Arabidopsis molybdenum cofactor sulfurase ABA3 contributes to anthocyanin accumulation and oxidative stress tolerance in ABA-dependent and independent ways

Shunsuke Watanabe,Akihiro Matsui,Motoaki Seki,Yuji Sawada,Muneo Sato,Yuri Kanno,Maho Tanaka,Masami Yokota Hirai,Atsushi Sakamoto,Mitsunori Seo

doi:10.1038/s41598-018-34862-1

Shunsuke Watanabe, Akihiro Matsui + Show 8 more

Open Access

https://doi.org/10.1038/s41598-018-34862-1

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Abstract

Arabidopsis ABA3 is an enzyme involved in the synthesis of the sulfurated form of the molybdenum (Mo) cofactor (MoCo), which is required for the enzymatic activity of so-called Mo enzymes such as aldehyde oxidase (AO) and xanthine dehydrogenase (XDH). It has been reported that AO and XDH are essential for the biosynthesis of the bioactive compounds, ABA and allantoin, respectively. However, aba3 mutants often exhibit pleiotropic phenotypes that are not explained by defects in ABA and/or allantoin biosynthesis, leading us to hypothesize that ABA3 regulates additional metabolic pathways. To reveal the currently unidentified functions of ABA3 we compared transcriptome and metabolome of the Arabidopsis aba3 mutant with those of wild type and a typical ABA-deficient mutant aba2. We found that endogenous levels of anthocyanins, members of the flavonoid group, were significantly lower in the aba3 mutant than in the wild type or the aba2 mutant under oxidative stress. In contrast, mutants defective in the AO and XDH holoenzymes accumulated significantly higher levels of anthocyanins when compared with aba3 mutant under the same conditions. Our findings shed light on a key role of ABA3 in the ABA- and allantoin-independent accumulation of anthocyanins during stress responses.

Highlights

Molybdenum (Mo) is an essential metal for most organisms because it is incorporated into pterin-based cofactors (Mo cofactor; MoCo) and functions as the catalytic center of enzymes involved in fundamental metabolic processes[1]
It is well known that the Arabidopsis ABA3 enzyme plays an essential role in ABA biosynthesis because the enzyme (AO) that catalyzes the last step of ABA biosynthesis requires sulfurated MoCo, synthesized by ABA3, for its enzymatic activity[25]
ABA2 is a member of the short-chain dehydrogenase/reductase (SDR) family, which is composed of 56 gene products in Arabidopsis, the enzyme involved in ABA biosynthesis appears to be encoded by a single gene (ABA2)[58]

Summary

Introduction

Molybdenum (Mo) is an essential metal for most organisms because it is incorporated into pterin-based cofactors (Mo cofactor; MoCo) and functions as the catalytic center of enzymes involved in fundamental metabolic processes[1]. RNA interference targeting of two Arabidopsis XDH genes (AtXDH1 and AtXDH2) caused typical symptoms of nitrogen deficiency, including growth retardation, early senescence, and reduced fertility, indicating that purine catabolism mediated by XDH plays important roles in nitrogen recycling in non-leguminous plants[29]. It has been reported that XDH plays important roles in response to prolonged dark periods[30], water deficit[31] and pathogen attack[32] These functions of XDH can be explained partly by the activities of allantoin to scavenge reactive oxygen species (ROS)[30,33] and/or to activate the β-glucosidase BGLU18 enzyme that catalyzes the hydrolysis of inactive ABA conjugates (ABA-glucose ester) to produce free bioactive ABA34,35

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