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Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice

The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice. To shed light on the mechanisms underlying its growth-promoting effect, we employed a combined omics approach integrating transcriptomics and metabolomics analysis of rice seedlings treated with zaxinone, a...

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Autores principales: Wang, Jian You, Alseekh, Saleh, Xiao, Tingting, Ablazov, Abdugaffor, Perez de Souza, Leonardo, Fiorilli, Valentina, Anggarani, Marita, Lin, Pei-Yu, Votta, Cristina, Novero, Mara, Jamil, Muhammad, Lanfranco, Luisa, Hsing, Yue-Ie C., Blilou, Ikram, Fernie, Alisdair R., Al-Babili, Salim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545949/
https://www.ncbi.nlm.nih.gov/pubmed/34697384
http://dx.doi.org/10.1038/s42003-021-02740-8
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author Wang, Jian You
Alseekh, Saleh
Xiao, Tingting
Ablazov, Abdugaffor
Perez de Souza, Leonardo
Fiorilli, Valentina
Anggarani, Marita
Lin, Pei-Yu
Votta, Cristina
Novero, Mara
Jamil, Muhammad
Lanfranco, Luisa
Hsing, Yue-Ie C.
Blilou, Ikram
Fernie, Alisdair R.
Al-Babili, Salim
author_facet Wang, Jian You
Alseekh, Saleh
Xiao, Tingting
Ablazov, Abdugaffor
Perez de Souza, Leonardo
Fiorilli, Valentina
Anggarani, Marita
Lin, Pei-Yu
Votta, Cristina
Novero, Mara
Jamil, Muhammad
Lanfranco, Luisa
Hsing, Yue-Ie C.
Blilou, Ikram
Fernie, Alisdair R.
Al-Babili, Salim
author_sort Wang, Jian You
collection PubMed
description The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice. To shed light on the mechanisms underlying its growth-promoting effect, we employed a combined omics approach integrating transcriptomics and metabolomics analysis of rice seedlings treated with zaxinone, and determined the resulting changes at the cellular and hormonal levels. Metabolites as well as transcripts analysis demonstrate that zaxinone application increased sugar content and triggered glycolysis, the tricarboxylic acid cycle and other sugar-related metabolic processes in rice roots. In addition, zaxinone treatment led to an increased root starch content and induced glycosylation of cytokinins. The transcriptomic, metabolic and hormonal changes were accompanied by striking alterations of roots at cellular level, which showed an increase in apex length, diameter, and the number of cells and cortex cell layers. Remarkably, zaxinone did not affect the metabolism of roots in a strigolactone deficient mutant, suggesting an essential role of strigolactone in the zaxinone growth-promoting activity. Taken together, our results unravel zaxinone as a global regulator of the transcriptome and metabolome, as well as of hormonal and cellular composition of rice roots. Moreover, they suggest that zaxinone promotes rice growth most likely by increasing sugar uptake and metabolism, and reinforce the potential of this compound in increasing rice performance.
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spelling pubmed-85459492021-10-29 Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice Wang, Jian You Alseekh, Saleh Xiao, Tingting Ablazov, Abdugaffor Perez de Souza, Leonardo Fiorilli, Valentina Anggarani, Marita Lin, Pei-Yu Votta, Cristina Novero, Mara Jamil, Muhammad Lanfranco, Luisa Hsing, Yue-Ie C. Blilou, Ikram Fernie, Alisdair R. Al-Babili, Salim Commun Biol Article The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice. To shed light on the mechanisms underlying its growth-promoting effect, we employed a combined omics approach integrating transcriptomics and metabolomics analysis of rice seedlings treated with zaxinone, and determined the resulting changes at the cellular and hormonal levels. Metabolites as well as transcripts analysis demonstrate that zaxinone application increased sugar content and triggered glycolysis, the tricarboxylic acid cycle and other sugar-related metabolic processes in rice roots. In addition, zaxinone treatment led to an increased root starch content and induced glycosylation of cytokinins. The transcriptomic, metabolic and hormonal changes were accompanied by striking alterations of roots at cellular level, which showed an increase in apex length, diameter, and the number of cells and cortex cell layers. Remarkably, zaxinone did not affect the metabolism of roots in a strigolactone deficient mutant, suggesting an essential role of strigolactone in the zaxinone growth-promoting activity. Taken together, our results unravel zaxinone as a global regulator of the transcriptome and metabolome, as well as of hormonal and cellular composition of rice roots. Moreover, they suggest that zaxinone promotes rice growth most likely by increasing sugar uptake and metabolism, and reinforce the potential of this compound in increasing rice performance. Nature Publishing Group UK 2021-10-25 /pmc/articles/PMC8545949/ /pubmed/34697384 http://dx.doi.org/10.1038/s42003-021-02740-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wang, Jian You
Alseekh, Saleh
Xiao, Tingting
Ablazov, Abdugaffor
Perez de Souza, Leonardo
Fiorilli, Valentina
Anggarani, Marita
Lin, Pei-Yu
Votta, Cristina
Novero, Mara
Jamil, Muhammad
Lanfranco, Luisa
Hsing, Yue-Ie C.
Blilou, Ikram
Fernie, Alisdair R.
Al-Babili, Salim
Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title_full Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title_fullStr Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title_full_unstemmed Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title_short Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
title_sort multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545949/
https://www.ncbi.nlm.nih.gov/pubmed/34697384
http://dx.doi.org/10.1038/s42003-021-02740-8
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