Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species

Abstract

<jats:title>Abstract</jats:title><jats:p>Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or oxidative stress. Cadmium (Cd) is a non-essential heavy metal that induces both Fe-deficiency and oxidative stress; however, the mechanisms underlying these Cd-induced responses are still elusive. Here we explored Cd-induced Fe-associated responses in wildtype <jats:italic>Arabidopsis</jats:italic> and <jats:italic>opt3-2</jats:italic>, a mutant that over-accumulates Fe. Gene expression profiling revealed a large overlap between transcripts induced by Fe-deficiency and Cd exposure in wildtype plants and the <jats:italic>opt3</jats:italic> mutant. Interestingly, vascular-localized Fe-responsive genes were found to be highly induced by Cd even in the presence of high Fe and H<jats:sub>2</jats:sub>O<jats:sub>2</jats:sub> levels, suggesting that Cd impairs Fe sensing. It was recently shown that Fe-S cluster-containing proteins AtNEET, play a role in Fe sensing. Our data shows that Cd negatively impacts both the stability and Fe-S transfer activity of AtNEET. Altogether, our data indicate that Fe-deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe-deficiency responses prevents the induction of specific gene networks when Fe and H<jats:sub>2</jats:sub>O<jats:sub>2</jats:sub> levels are high. Other Cd/Fe-responsive genes however, are insensitive to this negative feedback regulation suggesting that their induction is the result of an impaired Fe sensing as opposed to the traditional view of Cd/Fe uptake competition at the root level.</jats:p><jats:sec><jats:title>Highlight</jats:title><jats:p>Cadmium induces an iron-deficiency response often explained by root uptake competition; here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities.</jats:p></jats:sec>

OPEN leaf: an open-source cloud-based phenotyping system for tracking dynamic changes at leaf-specific resolution in Arabidopsis

“…during Fe deficiency experiments in Arabidopsis where prolonged Fe deprivation leads to a restricted distribution of Fe to developing (sink) leaves to preserve optimal photosynthesis in mature (source) leaves (Hantzis et al, 2018;McInturf et al, 2021).…”

“…Leaf responses to nutrient availability are expected to be striking different from roots as the Arabidopsis rosette includes both sink and source tissues ( i.e ., young and mature leaves), while roots are by definition a sink tissue. In fact, unique leaf-specific transcriptional responses have been described during Fe deficiency experiments in Arabidopsis where prolonged Fe deprivation leads to a restricted distribution of Fe to developing (sink) leaves to preserve optimal photosynthesis in mature (source) leaves (Hantzis et al , 2018; McInturf et al , 2021).…”