Article

Universal stress protein HRU1 mediates ROS homeostasis under anoxia

  • Nature Plants 1, Article number: 15151 (2015)
  • doi:10.1038/nplants.2015.151
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Abstract

Plant survival is greatly impaired when oxygen levels are limiting, such as during flooding or when anatomical constraints limit oxygen diffusion. Oxygen sensing in Arabidopsis thaliana is mediated by Ethylene Responsive Factor (ERF)-VII transcription factors, which control a core set of hypoxia- and anoxia-responsive genes responsible for metabolic acclimation to low-oxygen conditions. Anoxic conditions also induce genes related to reactive oxygen species (ROS). Whether the oxygen-sensing machinery coordinates ROS production under anoxia has remained unclear. Here we show that a low-oxygen-responsive universal stress protein (USP), Hypoxia Responsive Universal Stress Protein 1 (HRU1), is induced by RAP2.12 (Related to Apetala 2.12), an ERF-VII protein, and modulates ROS production in Arabidopsis. We found that HRU1 is strongly induced by submergence, but that this induction is abolished in plants lacking RAP2.12. Mutation of HRU1 through transfer DNA (T-DNA) insertion alters hydrogen peroxide production, and reduces tolerance to submergence and anoxia. Yeast two-hybrid and bimolecular fluorescence complementation (BiFC) analyses reveal that HRU1 interacts with proteins that induce ROS production, the GTPase ROP2 and the NADPH oxidase RbohD, pointing to the existence of a low-oxygen-specific mechanism for the modulation of ROS levels. We propose that HRU1 coordinates oxygen sensing with ROS signalling under anoxic conditions.

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Acknowledgements

We thank J. Bailey-Serres for reviewing an early version of this manuscript, A. Galli for helpful suggestions about the Y2H assay and C. Kiferle for helpful assistance in data analysis. We acknowledge Z. Yang (University of California, Riverside) for providing us with the plasmid carrying the coding sequence for the RIC1-Maltose Binding Protein (MBP) fusion protein.

Author information

Author notes

    • Silvia Gonzali
    •  & Elena Loreti

    These authors contributed equally to this work.

Affiliations

  1. PlantLab, Institute of Life Sciences, Scuola Superiore Sant'Anna, Via Mariscoglio 34, Pisa 56124, Italy

    • Silvia Gonzali
    • , Giacomo Novi
    • , Sandro Parlanti
    • , Chiara Pucciariello
    • , Laura Bassolino
    • , Valeria Banti
    • , Francesco Licausi
    •  & Pierdomenico Perata
  2. nanoPlant Center @NEST, Institute of Life Sciences, Scuola Superiore Sant'Anna, Piazza San Silvestro 12, Pisa 56127, Italy

    • Silvia Gonzali
    • , Chiara Pucciariello
    • , Francesco Licausi
    •  & Pierdomenico Perata
  3. Institute of Agricultural Biology and Biotechnology, National Research Council, Via Moruzzi 1, Pisa 56100, Italy

    • Elena Loreti
  4. Center for Nanotechnology Innovation @NEST, Istituto Italiano di Tecnologia, Piazza San Silvestro 12, Pisa 56127, Italy

    • Francesco Cardarelli

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Contributions

S.G., E.L., L.B., S.P., C.P. and F.L. performed the molecular biology experiments, Y2H, BiFC and split-luciferase assays. G.N. and S.P. obtained the mutants and performed the phenotypic characterization of the mutants and transgenic lines. G.N. performed the submergence and hypoxia tolerance assays. E.L. and P.P. performed the transient expression analysis in Nicotiana. V.B. and C.P. performed the ROP pull-down assays. F.C. designed, performed and analysed the FRAP experiments. P.P., S.G. and E.L. designed the experiments. P.P. and E.L. wrote the manuscript. All authors discussed and commented on the content of the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Pierdomenico Perata.

Supplementary information