Low-oxygen response is triggered by an ATP-dependent shift in oleoyl-CoA in Arabidopsis

TY - JOUR

T1 - Low-oxygen response is triggered by an ATP-dependent shift in oleoyl-CoA in Arabidopsis

AU - Schmidt, Romy

AU - Fulda, Martin

AU - Paul, Melanie

AU - Anders, Max

AU - Plum, Frederic

AU - Weits, Daniel

AU - Kosmacz, Monika

AU - Larson, Tony

AU - Graham, Ian Alexander

AU - Beemster, Gerrit

AU - Licausi, Francesco

AU - Gelgenberger, Peter

AU - Schippers, Jos

AU - van Dongen, Joost T.

N1 - © 2018 the Author(s)

PY - 2018/12/18

Y1 - 2018/12/18

N2 - Plant response to environmental stimuli involves integration of multiple signals. Upon low-oxygen stress, plants initiate a set of adaptive responses to circumvent an energy crisis. Here, we reveal how these stress responses are induced by combining (i) energy-dependent changes in the composition of the acyl-CoA pool and (ii) the cellular oxygen concentration. A hypoxia-induced decline of cellular ATP levels reduces LONG-CHAIN ACYL-COA SYNTHETASE activity, which leads to a shift in the composition of the acyl-CoA pool. Subsequently, we show that different acyl-CoAs induce unique molecular responses. Altogether, our data disclose a role for acyl-CoAs acting in a cellular signaling pathway in plants. Upon hypoxia, high oleoyl-CoA levels provide the initial trigger to release the transcription factor RAP2.12 from its interaction partner ACYL-COA BINDING PROTEIN at the plasma membrane. Subsequently, according to the N-end rule for proteasomal degradation, oxygen concentration-dependent stabilization of the subgroup VII ETHYLENE-RESPONSE FACTOR transcription factor RAP2.12 determines the level of hypoxia-specific gene expression. This research unveils a specific mechanism activating low-oxygen stress responses only when a decrease in the oxygen concentration coincides with a drop in energy.

AB - Plant response to environmental stimuli involves integration of multiple signals. Upon low-oxygen stress, plants initiate a set of adaptive responses to circumvent an energy crisis. Here, we reveal how these stress responses are induced by combining (i) energy-dependent changes in the composition of the acyl-CoA pool and (ii) the cellular oxygen concentration. A hypoxia-induced decline of cellular ATP levels reduces LONG-CHAIN ACYL-COA SYNTHETASE activity, which leads to a shift in the composition of the acyl-CoA pool. Subsequently, we show that different acyl-CoAs induce unique molecular responses. Altogether, our data disclose a role for acyl-CoAs acting in a cellular signaling pathway in plants. Upon hypoxia, high oleoyl-CoA levels provide the initial trigger to release the transcription factor RAP2.12 from its interaction partner ACYL-COA BINDING PROTEIN at the plasma membrane. Subsequently, according to the N-end rule for proteasomal degradation, oxygen concentration-dependent stabilization of the subgroup VII ETHYLENE-RESPONSE FACTOR transcription factor RAP2.12 determines the level of hypoxia-specific gene expression. This research unveils a specific mechanism activating low-oxygen stress responses only when a decrease in the oxygen concentration coincides with a drop in energy.

KW - ACBP

KW - Acyl-CoA

KW - ERFVII

KW - Integrative signaling

KW - Low-oxygen stress

KW - Diazepam Binding Inhibitor/metabolism

KW - Signal Transduction

KW - Arabidopsis/genetics

KW - Stress, Physiological

KW - Adenosine Triphosphate/metabolism

KW - Oxygen/metabolism

KW - Cell Hypoxia

KW - Models, Biological

KW - Acyl Coenzyme A/metabolism

KW - Gene Expression Regulation, Plant

KW - Arabidopsis Proteins/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85058697768&partnerID=8YFLogxK

U2 - 10.1073/pnas.1809429115

DO - 10.1073/pnas.1809429115

M3 - Article

C2 - 30509981

SN - 0027-8424

VL - 115

SP - E12101–E12110

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 51

ER -