O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis.
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2016-01
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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 BRASSINAZOLE-RESISTANT1 (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.
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Zentella, Rodolfo, Jianhong Hu, Wen-Ping Hsieh, Peter A Matsumoto, Andrew Dawdy, Benjamin Barnhill, HarriĆ«tte Oldenhof, Lynn M Hartweck, et al. (2016). O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis. Genes & development, 30(2). pp. 164ā176. 10.1101/gad.270587.115 Retrieved from https://hdl.handle.net/10161/19696.
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Michael Scott Boyce
The Boyce Lab studies mammalian cell signaling through protein glycosylation. For the latest news, project information and publications from our group, please visit our web site at http://www.boycelab.org or follow us on Twitter at https://twitter.com/BoyceLab.
Tai-ping Sun
The diterpenoid phytohormone gibberellin (GA) plays pivotal roles in regulating growth and development throughout the life cycle of higher plants. Mutations affecting GA biosynthesis or GA response were the key to control plant stature in wheat and rice that led to dramatically increased grain yield and contributed greatly to the success of the āGreen Revolutionā in the 1960s. By multi-faceted approaches using the reference plant Arabidopsis, my lab has made major breakthroughs in elucidating the sites and regulatory mechanisms of GA biosynthesis, and the conserved molecular events of GA perception and the early GA signaling pathway. We identified the nuclear transcriptional regulators DELLA proteins, which function as master growth repressors by inhibiting all aspects of GA responses. Binding of GA to its nuclear receptor GID1 enhances the GID1-DELLA interaction, which in turn leads to the rapid proteolysis of DELLA through the ubiquitin-proteasome pathway, and allows transcriptional reprogramming of GA-responsive genes. We and other researchers further showed that GA-GID1-DELLA is a key regulatory module that controls plant growth by integrating internal developmental cues, and external biotic and abiotic signals (light, cold, salt and pathogen stresses). DELLA proteins play a central role in these processes via direct protein-protein interactions with key transcription factors. Our recent studies using genetic and physiological analyses together with chemical biology methods indicate that DELLAās binding affinity to interacting proteins are oppositely regulated by two novel O-linked glycosylations on specific Ser/Thr residues: O-linked N-acetylglucosamine (O-GlcNAc) modification reduces DELLA activity, whereas O-fucosylation enhances DELLA activity. We are investigating the global functions of O-GlcNAcylation and O-fucosylation in regulating plant development.
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