Deregulated High Affinity Copper Transport Alters Iron Homeostasis in Arabidopsis

Abstract

The present work describes the effects on iron homeostasis when copper transport was deregulated in Arabidopsis thaliana by overexpressing high affinity copper transporters COPT1 and COPT3 ( COPT OE ). A genome-wide analysis conducted on COPT1 OE plants, highlighted that iron homeostasis gene expression was affected under both copper deficiency and excess. Among the altered genes were those encoding the iron uptake machinery and their transcriptional regulators. Subsequently, COPT OE seedlings contained less iron and were more sensitive than controls to iron deficiency. The deregulation of copper (I) uptake hindered the transcriptional activation of the subgroup Ib of basic helix-loop-helix ( bHLH-Ib ) factors under copper deficiency. Oppositely, copper excess inhibited the expression of the master regulator FIT but activated bHLH-Ib expression in COPT OE plants, in both cases leading to the lack of an adequate iron uptake response. As copper increased in the media, iron (III) was accumulated in roots, and the ratio iron (III)/iron (II) was increased in COPT OE plants. Thus, iron (III) overloading in COPT OE roots inhibited local iron deficiency responses, aimed to metal uptake from soil, leading to a general lower iron content in the COPT OE seedlings. These results emphasized the importance of appropriate spatiotemporal copper uptake for iron homeostasis under non-optimal copper supply. The understanding of the role of copper uptake in iron metabolism could be applied for increasing crops resistance to iron deficiency.

Age Dependent Partitioning Patterns of Essential Nutrients Induced by Copper Feeding Status in Leaves and Stems of Poplar

“…This difference could be due to the cross talk between Fe and Cu homeostasis ( Carrió-Seguí et al, 2019 ; Rai et al, 2021 ), such as increased activities of enzymes with a Fe cofactor (e.g., Fe superoxide dismutase) that could compensate for decreased activities of functionally analogous enzymes that require a Cu cofactor (e.g., Cu/Zn-superoxide dismutase; Kliebenstein et al, 1998 ; Cohu and Pilon, 2007 ). Perea-García et al (2020) observed an increase in root and shoot Fe concentrations in wild type Arabidopsis under Cu deficiency, and Waters and Armbrust (2013) found increased Cu concentrations under Fe deficiency. Additionally, it has been observed that Cu deficiency induces the expression of Cu-II chelate reductase activity in root tips ( Bernal et al, 2012 ).…”

FIT and bHLH Ib transcription factors modulate iron and copper crosstalk in Arabidopsis

“…SPL7 does not only govern Cu homeostasis signaling pathway but also represses Fe-homeostasis genes, IRON MANs (IMAs) and bHLH Ib, by an unknown strategy (Kastoori Ramamurthy et al, 2018). A recent report found that excessive Cu reduces the expression of FIT but activates bHLH Ib in the COPT1 overexpression plants (Perea-García et al, 2020). Thus, further investigation in depth is required to uncover the molecular mechanism underling the crosstalk between Fe and Cu homeostasis.…”

“…COPT2 is also up‐regulated by Fe or (and) Cu deficiency (Perea‐García et al, 2013). In addition, several studies reported the crosstalk between Fe and Cu signalling networks in plants (Bernal et al, 2012; Garcia‐Molina, Marino, Lehmann, & Leister, 2020; Kastoori Ramamurthy et al, 2018; Perea‐García et al, 2013, 2020; Puig et al, 2007; Waters et al, 2012; Waters & Armbrust, 2013). However, the molecular mechanism underling Fe and Cu crosstalk remains unclear.…”

Involvement of Arabidopsis Multi-Copper Oxidase-Encoding LACCASE12 in Root-to-Shoot Iron Partitioning: A Novel Example of Copper-Iron Crosstalk

“…These plants show an altered expression of several Fe homeostasis genes, including genes of the Fe uptake system and their transcriptional regulators. This suggests the relevance of a correct interconnection between Cu and Fe homeostasis under metal deficiency growth conditions (Perea-García et al, 2020).…”