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TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis

Spermidine (Spd) is a nitrogen sink and signaling molecule that plays pivotal roles in eukaryotic cell growth and must be finetuned to meet various energy demands. In eukaryotes, target of rapamycin (TOR) is a central nutrient sensor, especially N, and a master-regulator of growth and development. H...

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Autores principales: Salazar-Díaz, Kenia, Dong, Yihan, Papdi, Csaba, Ferruzca-Rubio, Ernesto Miguel, Olea-Badillo, Grecia, Ryabova, Lyubov A., Dinkova, Tzvetanka D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571727/
https://www.ncbi.nlm.nih.gov/pubmed/34765910
http://dx.doi.org/10.1016/j.isci.2021.103260
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author Salazar-Díaz, Kenia
Dong, Yihan
Papdi, Csaba
Ferruzca-Rubio, Ernesto Miguel
Olea-Badillo, Grecia
Ryabova, Lyubov A.
Dinkova, Tzvetanka D.
author_facet Salazar-Díaz, Kenia
Dong, Yihan
Papdi, Csaba
Ferruzca-Rubio, Ernesto Miguel
Olea-Badillo, Grecia
Ryabova, Lyubov A.
Dinkova, Tzvetanka D.
author_sort Salazar-Díaz, Kenia
collection PubMed
description Spermidine (Spd) is a nitrogen sink and signaling molecule that plays pivotal roles in eukaryotic cell growth and must be finetuned to meet various energy demands. In eukaryotes, target of rapamycin (TOR) is a central nutrient sensor, especially N, and a master-regulator of growth and development. Here, we discovered that Spd stimulates the growth of maize and Arabidopsis seedlings through TOR signaling. Inhibition of Spd biosynthesis led to TOR inactivation and growth defects. Furthermore, disruption of a TOR complex partner RAPTOR1B abolished seedling growth stimulation by Spd. Strikingly, TOR activated by Spd promotes translation of key metabolic enzyme upstream open reading frame (uORF)-containing mRNAs, PAO and CuAO, by facilitating translation reinitiation and providing feedback to polyamine metabolism and TOR activation. The Spd-TOR relay protected young-age seedlings of maize from expeditious stress heat shock. Our results demonstrate Spd is an upstream effector of TOR kinase in planta and provide its potential application for crop protection.
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spelling pubmed-85717272021-11-10 TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis Salazar-Díaz, Kenia Dong, Yihan Papdi, Csaba Ferruzca-Rubio, Ernesto Miguel Olea-Badillo, Grecia Ryabova, Lyubov A. Dinkova, Tzvetanka D. iScience Article Spermidine (Spd) is a nitrogen sink and signaling molecule that plays pivotal roles in eukaryotic cell growth and must be finetuned to meet various energy demands. In eukaryotes, target of rapamycin (TOR) is a central nutrient sensor, especially N, and a master-regulator of growth and development. Here, we discovered that Spd stimulates the growth of maize and Arabidopsis seedlings through TOR signaling. Inhibition of Spd biosynthesis led to TOR inactivation and growth defects. Furthermore, disruption of a TOR complex partner RAPTOR1B abolished seedling growth stimulation by Spd. Strikingly, TOR activated by Spd promotes translation of key metabolic enzyme upstream open reading frame (uORF)-containing mRNAs, PAO and CuAO, by facilitating translation reinitiation and providing feedback to polyamine metabolism and TOR activation. The Spd-TOR relay protected young-age seedlings of maize from expeditious stress heat shock. Our results demonstrate Spd is an upstream effector of TOR kinase in planta and provide its potential application for crop protection. Elsevier 2021-10-12 /pmc/articles/PMC8571727/ /pubmed/34765910 http://dx.doi.org/10.1016/j.isci.2021.103260 Text en © 2021 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Salazar-Díaz, Kenia
Dong, Yihan
Papdi, Csaba
Ferruzca-Rubio, Ernesto Miguel
Olea-Badillo, Grecia
Ryabova, Lyubov A.
Dinkova, Tzvetanka D.
TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title_full TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title_fullStr TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title_full_unstemmed TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title_short TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis
title_sort tor senses and regulates spermidine metabolism during seedling establishment and growth in maize and arabidopsis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571727/
https://www.ncbi.nlm.nih.gov/pubmed/34765910
http://dx.doi.org/10.1016/j.isci.2021.103260
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