O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

Rodolfo Zentella; Jianhong Hu; Wen Ping Hsieh; Peter A. Matsumoto; Andrew Dawdy; Benjamin Barnhill; Harriëtte Oldenhof; Lynn M. Hartweck; Sushmit Maitra; Stephen G. Thomas; Shelley Cockrell; Michael Boyce; Jeffrey Shabanowitz; Donald F. Hunt; Neil E. Olszewski; Tai Ping Sun

doi:10.1101/gad.270587.115

O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

Rodolfo Zentella, Jianhong Hu, Wen Ping Hsieh, Peter A. Matsumoto, Andrew Dawdy, Benjamin Barnhill, Harriëtte Oldenhof, Lynn M. Hartweck, Sushmit Maitra, Stephen G. Thomas, Shelley Cockrell, Michael Boyce, Jeffrey Shabanowitz, Donald F. Hunt, Neil E. Olszewski, Tai Ping Sun

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Abstract

The DELLA family of transcription regulators functions as master growth repressors in plants by inhibiting phytohormone gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also play a central role in mediating cross-talk between GA and other signaling pathways via antagonistic direct interactions with key transcription factors. However, how these crucial protein-protein interactions can be dynamically regulated during plant development remains unclear. Here, we show that DELLAs are modified by the O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) SECRET AGENT (SEC) in Arabidopsis. O-GlcNAcylation of the DELLA protein REPRESSOR OF ga1-3 (RGA) inhibits RGA binding to four of its interactors-PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, JASMONATE-ZIM DOMAIN1, and BRASSINAZOLERESISTANT1 (BZR1)—that are key regulators in light, jasmonate, and brassinosteroid signaling pathways, respectively. Consistent with this, the sec-null mutant displayed reduced responses to GA and brassinosteroid and showed decreased expression of several common target genes of DELLAs, BZR1, and PIFs. Our results reveal a direct role of OGT in repressing DELLA activity and indicate that O-GlcNAcylation of DELLAs provides a fine-tuning mechanism in coordinating multiple signaling activities during plant development.

Original language	English (US)
Pages (from-to)	164-176
Number of pages	13
Journal	Genes and Development
Volume	30
Issue number	2
DOIs	https://doi.org/10.1101/gad.270587.115
State	Published - Jan 15 2016

Bibliographical note

Funding Information:
We thank Philip Benfey, Zhen-Ming Pei, and Jim Siedow for helpful comments on the manuscript. We also thank Jeongmoo Park for providing pGST-PIF3, Emily Jie-Ning Yang for her assistance in Y2H assays, and Jonathan Dayan and the Duke University Light Microscopy Core Facility for their help with confocal microscopy. This work was supported by the National Science Foundation (IOS-0641548 and MCB-0923723 to T.-P.S., and MCB-0516690, MCB-0820666, and MCB-1158089 to N.E.O.), U.S. Department of Agriculture (2014-67013-21548 to T.-P.S.), and National Institutes of Health (R01 GM100051 to T.-P.S.,and R01 GM037537 to D.F.H.).

Publisher Copyright:
© 2016 Zentella et al.

Keywords

DELLA-interacting proteins
Gibberellin signaling
Hormone signaling
O-GlcNAc transferase
O-GlcNAcylation of DELLA
SECRET AGENTs

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Zentella, R., Hu, J., Hsieh, W. P., Matsumoto, P. A., Dawdy, A., Barnhill, B., Oldenhof, H., Hartweck, L. M., Maitra, S., Thomas, S. G., Cockrell, S., Boyce, M., Shabanowitz, J., Hunt, D. F., Olszewski, N. E., & Sun, T. P. (2016). O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis. Genes and Development, 30(2), 164-176. https://doi.org/10.1101/gad.270587.115

Zentella, R, Hu, J, Hsieh, WP, Matsumoto, PA, Dawdy, A, Barnhill, B, Oldenhof, H, Hartweck, LM, Maitra, S, Thomas, SG, Cockrell, S, Boyce, M, Shabanowitz, J, Hunt, DF, Olszewski, NE & Sun, TP 2016, 'O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis', Genes and Development, vol. 30, no. 2, pp. 164-176. https://doi.org/10.1101/gad.270587.115

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title = "O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis",

abstract = "The DELLA family of transcription regulators functions as master growth repressors in plants by inhibiting phytohormone gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also play a central role in mediating cross-talk between GA and other signaling pathways via antagonistic direct interactions with key transcription factors. However, how these crucial protein-protein interactions can be dynamically regulated during plant development remains unclear. Here, we show that DELLAs are modified by the O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) SECRET AGENT (SEC) in Arabidopsis. O-GlcNAcylation of the DELLA protein REPRESSOR OF ga1-3 (RGA) inhibits RGA binding to four of its interactors-PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, JASMONATE-ZIM DOMAIN1, and BRASSINAZOLERESISTANT1 (BZR1)—that are key regulators in light, jasmonate, and brassinosteroid signaling pathways, respectively. Consistent with this, the sec-null mutant displayed reduced responses to GA and brassinosteroid and showed decreased expression of several common target genes of DELLAs, BZR1, and PIFs. Our results reveal a direct role of OGT in repressing DELLA activity and indicate that O-GlcNAcylation of DELLAs provides a fine-tuning mechanism in coordinating multiple signaling activities during plant development.",

keywords = "DELLA-interacting proteins, Gibberellin signaling, Hormone signaling, O-GlcNAc transferase, O-GlcNAcylation of DELLA, SECRET AGENTs",

author = "Rodolfo Zentella and Jianhong Hu and Hsieh, {Wen Ping} and Matsumoto, {Peter A.} and Andrew Dawdy and Benjamin Barnhill and Harri{\"e}tte Oldenhof and Hartweck, {Lynn M.} and Sushmit Maitra and Thomas, {Stephen G.} and Shelley Cockrell and Michael Boyce and Jeffrey Shabanowitz and Hunt, {Donald F.} and Olszewski, {Neil E.} and Sun, {Tai Ping}",

note = "Funding Information: We thank Philip Benfey, Zhen-Ming Pei, and Jim Siedow for helpful comments on the manuscript. We also thank Jeongmoo Park for providing pGST-PIF3, Emily Jie-Ning Yang for her assistance in Y2H assays, and Jonathan Dayan and the Duke University Light Microscopy Core Facility for their help with confocal microscopy. This work was supported by the National Science Foundation (IOS-0641548 and MCB-0923723 to T.-P.S., and MCB-0516690, MCB-0820666, and MCB-1158089 to N.E.O.), U.S. Department of Agriculture (2014-67013-21548 to T.-P.S.), and National Institutes of Health (R01 GM100051 to T.-P.S.,and R01 GM037537 to D.F.H.). Publisher Copyright: {\textcopyright} 2016 Zentella et al.",

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T1 - O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

AU - Zentella, Rodolfo

AU - Hu, Jianhong

AU - Hsieh, Wen Ping

AU - Matsumoto, Peter A.

AU - Dawdy, Andrew

AU - Barnhill, Benjamin

AU - Oldenhof, Harriëtte

AU - Hartweck, Lynn M.

AU - Maitra, Sushmit

AU - Thomas, Stephen G.

AU - Cockrell, Shelley

AU - Boyce, Michael

AU - Shabanowitz, Jeffrey

AU - Hunt, Donald F.

AU - Olszewski, Neil E.

AU - Sun, Tai Ping

N1 - Funding Information: We thank Philip Benfey, Zhen-Ming Pei, and Jim Siedow for helpful comments on the manuscript. We also thank Jeongmoo Park for providing pGST-PIF3, Emily Jie-Ning Yang for her assistance in Y2H assays, and Jonathan Dayan and the Duke University Light Microscopy Core Facility for their help with confocal microscopy. This work was supported by the National Science Foundation (IOS-0641548 and MCB-0923723 to T.-P.S., and MCB-0516690, MCB-0820666, and MCB-1158089 to N.E.O.), U.S. Department of Agriculture (2014-67013-21548 to T.-P.S.), and National Institutes of Health (R01 GM100051 to T.-P.S.,and R01 GM037537 to D.F.H.). Publisher Copyright: © 2016 Zentella et al.

PY - 2016/1/15

Y1 - 2016/1/15

N2 - The DELLA family of transcription regulators functions as master growth repressors in plants by inhibiting phytohormone gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also play a central role in mediating cross-talk between GA and other signaling pathways via antagonistic direct interactions with key transcription factors. However, how these crucial protein-protein interactions can be dynamically regulated during plant development remains unclear. Here, we show that DELLAs are modified by the O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) SECRET AGENT (SEC) in Arabidopsis. O-GlcNAcylation of the DELLA protein REPRESSOR OF ga1-3 (RGA) inhibits RGA binding to four of its interactors-PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, JASMONATE-ZIM DOMAIN1, and BRASSINAZOLERESISTANT1 (BZR1)—that are key regulators in light, jasmonate, and brassinosteroid signaling pathways, respectively. Consistent with this, the sec-null mutant displayed reduced responses to GA and brassinosteroid and showed decreased expression of several common target genes of DELLAs, BZR1, and PIFs. Our results reveal a direct role of OGT in repressing DELLA activity and indicate that O-GlcNAcylation of DELLAs provides a fine-tuning mechanism in coordinating multiple signaling activities during plant development.

AB - The DELLA family of transcription regulators functions as master growth repressors in plants by inhibiting phytohormone gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also play a central role in mediating cross-talk between GA and other signaling pathways via antagonistic direct interactions with key transcription factors. However, how these crucial protein-protein interactions can be dynamically regulated during plant development remains unclear. Here, we show that DELLAs are modified by the O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) SECRET AGENT (SEC) in Arabidopsis. O-GlcNAcylation of the DELLA protein REPRESSOR OF ga1-3 (RGA) inhibits RGA binding to four of its interactors-PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, JASMONATE-ZIM DOMAIN1, and BRASSINAZOLERESISTANT1 (BZR1)—that are key regulators in light, jasmonate, and brassinosteroid signaling pathways, respectively. Consistent with this, the sec-null mutant displayed reduced responses to GA and brassinosteroid and showed decreased expression of several common target genes of DELLAs, BZR1, and PIFs. Our results reveal a direct role of OGT in repressing DELLA activity and indicate that O-GlcNAcylation of DELLAs provides a fine-tuning mechanism in coordinating multiple signaling activities during plant development.

KW - DELLA-interacting proteins

KW - Gibberellin signaling

KW - Hormone signaling

KW - O-GlcNAc transferase

KW - O-GlcNAcylation of DELLA

KW - SECRET AGENTs

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AN - SCOPUS:84954553651

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JO - Genes and Development

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ER -

O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

Abstract

Bibliographical note

Keywords

Access

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