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, 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

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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 -