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Role of acylamino acid-releasing enzyme/oxidized protein hydrolase in sustaining homeostasis of the cytoplasmic antioxidative system

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Abstract

Acylamino acid-releasing enzyme/oxidized protein hydrolase (AARE/OPH) has been biochemically demonstrated to be a bifunctional protease that has exopeptidase activity against Nα-acylated peptides and endopeptidase activity against oxidized and glycated proteins; however, its physiological role remains unknown. In this study, to determine its physiological significance, we produced AARE/OPH-overexpressing and -suppressed plants and assessed the biological impacts of AARE/OPH. The subcellular localization of Arabidopsis AARE/OPH was found to be cytoplasmic and nuclear by transient expression analysis of tdTomato-fused Arabidopsis AARE/OPH. Overexpression of AARE/OPH exhibited no apparent effect on the level of oxidized proteins because wild types probably have inherently high AARE/OPH activity. Through RNAi gene suppressing, we successfully produced AARE/OPH-suppressed Arabidopsis plants (aare) that exhibited almost no AARE activity. In the aare plant, electrolyte leakage by methyl viologen treatment was enhanced compared to that of non-transformant plants, suggesting that the plasma membranes of aare easily suffered oxidative damage, probably as a result of deterioration of the cytoplasmic antioxidative system. Correspondingly, proteomic analysis revealed that the aare plant accumulated a number of oxidized proteins including cytoplasmic antioxidant enzymes. On the basis of these results, we concluded that AARE/OPH plays a homeostatic role in sustaining the cytoplasmic antioxidative system.

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Abbreviations

AARE:

Acylamino acid-releasing enzyme

DNP:

Dinitrophenylhydrazone

DNPH:

Dinitrophenylhydrazine

Fv/Fm:

Maximal photochemical quantum yield of photosystem II

GST:

Glutathione-S-transferase

GUS:

β-Glucuronidase

ME:

2-Mercaptoethanol

NA:

Nitroanilide

OPH:

Oxidized protein hydrolase

PMSR:

Peptide methionine sulfoxide reductase

RCS:

Reactive carbonyls

ROS:

Reactive oxygen species

SDS:

Sodium dodecyl sulfate

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Acknowledgments

This work was supported by a grant from the Global Center of Excellence for Dryland Science of the Arid Land Research Center, Tottori University, and Grants-in-Aid for Scientific Research for Plant Graduate Student from the Nara Institute of Science and Technology supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan. We thank Dr. Tsuyoshi Nakagawa (Shimane University, Japan) for providing gateway plant expression vector pGWB2.

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Authors and Affiliations

  1. Faculty of Agriculture, Tottori University, Koyama-cho Minami 4-101, Tottori, 680-8553, Japan

    Atsushi Nakai, Sawako Sumi & Kiyoshi Tanaka

  2. Graduate School of Agricultural Science, Kobe University, Rokkodai 1-1, Kobe, 657-8501, Japan

    Yasuo Yamauchi

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  1. Atsushi Nakai
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  2. Yasuo Yamauchi
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  3. Sawako Sumi
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  4. Kiyoshi Tanaka
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Correspondence to Yasuo Yamauchi or Kiyoshi Tanaka.

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A. Nakai and Y. Yamauchi contributed equally to this work.

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Nakai, A., Yamauchi, Y., Sumi, S. et al. Role of acylamino acid-releasing enzyme/oxidized protein hydrolase in sustaining homeostasis of the cytoplasmic antioxidative system. Planta 236, 427–436 (2012). https://doi.org/10.1007/s00425-012-1614-1

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