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Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses

(2024) JOURNAL OF EXPERIMENTAL BOTANY. 75(15). p.4655-4670
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Abstract
Plants, being sessile organisms, constantly need to respond to environmental stresses, often leading to the accumulation of reactive oxygen species (ROS). While ROS can be harmful, they also act as second messengers guiding plant growth and stress responses. Because chloroplasts are sensitive to environmental changes and are both a source and a target of ROS during stress conditions, they are important in conveying environmental changes to the nucleus, where acclimation responses are coordinated to maintain organellar and overall cellular homeostasis. ANAC102 has previously been established as a regulator of beta-cyclocitral-mediated chloroplast-to-nucleus signaling, protecting plants against photooxidative stress. However, debates persist about where ANAC102 is located-in chloroplasts or in the nucleus. Our study, utilizing the genomic ANAC102 sequence driven by its native promoter, establishes ANAC102 primarily as a nuclear protein, lacking a complete N-terminal chloroplast-targeting peptide. Moreover, our research reveals the sensitivity of plants overexpressing ANAC102 to severe superoxide-induced chloroplast oxidative stress. Transcriptome analysis unraveled a dual role of ANAC102 in negatively and positively regulating genome-wide transcriptional responses to chloroplast oxidative stress. Through the integration of published data and our own study, we constructed a comprehensive transcriptional network, which suggests that ANAC102 exerts direct and indirect control over transcriptional responses through downstream transcription factor networks, providing deeper insights into the ANAC102-mediated regulatory landscape during oxidative stress. We revealed the multifaceted role of ANAC102 as both a positive and negative regulator of chloroplast oxidative stress responses through complex gene regulatory networks in the nucleus.
Keywords
Arabidopsis, chloroplasts, gene regulatory networks, oxidative stress, retrograde signaling, transcription factors, GENE-EXPRESSION, PLANT, OXYGEN, MITOCHONDRIAL, LOCALIZATION, REPRESSES, CYTOSCAPE, REVEALS, SIGNALS, PATHWAY

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Citation

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MLA
Luo, Xiaopeng, et al. “Arabidopsis Transcription Factor ANAC102 Predominantly Expresses a Nuclear Protein and Acts as a Negative Regulator of Methyl Viologen-Induced Oxidative Stress Responses.” JOURNAL OF EXPERIMENTAL BOTANY, vol. 75, no. 15, 2024, pp. 4655–70, doi:10.1093/jxb/erae235.
APA
Luo, X., Jiang, X., Schmitt, V., Kulkarni, S. R., Tran, H. C., Kacprzak, S. M., … De Clercq, I. (2024). Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses. JOURNAL OF EXPERIMENTAL BOTANY, 75(15), 4655–4670. https://doi.org/10.1093/jxb/erae235
Chicago author-date
Luo, Xiaopeng, Xinqiang Jiang, Vivian Schmitt, Shubhada Rajabhau Kulkarni, Huy Cuong Tran, Sylwia M Kacprzak, Frank Van Breusegem, Olivier Van Aken, Klaas Vandepoele, and Inge De Clercq. 2024. “Arabidopsis Transcription Factor ANAC102 Predominantly Expresses a Nuclear Protein and Acts as a Negative Regulator of Methyl Viologen-Induced Oxidative Stress Responses.” JOURNAL OF EXPERIMENTAL BOTANY 75 (15): 4655–70. https://doi.org/10.1093/jxb/erae235.
Chicago author-date (all authors)
Luo, Xiaopeng, Xinqiang Jiang, Vivian Schmitt, Shubhada Rajabhau Kulkarni, Huy Cuong Tran, Sylwia M Kacprzak, Frank Van Breusegem, Olivier Van Aken, Klaas Vandepoele, and Inge De Clercq. 2024. “Arabidopsis Transcription Factor ANAC102 Predominantly Expresses a Nuclear Protein and Acts as a Negative Regulator of Methyl Viologen-Induced Oxidative Stress Responses.” JOURNAL OF EXPERIMENTAL BOTANY 75 (15): 4655–4670. doi:10.1093/jxb/erae235.
Vancouver
1.
Luo X, Jiang X, Schmitt V, Kulkarni SR, Tran HC, Kacprzak SM, et al. Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses. JOURNAL OF EXPERIMENTAL BOTANY. 2024;75(15):4655–70.
IEEE
[1]
X. Luo et al., “Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses,” JOURNAL OF EXPERIMENTAL BOTANY, vol. 75, no. 15, pp. 4655–4670, 2024.
@article{01J03DCHVJWKHNGHYN4TERP602,
  abstract     = {{Plants, being sessile organisms, constantly need to respond to environmental stresses, often leading to the accumulation of reactive oxygen species (ROS). While ROS can be harmful, they also act as second messengers guiding plant growth and stress responses. Because chloroplasts are sensitive to environmental changes and are both a source and a target of ROS during stress conditions, they are important in conveying environmental changes to the nucleus, where acclimation responses are coordinated to maintain organellar and overall cellular homeostasis. ANAC102 has previously been established as a regulator of beta-cyclocitral-mediated chloroplast-to-nucleus signaling, protecting plants against photooxidative stress. However, debates persist about where ANAC102 is located-in chloroplasts or in the nucleus. Our study, utilizing the genomic ANAC102 sequence driven by its native promoter, establishes ANAC102 primarily as a nuclear protein, lacking a complete N-terminal chloroplast-targeting peptide. Moreover, our research reveals the sensitivity of plants overexpressing ANAC102 to severe superoxide-induced chloroplast oxidative stress. Transcriptome analysis unraveled a dual role of ANAC102 in negatively and positively regulating genome-wide transcriptional responses to chloroplast oxidative stress. Through the integration of published data and our own study, we constructed a comprehensive transcriptional network, which suggests that ANAC102 exerts direct and indirect control over transcriptional responses through downstream transcription factor networks, providing deeper insights into the ANAC102-mediated regulatory landscape during oxidative stress.

We revealed the multifaceted role of ANAC102 as both a positive and negative regulator of chloroplast oxidative stress responses through complex gene regulatory networks in the nucleus.}},
  author       = {{Luo, Xiaopeng and Jiang, Xinqiang and Schmitt, Vivian and Kulkarni, Shubhada Rajabhau and Tran, Huy Cuong and Kacprzak, Sylwia M and Van Breusegem, Frank and Van Aken, Olivier and Vandepoele, Klaas and De Clercq, Inge}},
  issn         = {{0022-0957}},
  journal      = {{JOURNAL OF EXPERIMENTAL BOTANY}},
  keywords     = {{Arabidopsis,chloroplasts,gene regulatory networks,oxidative stress,retrograde signaling,transcription factors,GENE-EXPRESSION,PLANT,OXYGEN,MITOCHONDRIAL,LOCALIZATION,REPRESSES,CYTOSCAPE,REVEALS,SIGNALS,PATHWAY}},
  language     = {{eng}},
  number       = {{15}},
  pages        = {{4655--4670}},
  title        = {{Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses}},
  url          = {{http://doi.org/10.1093/jxb/erae235}},
  volume       = {{75}},
  year         = {{2024}},
}

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