Zinc Excess Induces a Hypoxia-Like Response by Inhibiting Cysteine Oxidases in Poplar Roots

Abstract

Poplar (Populus spp.) is a tree species considered for the remediation of soil contaminated by metals, including zinc (Zn). To improve poplar's capacity for Zn assimilation and compartmentalization, it is necessary to understand the physiological and biochemical mechanisms that enable these features as well as their regulation at the molecular level. We observed that the molecular response of poplar roots to Zn excess overlapped with that activated by hypoxia. Therefore, we tested the effect of Zn excess on hypoxia-sensing components and investigated the consequence of root hypoxia on poplar fitness and Zn accumulation capacity. Our results suggest that high intracellular Zn concentrations mimic iron deficiency and inhibit the activity of the oxygen sensors Plant Cysteine Oxidases, leading to the stabilization and activation of ERF-VII transcription factors, which are key regulators of the molecular response to hypoxia. Remarkably, excess Zn and waterlogging similarly decreased poplar growth and development. Simultaneous excess Zn and waterlogging did not exacerbate these parameters, although Zn uptake was limited. This study unveils the contribution of the oxygen-sensing machinery to the Zn excess response in poplar, which may be exploited to improve Zn tolerance and increase Zn accumulation capacity in plants.

Comparative Biology of Oxygen Sensing in Plants and Animals

“…A sub-pool of ERFVIIs is stable and sequestered at the plasma membrane through association with ACYL CoA BINDING PROTEINs (ACBP) during normoxia [14,54]. Zinc excess in the soil (detrimental to plant growth), inhibits PCO enzymes, thus causing stabilisation of ERFVIIs [55]. Non-canonical mechanisms also control HIF stability; for example, increases in succinate during the progression of certain types of cancer can allosterically inhibit PHD activity to trigger HIF accumulation under normoxia [56,57].…”

The Geomagnetic Field Is a Contributing Factor for an Efficient Iron Uptake in Arabidopsis thaliana

“…The absence of IRT1 protein in Arabidopsis has been observed under Zn excess (Connolly et al, 2002) and IRT1 protein levels are regulated post-translationally through ubiquitin-mediated proteasomal degradation (Kerkeb et al, 2008;Barberon et al, 2011;Dubeaux et al, 2018). Moreover, intracellular Zn accumulation mimics Fe deficiency and inhibits plant cysteine oxidase (PCO), which is considered the oxygen sensors in plants (Dalle Carbonare et al, 2019). Hence, we cannot exclude that the alteration of Fe deficiency-induced genes expression in plants exposed to NNMF might be linked to such unbalance of metal uptake occurring under this condition, and work is in progress in order to test this hypothesis.…”

The Contribution of Plant Dioxygenases to Hypoxia Signaling

“…Besides hypoxia, conditions that reduce NCO activity such as nitric oxide and low temperature elicit a similar response ( Gibbs et al., 2014 ; Gibbs et al., 2018 ; Hartman et al., 2019 ). For instance, stabilization of ERF-VII transcription factors and induction of anaerobic genes in conditions of iron deficiency and zinc excess has been proposed to result from the PCO inactivation that is observed in both conditions ( Dalle Carbonare et al., 2019 ). These observations support the proposed role of plant dioxygenases as metal sensors ( Vigani et al., 2013 ).…”