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GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton

Wounded plant cells can form callus to seal the wound site. Alternatively, wounding can cause adventitious organogenesis or somatic embryogenesis. These distinct developmental pathways require specific cell fate decisions. Here, we identify GhTCE1, a basic helix–loop–helix family transcription facto...

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Autores principales: Deng, Jinwu, Sun, Weinan, Zhang, Boyang, Sun, Simin, Xia, Linjie, Miao, Yuhuan, He, Liangrong, Lindsey, Keith, Yang, Xiyan, Zhang, Xianlong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9614502/
https://www.ncbi.nlm.nih.gov/pubmed/35972347
http://dx.doi.org/10.1093/plcell/koac252
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author Deng, Jinwu
Sun, Weinan
Zhang, Boyang
Sun, Simin
Xia, Linjie
Miao, Yuhuan
He, Liangrong
Lindsey, Keith
Yang, Xiyan
Zhang, Xianlong
author_facet Deng, Jinwu
Sun, Weinan
Zhang, Boyang
Sun, Simin
Xia, Linjie
Miao, Yuhuan
He, Liangrong
Lindsey, Keith
Yang, Xiyan
Zhang, Xianlong
author_sort Deng, Jinwu
collection PubMed
description Wounded plant cells can form callus to seal the wound site. Alternatively, wounding can cause adventitious organogenesis or somatic embryogenesis. These distinct developmental pathways require specific cell fate decisions. Here, we identify GhTCE1, a basic helix–loop–helix family transcription factor, and its interacting partners as a central regulatory module of early cell fate transition during in vitro dedifferentiation of cotton (Gossypium hirsutum). RNAi- or CRISPR/Cas9-mediated loss of GhTCE1 function resulted in excessive accumulation of reactive oxygen species (ROS), arrested callus cell elongation, and increased adventitious organogenesis. In contrast, GhTCE1-overexpressing tissues underwent callus cell growth, but organogenesis was repressed. Transcriptome analysis revealed that several pathways depend on proper regulation of GhTCE1 expression, including lipid transfer pathway components, ROS homeostasis, and cell expansion. GhTCE1 bound to the promoters of the target genes GhLTP2 and GhLTP3, activating their expression synergistically, and the heterodimer TCE1-TCEE1 enhances this activity. GhLTP2- and GhLTP3-deficient tissues accumulated ROS and had arrested callus cell elongation, which was restored by ROS scavengers. These results reveal a unique regulatory network involving ROS and lipid transfer proteins, which act as potential ROS scavengers. This network acts as a switch between unorganized callus growth and organized development during in vitro dedifferentiation of cotton cells.
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spelling pubmed-96145022022-11-01 GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton Deng, Jinwu Sun, Weinan Zhang, Boyang Sun, Simin Xia, Linjie Miao, Yuhuan He, Liangrong Lindsey, Keith Yang, Xiyan Zhang, Xianlong Plant Cell Research Articles Wounded plant cells can form callus to seal the wound site. Alternatively, wounding can cause adventitious organogenesis or somatic embryogenesis. These distinct developmental pathways require specific cell fate decisions. Here, we identify GhTCE1, a basic helix–loop–helix family transcription factor, and its interacting partners as a central regulatory module of early cell fate transition during in vitro dedifferentiation of cotton (Gossypium hirsutum). RNAi- or CRISPR/Cas9-mediated loss of GhTCE1 function resulted in excessive accumulation of reactive oxygen species (ROS), arrested callus cell elongation, and increased adventitious organogenesis. In contrast, GhTCE1-overexpressing tissues underwent callus cell growth, but organogenesis was repressed. Transcriptome analysis revealed that several pathways depend on proper regulation of GhTCE1 expression, including lipid transfer pathway components, ROS homeostasis, and cell expansion. GhTCE1 bound to the promoters of the target genes GhLTP2 and GhLTP3, activating their expression synergistically, and the heterodimer TCE1-TCEE1 enhances this activity. GhLTP2- and GhLTP3-deficient tissues accumulated ROS and had arrested callus cell elongation, which was restored by ROS scavengers. These results reveal a unique regulatory network involving ROS and lipid transfer proteins, which act as potential ROS scavengers. This network acts as a switch between unorganized callus growth and organized development during in vitro dedifferentiation of cotton cells. Oxford University Press 2022-08-16 /pmc/articles/PMC9614502/ /pubmed/35972347 http://dx.doi.org/10.1093/plcell/koac252 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Articles
Deng, Jinwu
Sun, Weinan
Zhang, Boyang
Sun, Simin
Xia, Linjie
Miao, Yuhuan
He, Liangrong
Lindsey, Keith
Yang, Xiyan
Zhang, Xianlong
GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title_full GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title_fullStr GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title_full_unstemmed GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title_short GhTCE1–GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
title_sort ghtce1–ghtcee1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9614502/
https://www.ncbi.nlm.nih.gov/pubmed/35972347
http://dx.doi.org/10.1093/plcell/koac252
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