Iron and Phosphate Deficiency Regulators Concertedly Control Coumarin Profiles in Arabidopsis thaliana Roots During Iron, Phosphate, and Combined Deficiencies.

Jörg Ziegler,Ranju Chutia,Steffen Abel

doi:10.3389/fpls.2019.00113

Jörg Ziegler, Ranju Chutia + Show 1 more

Open Access

https://doi.org/10.3389/fpls.2019.00113

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Abstract

Plants face varying nutrient conditions, to which they have to adapt to. Adaptive responses are nutrient-specific and strategies to ensure supply and homeostasis for one nutrient might be opposite to another one, as shown for phosphate (Pi) and iron (Fe) deficiency responses, where many genes are regulated in an opposing manner. This was also observed on the metabolite levels. Whereas root and exudate levels of catechol-type coumarins, phenylpropanoid-derived 2-benzopyranones, which facilitate Fe acquisition, are elevated after Fe deficiency, they are decreased after Pi deficiency. Exposing plants to combined Pi and Fe deficiency showed that the generation of coumarin profiles in Arabidopsis thaliana roots by Pi deficiency considerably depends on the availability of Fe. Similarly, the effect of Fe deficiency on coumarin profiles is different at low compared to high Pi availability. These findings suggest a fine-tuning of coumarin profiles, which depends on Fe and Pi availability. T-DNA insertion lines exhibiting aberrant expression of genes involved in the regulation of Pi starvation responses (PHO1, PHR1, bHLH32, PHL1, SPX1) and Fe starvation responses (BRUTUS, PYE, bHLH104, FIT) were used to analyze the regulation of the generation of coumarin profiles in Arabidopsis thaliana roots by Pi, Fe, and combined Pi and Fe deficiency. The analysis revealed a role of several Fe-deficiency response regulators in the regulation of Fe and of Pi deficiency-induced coumarin profiles as well as for Pi deficiency response regulators in the regulation of Pi and of Fe deficiency-induced coumarin profiles. Additionally, the regulation of Fe deficiency-induced coumarin profiles by Fe deficiency response regulators is influenced by Pi availability. Conversely, regulation of Pi deficiency-induced coumarin profiles by Pi deficiency response regulators is modified by Fe availability.

Highlights

Coumarins are a group of compounds derived from the phenylpropanoid pathway
Our analysis showed that sideritin glucoside and fraxin levels were strongly reduced (50- and 20- fold, respectively) in these plants compared to WT after exposure to Fe limiting conditions (+Pi, −Fe), scopolin and scopoletin levels were diminished by 30%, whereas esculin levels were indistinguishable to WT (Figure 5 and Supplementary Figure S3)
We recently showed an opposite effect of Pi deficiency on coumarin profiles, resulting in reduced exudation and reduced accumulation especially of catechol type coumarins and their glucosides (Ziegler et al, 2016)

Summary

Introduction

Coumarins are a group of compounds derived from the phenylpropanoid pathway. They possess a 2-benzopyranone core structure and individual members of this class of compounds exhibit different substitution patterns (Shimizu, 2014). It was shown that biosynthesis and exudation of coumarins, especially of catechol type coumarins, contribute to iron acquisition under iron limiting conditions (RodríguezCelma et al, 2013; Fourcroy et al, 2014, 2016; Schmid et al, 2014; Schmidt et al, 2014; Sisó-Terraza et al, 2016; Rajniak et al, 2018; Siwinska et al, 2018; Tsai et al, 2018). With the exception of FIT, the contribution of these regulators to iron deficiency-induced coumarin accumulation has not been investigated so far

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