Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets

Mark D White, Maria Klecker, Richard J Hopkinson, Daan A Weits, Carolin Mueller, Christin Naumann, Rebecca O'Neill, James Wickens, Jiayu Yang, Jonathan C Brooks-Bartlett, Elspeth F Garman, Tom N Grossmann, Nico Dissmeyer, Emily Flashman

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.

Original languageEnglish
Pages (from-to)14690
JournalNature Communications
Volume8
DOIs
Publication statusPublished - 23 Mar 2017

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Cysteine Dioxygenase
Sulfinic Acids
Dioxygenases
oxidase
cysteine
Transferases
Stabilization
hypoxia
Oxidation
Food Supply
Substrates
stabilization
Agriculture
Crops
Cysteine
oxidation
acids
agriculture
crops
food

Keywords

  • Journal Article

Cite this

White, M. D., Klecker, M., Hopkinson, R. J., Weits, D. A., Mueller, C., Naumann, C., ... Flashman, E. (2017). Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nature Communications, 8, 14690. https://doi.org/10.1038/ncomms14690
White, Mark D ; Klecker, Maria ; Hopkinson, Richard J ; Weits, Daan A ; Mueller, Carolin ; Naumann, Christin ; O'Neill, Rebecca ; Wickens, James ; Yang, Jiayu ; Brooks-Bartlett, Jonathan C ; Garman, Elspeth F ; Grossmann, Tom N ; Dissmeyer, Nico ; Flashman, Emily. / Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. In: Nature Communications. 2017 ; Vol. 8. pp. 14690.
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abstract = "Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.",
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White, MD, Klecker, M, Hopkinson, RJ, Weits, DA, Mueller, C, Naumann, C, O'Neill, R, Wickens, J, Yang, J, Brooks-Bartlett, JC, Garman, EF, Grossmann, TN, Dissmeyer, N & Flashman, E 2017, 'Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets' Nature Communications, vol. 8, pp. 14690. https://doi.org/10.1038/ncomms14690

Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. / White, Mark D; Klecker, Maria; Hopkinson, Richard J; Weits, Daan A; Mueller, Carolin; Naumann, Christin; O'Neill, Rebecca; Wickens, James; Yang, Jiayu; Brooks-Bartlett, Jonathan C; Garman, Elspeth F; Grossmann, Tom N; Dissmeyer, Nico; Flashman, Emily.

In: Nature Communications, Vol. 8, 23.03.2017, p. 14690.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets

AU - White, Mark D

AU - Klecker, Maria

AU - Hopkinson, Richard J

AU - Weits, Daan A

AU - Mueller, Carolin

AU - Naumann, Christin

AU - O'Neill, Rebecca

AU - Wickens, James

AU - Yang, Jiayu

AU - Brooks-Bartlett, Jonathan C

AU - Garman, Elspeth F

AU - Grossmann, Tom N

AU - Dissmeyer, Nico

AU - Flashman, Emily

PY - 2017/3/23

Y1 - 2017/3/23

N2 - Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.

AB - Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.

KW - Journal Article

U2 - 10.1038/ncomms14690

DO - 10.1038/ncomms14690

M3 - Article

VL - 8

SP - 14690

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

ER -