Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i>
<i>WUSCHEL</i> (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 und...
| Main Authors: | , , , , , , , , , , , , , , , |
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MDPI AG
2023-07-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/13/11190 |
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| author | Xianwen Zhang Shuang Liang Biao Luo Zhongjing Zhou Jiandong Bao Ruiqiu Fang Fang Wang Xijiao Song Zhenfeng Liao Guang Chen Yan Wang Fei Xu Yi Teng Wanchang Li Shengchun Xu Fu-Cheng Lin |
| author_facet | Xianwen Zhang Shuang Liang Biao Luo Zhongjing Zhou Jiandong Bao Ruiqiu Fang Fang Wang Xijiao Song Zhenfeng Liao Guang Chen Yan Wang Fei Xu Yi Teng Wanchang Li Shengchun Xu Fu-Cheng Lin |
| author_sort | Xianwen Zhang |
| collection | DOAJ |
| description | <i>WUSCHEL</i> (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 <i>ZmWus2</i> caused severe leaf necrosis in <i>Nicotiana benthamiana</i>. We performed transcriptomic and non-target metabolomic analyses on tobacco leaves during healthy to wilted states after <i>ZmWus2</i> transient overexpression. Transcriptomic analysis revealed that <i>ZmWus2</i> 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 <i>ZmWus2</i>. 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. |
| first_indexed | 2024-03-11T01:37:48Z |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T01:37:48Z |
| publishDate | 2023-07-01 |
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| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-1e50ecf175834955a6ec5ec811d20bd02023-11-18T16:49:26ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-07-0124131119010.3390/ijms241311190Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i>Xianwen Zhang0Shuang Liang1Biao Luo2Zhongjing Zhou3Jiandong Bao4Ruiqiu Fang5Fang Wang6Xijiao Song7Zhenfeng Liao8Guang Chen9Yan Wang10Fei Xu11Yi Teng12Wanchang Li13Shengchun Xu14Fu-Cheng Lin15Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaInstitute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaInstitute of Maize and Featured Upland Crops, Zhejiang Academy of Agricultural Sciences, Dongyang 322100, ChinaInstitute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaInstitute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaInstitute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China<i>WUSCHEL</i> (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 <i>ZmWus2</i> caused severe leaf necrosis in <i>Nicotiana benthamiana</i>. We performed transcriptomic and non-target metabolomic analyses on tobacco leaves during healthy to wilted states after <i>ZmWus2</i> transient overexpression. Transcriptomic analysis revealed that <i>ZmWus2</i> 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 <i>ZmWus2</i>. 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.https://www.mdpi.com/1422-0067/24/13/11190<i>WUSCHEL</i>necrosistranscriptomicsmetabolomicstobaccoplant transgenic technology |
| spellingShingle | Xianwen Zhang Shuang Liang Biao Luo Zhongjing Zhou Jiandong Bao Ruiqiu Fang Fang Wang Xijiao Song Zhenfeng Liao Guang Chen Yan Wang Fei Xu Yi Teng Wanchang Li Shengchun Xu Fu-Cheng Lin Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> International Journal of Molecular Sciences <i>WUSCHEL</i> necrosis transcriptomics metabolomics tobacco plant transgenic technology |
| title | Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> |
| title_full | Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> |
| title_fullStr | Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> |
| title_full_unstemmed | Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> |
| title_short | Transcriptomic and Metabolomic Investigation on Leaf Necrosis Induced by <i>ZmWus2</i> Transient Overexpression in <i>Nicotiana benthamiana</i> |
| title_sort | transcriptomic and metabolomic investigation on leaf necrosis induced by i zmwus2 i transient overexpression in i nicotiana benthamiana i |
| topic | <i>WUSCHEL</i> necrosis transcriptomics metabolomics tobacco plant transgenic technology |
| url | https://www.mdpi.com/1422-0067/24/13/11190 |
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