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

Jian You Wang; Saleh Alseekh; Tingting Xiao; Abdugaffor Ablazov; Leonardo Perez de Souza; Valentina Fiorilli; Marita Anggarani; Pei-Yu Lin; Cristina Votta; Mara Novero; Muhammad Jamil; Luisa Lanfranco; Yue-Ie C. Hsing; Ikram Blilou; Alisdair R. Fernie; Salim Al-Babili

doi:10.1038/s42003-021-02740-8

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

Jian You Wang, Saleh Alseekh, Tingting Xiao, Abdugaffor Ablazov, Leonardo Perez de Souza, Valentina Fiorilli, Marita Anggarani, Pei-Yu Lin, Cristina Votta, Mara Novero, Muhammad Jamil, Luisa Lanfranco, Yue-Ie C. Hsing, Ikram Blilou, Alisdair R. Fernie, Salim Al-Babili

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Abstract

AbstractThe 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.

Original language	English (US)
Journal	Communications Biology
Volume	4
Issue number	1
DOIs	https://doi.org/10.1038/s42003-021-02740-8
State	Published - Oct 25 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-10-29
Acknowledged KAUST grant number(s): CRG2017, CRG2020
Acknowledgements: We thank Dr. Kennedy Odokonyero for technical support in photosynthesis experiments and Dr. Hendrik N. J. Kuijer for reading and correcting the manuscript. We are grateful to the KAUST bioscience core lab for RNA-seq, the members of the Bioactives lab in KAUST, members of AG Fernie in MPIMP, and Prof. Anna Fusconi and Prof. Paola Bonfante in the University of Torino for their helpful discussions and assistance. This work was supported by baseline funding and Competitive Research Grants (CRG2017 and CRG2020) given to S.A.-B. from King Abdullah University of Science and Technology (KAUST), and by grants from the European Union’s Horizon 2020 research and innovation programme, project PlantaSYST (SGA-CSA No. 739582 under FPA No. 664620) to A.R.F. and S.A.

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10.1038/s42003-021-02740-8

https://repository.kaust.edu.sa/bitstream/10754/672989/1/s42003-021-02740-8.pdf

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Wang, J. Y., Alseekh, S., Xiao, T., Ablazov, A., de Souza, L. P., Fiorilli, V., Anggarani, M., Lin, P.-Y., Votta, C., Novero, M., Jamil, M., Lanfranco, L., Hsing, Y.-I. C., Blilou, I., Fernie, A. R., & Al-Babili, S. (2021). Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice. Communications Biology, 4(1). https://doi.org/10.1038/s42003-021-02740-8

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title = "Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice",

abstract = "AbstractThe 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.",

author = "Wang, {Jian You} and Saleh Alseekh and Tingting Xiao and Abdugaffor Ablazov and {de Souza}, {Leonardo Perez} and Valentina Fiorilli and Marita Anggarani and Pei-Yu Lin and Cristina Votta and Mara Novero and Muhammad Jamil and Luisa Lanfranco and Hsing, {Yue-Ie C.} and Ikram Blilou and Fernie, {Alisdair R.} and Salim Al-Babili",

note = "KAUST Repository Item: Exported on 2021-10-29 Acknowledged KAUST grant number(s): CRG2017, CRG2020 Acknowledgements: We thank Dr. Kennedy Odokonyero for technical support in photosynthesis experiments and Dr. Hendrik N. J. Kuijer for reading and correcting the manuscript. We are grateful to the KAUST bioscience core lab for RNA-seq, the members of the Bioactives lab in KAUST, members of AG Fernie in MPIMP, and Prof. Anna Fusconi and Prof. Paola Bonfante in the University of Torino for their helpful discussions and assistance. This work was supported by baseline funding and Competitive Research Grants (CRG2017 and CRG2020) given to S.A.-B. from King Abdullah University of Science and Technology (KAUST), and by grants from the European Union{\textquoteright}s Horizon 2020 research and innovation programme, project PlantaSYST (SGA-CSA No. 739582 under FPA No. 664620) to A.R.F. and S.A.",

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doi = "10.1038/s42003-021-02740-8",

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Wang, JY, Alseekh, S, Xiao, T, Ablazov, A, de Souza, LP, Fiorilli, V, Anggarani, M, Lin, P-Y, Votta, C, Novero, M, Jamil, M, Lanfranco, L, Hsing, Y-IC, Blilou, I, Fernie, AR & Al-Babili, S 2021, 'Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice', Communications Biology, vol. 4, no. 1. https://doi.org/10.1038/s42003-021-02740-8

TY - JOUR

T1 - Multi-omics approaches explain the growth-promoting effect of the apocarotenoid growth regulator zaxinone in rice

AU - Wang, Jian You

AU - Alseekh, Saleh

AU - Xiao, Tingting

AU - Ablazov, Abdugaffor

AU - de Souza, Leonardo Perez

AU - Fiorilli, Valentina

AU - Anggarani, Marita

AU - Lin, Pei-Yu

AU - Votta, Cristina

AU - Novero, Mara

AU - Jamil, Muhammad

AU - Lanfranco, Luisa

AU - Hsing, Yue-Ie C.

AU - Blilou, Ikram

AU - Fernie, Alisdair R.

AU - Al-Babili, Salim

N1 - KAUST Repository Item: Exported on 2021-10-29 Acknowledged KAUST grant number(s): CRG2017, CRG2020 Acknowledgements: We thank Dr. Kennedy Odokonyero for technical support in photosynthesis experiments and Dr. Hendrik N. J. Kuijer for reading and correcting the manuscript. We are grateful to the KAUST bioscience core lab for RNA-seq, the members of the Bioactives lab in KAUST, members of AG Fernie in MPIMP, and Prof. Anna Fusconi and Prof. Paola Bonfante in the University of Torino for their helpful discussions and assistance. This work was supported by baseline funding and Competitive Research Grants (CRG2017 and CRG2020) given to S.A.-B. from King Abdullah University of Science and Technology (KAUST), and by grants from the European Union’s Horizon 2020 research and innovation programme, project PlantaSYST (SGA-CSA No. 739582 under FPA No. 664620) to A.R.F. and S.A.

PY - 2021/10/25

Y1 - 2021/10/25

N2 - AbstractThe 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.

AB - AbstractThe 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.

UR - http://hdl.handle.net/10754/672989

UR - https://www.nature.com/articles/s42003-021-02740-8

U2 - 10.1038/s42003-021-02740-8

DO - 10.1038/s42003-021-02740-8

M3 - Article

C2 - 34697384

SN - 2399-3642

VL - 4

JO - Communications Biology

JF - Communications Biology

IS - 1

ER -

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

Abstract

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