Arabidopsis transcription factor ANAC102 predominantly expresses a nuclear protein and acts as a negative regulator of methyl viologen-induced oxidative stress responses
Luo, Xiaopeng ; Jiang, Xinqiang ; Schmitt, Vivian LU ; Kulkarni, Shubhada R. ; Tran, Huy Cuong LU
; Kacprzak, Sylwia M.
LU
; Van Breusegem, Frank
; Van Aken, Olivier
LU
; Vandepoele, Klaas
and De Clercq, Inge
(2024)
In Journal of Experimental Botany
75(15).
p.4655-4670
- 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 β-cyclocitral-mediated chloroplast-to-nucleus signaling, protecting plants against photooxidative stress. However, debates persist... (More)
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 β-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.
(Less)
- author
- Luo, Xiaopeng
; Jiang, Xinqiang
; Schmitt, Vivian
LU
; Kulkarni, Shubhada R.
; Tran, Huy Cuong
LU
; Kacprzak, Sylwia M.
LU
; Van Breusegem, Frank
; Van Aken, Olivier
LU
; Vandepoele, Klaas
and De Clercq, Inge
- organization
- publishing date
- 2024-08
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Arabidopsis, chloroplasts, gene regulatory networks, oxidative stress, retrograde signaling, transcription factors
- in
- Journal of Experimental Botany
- volume
- 75
- issue
- 15
- pages
- 16 pages
- publisher
- Oxford University Press
- external identifiers
-
- pmid:38812358
- scopus:85200941161
- ISSN
- 0022-0957
- DOI
- 10.1093/jxb/erae235
- language
- English
- LU publication?
- yes
- id
- 6336d0c5-777e-4f19-b97f-97f036eca859
- date added to LUP
- 2024-09-09 14:37:16
- date last changed
- 2024-10-07 18:45:20
@article{6336d0c5-777e-4f19-b97f-97f036eca859,
abstract = {{<p>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 β-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.</p>}},
author = {{Luo, Xiaopeng and Jiang, Xinqiang and Schmitt, Vivian and Kulkarni, Shubhada R. 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}},
keywords = {{Arabidopsis; chloroplasts; gene regulatory networks; oxidative stress; retrograde signaling; transcription factors}},
language = {{eng}},
number = {{15}},
pages = {{4655--4670}},
publisher = {{Oxford University Press}},
series = {{Journal of Experimental Botany}},
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://dx.doi.org/10.1093/jxb/erae235}},
doi = {{10.1093/jxb/erae235}},
volume = {{75}},
year = {{2024}},
}