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Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana

WUSCHEL (WUS) is a crucial transcription factor in regulating plant stem cell development, and its expression can also improve genetic transformation. However, the ectopic expression of WUS always causes pleiotropic effects during genetic transformation, making it important to understand the regulat...

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Autores principales: Zhang, Xianwen, Liang, Shuang, Luo, Biao, Zhou, Zhongjing, Bao, Jiandong, Fang, Ruiqiu, Wang, Fang, Song, Xijiao, Liao, Zhenfeng, Chen, Guang, Wang, Yan, Xu, Fei, Teng, Yi, Li, Wanchang, Xu, Shengchun, Lin, Fu-Cheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10342293/
https://www.ncbi.nlm.nih.gov/pubmed/37446367
http://dx.doi.org/10.3390/ijms241311190
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author Zhang, Xianwen
Liang, Shuang
Luo, Biao
Zhou, Zhongjing
Bao, Jiandong
Fang, Ruiqiu
Wang, Fang
Song, Xijiao
Liao, Zhenfeng
Chen, Guang
Wang, Yan
Xu, Fei
Teng, Yi
Li, Wanchang
Xu, Shengchun
Lin, Fu-Cheng
author_facet Zhang, Xianwen
Liang, Shuang
Luo, Biao
Zhou, Zhongjing
Bao, Jiandong
Fang, Ruiqiu
Wang, Fang
Song, Xijiao
Liao, Zhenfeng
Chen, Guang
Wang, Yan
Xu, Fei
Teng, Yi
Li, Wanchang
Xu, Shengchun
Lin, Fu-Cheng
author_sort Zhang, Xianwen
collection PubMed
description WUSCHEL (WUS) is a crucial transcription factor in regulating plant stem cell development, and its expression can also improve genetic transformation. However, the ectopic expression of WUS always causes pleiotropic effects during genetic transformation, making it important to understand the regulatory mechanisms underlying these phenomena. In our study, we found that the transient expression of the maize WUS ortholog ZmWus2 caused severe leaf necrosis in Nicotiana benthamiana. We performed transcriptomic and non-target metabolomic analyses on tobacco leaves during healthy to wilted states after ZmWus2 transient overexpression. Transcriptomic analysis revealed that ZmWus2 transformation caused active metabolism of inositol trisphosphate and glycerol-3-phosphate, while also upregulating plant hormone signaling and downregulating photosystem and protein folding pathways. Metabolomic analysis mainly identified changes in the synthesis of phenylpropanoid compounds and various lipid classes, including steroid synthesis. In addition, transcription factors such as ethylene-responsive factors (ERFs), the basic helix–loop–helix (bHLH) factors, and MYBs were found to be regulated by ZmWus2. By integrating these findings, we developed a WUS regulatory model that includes plant hormone accumulation, stress responses, lipid remodeling, and leaf necrosis. Our study sheds light on the mechanisms underlying WUS ectopic expression causing leaf necrosis and may inform the development of future genetic transformation strategies.
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spelling pubmed-103422932023-07-14 Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana Zhang, Xianwen Liang, Shuang Luo, Biao Zhou, Zhongjing Bao, Jiandong Fang, Ruiqiu Wang, Fang Song, Xijiao Liao, Zhenfeng Chen, Guang Wang, Yan Xu, Fei Teng, Yi Li, Wanchang Xu, Shengchun Lin, Fu-Cheng Int J Mol Sci Article WUSCHEL (WUS) is a crucial transcription factor in regulating plant stem cell development, and its expression can also improve genetic transformation. However, the ectopic expression of WUS always causes pleiotropic effects during genetic transformation, making it important to understand the regulatory mechanisms underlying these phenomena. In our study, we found that the transient expression of the maize WUS ortholog ZmWus2 caused severe leaf necrosis in Nicotiana benthamiana. We performed transcriptomic and non-target metabolomic analyses on tobacco leaves during healthy to wilted states after ZmWus2 transient overexpression. Transcriptomic analysis revealed that ZmWus2 transformation caused active metabolism of inositol trisphosphate and glycerol-3-phosphate, while also upregulating plant hormone signaling and downregulating photosystem and protein folding pathways. Metabolomic analysis mainly identified changes in the synthesis of phenylpropanoid compounds and various lipid classes, including steroid synthesis. In addition, transcription factors such as ethylene-responsive factors (ERFs), the basic helix–loop–helix (bHLH) factors, and MYBs were found to be regulated by ZmWus2. By integrating these findings, we developed a WUS regulatory model that includes plant hormone accumulation, stress responses, lipid remodeling, and leaf necrosis. Our study sheds light on the mechanisms underlying WUS ectopic expression causing leaf necrosis and may inform the development of future genetic transformation strategies. MDPI 2023-07-07 /pmc/articles/PMC10342293/ /pubmed/37446367 http://dx.doi.org/10.3390/ijms241311190 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Zhang, Xianwen
Liang, Shuang
Luo, Biao
Zhou, Zhongjing
Bao, Jiandong
Fang, Ruiqiu
Wang, Fang
Song, Xijiao
Liao, Zhenfeng
Chen, Guang
Wang, Yan
Xu, Fei
Teng, Yi
Li, Wanchang
Xu, Shengchun
Lin, Fu-Cheng
Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title_full Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title_fullStr Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title_full_unstemmed Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title_short Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by ZmWus2 Transient Overexpression in Nicotiana benthamiana
title_sort transcriptomic and metabolomic investigation on leaf necrosis induced by zmwus2 transient overexpression in nicotiana benthamiana
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10342293/
https://www.ncbi.nlm.nih.gov/pubmed/37446367
http://dx.doi.org/10.3390/ijms241311190
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