, HMA6/PAA1. Copper may also be imported by HMA1, another chloroplast-envelope PIB-ATPase. To get more insights into the specific functional roles of HMA1 and PAA1 in copper homeostasis, this study analysed the phenotypes of plants affected in the expression of both HMA1 and PAA1 ATPases, as well as of plants overexpressing HMA1 in a paa1 mutant background. The results presented here provide new evidence associating HMA1 with copper homeostasis in the chloroplast. These data suggest that HMA1 and PAA1 behave as distinct pathways for copper import and targeting to the chloroplast. Finally, this work also provides evidence for an alternative route for copper import into the chloroplast mediated by an as-yet unidentified transporter that is neither HMA1 nor PAA1.

Metabolic connectivity as a driver of host and endosymbiont integration

“…S1). Another family of interest contained the copper transporting P-type ATPases HMA1 and PAA1 (34)(35)(36). This component included the eukaryote derived ACA1/PEA1 (a calcium ATPase; Table S1) family that shares some links with the HMA1/PAA1 cluster ( Figs.…”

“…However, due to its high toxicity (e.g., it can catalyze the production of free radicals), in plant cells, copper is associated with Cu chaperones (39,40). Recent work suggests that the HMA1 and PAA1 transporters operate as distinct pathways for copper import into plastids (36), thereby putatively explaining the maintenance of two diverged copies in Archaeplastida.…”

Genome-Wide Identification, Cloning and Functional Analysis of the Zinc/Iron-Regulated Transporter-Like Protein (ZIP) Gene Family in Trifoliate Orange (Poncirus trifoliata L. Raf.)

“…To cope with this issue, plants have developed a tightly regulated cellular homeostasis system to balance the uptake, distribution and utilization of these metal ions (Clemens, 2001; Grotz and Guerinot, 2006). In this system, various members of the zinc/iron-regulated transporter (ZRT/IRT)-related protein (ZIP) family, natural resistance associated macrophage protein (NRAMP) family, cation diffusion facilitator (CDF) family, yellow stripe-like (YSL) family, major facilitator super family (MFS), P 1B -type heavy metal ATPase (HMA) family, vacuolar iron transporter (VIT) family, and the cation exchange (CAX) family have been shown to play key roles (Vigani et al, 2013; Boutigny et al, 2014; Bashir et al, 2016). …”

Got to hide your Zn away: Molecular control of Zn accumulation and biotechnological applications

“…In a recent study, however, plants overexpressing AtHMA1 in a paa1 background (lacking the Cu importer responsible for providing Cu to plastocyanin) showed similar Zn concentration in chloroplasts compared to wild-type, thus suggesting that AtHMA1 is not a metal exporter. Arabidopsis plants over-expressing AtHMA1 are not resistant to high Zn concentration [61]. It was proposed that the previously observed high Zn sensitivity in hma1 mutants is an indirect effect, caused by the absence of the AtHMA3 gene in the Col-0 background in which the experiments were performed.…”