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Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways

Cross-regulation between hormone signaling pathways is indispensable for plant growth and development. However, the molecular mechanisms by which multiple hormones interact and co-ordinate activity need to be understood. Here, we generated a cross-regulation network explaining how hormone signals ar...

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Autores principales: Yin, Lingling, Zander, Mark, Huang, Shao-shan Carol, Xie, Mingtang, Song, Liang, Saldierna Guzmán, J. Paola, Hann, Elizabeth, Shanbhag, Bhuvana K., Ng, Sophia, Jain, Siddhartha, Janssen, Bart J., Clark, Natalie M., Walley, Justin W., Beddoe, Travis, Bar-Joseph, Ziv, Lewsey, Mathew G., Ecker, Joseph R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028877/
https://www.ncbi.nlm.nih.gov/pubmed/36945593
http://dx.doi.org/10.1101/2023.03.07.531630
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author Yin, Lingling
Zander, Mark
Huang, Shao-shan Carol
Xie, Mingtang
Song, Liang
Saldierna Guzmán, J. Paola
Hann, Elizabeth
Shanbhag, Bhuvana K.
Ng, Sophia
Jain, Siddhartha
Janssen, Bart J.
Clark, Natalie M.
Walley, Justin W.
Beddoe, Travis
Bar-Joseph, Ziv
Lewsey, Mathew G.
Ecker, Joseph R.
author_facet Yin, Lingling
Zander, Mark
Huang, Shao-shan Carol
Xie, Mingtang
Song, Liang
Saldierna Guzmán, J. Paola
Hann, Elizabeth
Shanbhag, Bhuvana K.
Ng, Sophia
Jain, Siddhartha
Janssen, Bart J.
Clark, Natalie M.
Walley, Justin W.
Beddoe, Travis
Bar-Joseph, Ziv
Lewsey, Mathew G.
Ecker, Joseph R.
author_sort Yin, Lingling
collection PubMed
description Cross-regulation between hormone signaling pathways is indispensable for plant growth and development. However, the molecular mechanisms by which multiple hormones interact and co-ordinate activity need to be understood. Here, we generated a cross-regulation network explaining how hormone signals are integrated from multiple pathways in etiolated Arabidopsis (Arabidopsis thaliana) seedlings. To do so we comprehensively characterized transcription factor activity during plant hormone responses and reconstructed dynamic transcriptional regulatory models for six hormones; abscisic acid, brassinosteroid, ethylene, jasmonic acid, salicylic acid and strigolactone/karrikin. These models incorporated target data for hundreds of transcription factors and thousands of protein-protein interactions. Each hormone recruited different combinations of transcription factors, a subset of which were shared between hormones. Hub target genes existed within hormone transcriptional networks, exhibiting transcription factor activity themselves. In addition, a group of MITOGEN-ACTIVATED PROTEIN KINASES (MPKs) were identified as potential key points of cross-regulation between multiple hormones. Accordingly, the loss of function of one of these (MPK6) disrupted the global proteome, phosphoproteome and transcriptome during hormone responses. Lastly, we determined that all hormones drive substantial alternative splicing that has distinct effects on the transcriptome compared with differential gene expression, acting in early hormone responses. These results provide a comprehensive understanding of the common features of plant transcriptional regulatory pathways and how cross-regulation between hormones acts upon gene expression.
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spelling pubmed-100288772023-03-22 Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways Yin, Lingling Zander, Mark Huang, Shao-shan Carol Xie, Mingtang Song, Liang Saldierna Guzmán, J. Paola Hann, Elizabeth Shanbhag, Bhuvana K. Ng, Sophia Jain, Siddhartha Janssen, Bart J. Clark, Natalie M. Walley, Justin W. Beddoe, Travis Bar-Joseph, Ziv Lewsey, Mathew G. Ecker, Joseph R. bioRxiv Article Cross-regulation between hormone signaling pathways is indispensable for plant growth and development. However, the molecular mechanisms by which multiple hormones interact and co-ordinate activity need to be understood. Here, we generated a cross-regulation network explaining how hormone signals are integrated from multiple pathways in etiolated Arabidopsis (Arabidopsis thaliana) seedlings. To do so we comprehensively characterized transcription factor activity during plant hormone responses and reconstructed dynamic transcriptional regulatory models for six hormones; abscisic acid, brassinosteroid, ethylene, jasmonic acid, salicylic acid and strigolactone/karrikin. These models incorporated target data for hundreds of transcription factors and thousands of protein-protein interactions. Each hormone recruited different combinations of transcription factors, a subset of which were shared between hormones. Hub target genes existed within hormone transcriptional networks, exhibiting transcription factor activity themselves. In addition, a group of MITOGEN-ACTIVATED PROTEIN KINASES (MPKs) were identified as potential key points of cross-regulation between multiple hormones. Accordingly, the loss of function of one of these (MPK6) disrupted the global proteome, phosphoproteome and transcriptome during hormone responses. Lastly, we determined that all hormones drive substantial alternative splicing that has distinct effects on the transcriptome compared with differential gene expression, acting in early hormone responses. These results provide a comprehensive understanding of the common features of plant transcriptional regulatory pathways and how cross-regulation between hormones acts upon gene expression. Cold Spring Harbor Laboratory 2023-03-09 /pmc/articles/PMC10028877/ /pubmed/36945593 http://dx.doi.org/10.1101/2023.03.07.531630 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Yin, Lingling
Zander, Mark
Huang, Shao-shan Carol
Xie, Mingtang
Song, Liang
Saldierna Guzmán, J. Paola
Hann, Elizabeth
Shanbhag, Bhuvana K.
Ng, Sophia
Jain, Siddhartha
Janssen, Bart J.
Clark, Natalie M.
Walley, Justin W.
Beddoe, Travis
Bar-Joseph, Ziv
Lewsey, Mathew G.
Ecker, Joseph R.
Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title_full Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title_fullStr Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title_full_unstemmed Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title_short Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways
title_sort transcription factor dynamics in cross-regulation of plant hormone signaling pathways
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028877/
https://www.ncbi.nlm.nih.gov/pubmed/36945593
http://dx.doi.org/10.1101/2023.03.07.531630
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