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ACCERBATIN, a small molecule at the intersection of auxin and reactive oxygen species homeostasis with herbicidal properties

Yuming Hu, Thomas Depaepe UGent, Dajo Smet UGent, Klara Hoyerova, Petr Klima, Ann Cuypers, Sean Cutler, Dieter Buyst UGent, Kris Morreel UGent, Wout Boerjan UGent, et al. (2017) JOURNAL OF EXPERIMENTAL BOTANY. 68(15). p.4185-4203
abstract
The volatile two-carbon hormone ethylene acts in concert with an array of signals to affect etiolated seedling development. From a chemical screen, we isolated a quinoline carboxamide designated ACCERBATIN (AEX) that exacerbates the 1-aminocyclopropane-1-carboxylic acid-induced triple response, typical for ethylene-treated seedlings in darkness. Phenotypic analyses revealed distinct AEX effects including inhibition of root hair development and shortening of the root meristem. Mutant analysis and reporter studies further suggested that AEX most probably acts in parallel to ethylene signaling. We demonstrated that AEX functions at the intersection of auxin metabolism and reactive oxygen species (ROS) homeostasis. AEX inhibited auxin efflux in BY-2 cells and promoted indole-3-acetic acid (IAA) oxidation in the shoot apical meristem and cotyledons of etiolated seedlings. Gene expression studies and superoxide/hydrogen peroxide staining further revealed that the disrupted auxin homeostasis was accompanied by oxidative stress. Interestingly, in light conditions, AEX exhibited properties reminiscent of the quinoline carboxylate-type auxin-like herbicides. We propose that AEX interferes with auxin transport from its major biosynthesis sites, either as a direct consequence of poor basipetal transport from the shoot meristematic region, or indirectly, through excessive IAA oxidation and ROS accumulation. Further investigation of AEX can provide new insights into the mechanisms connecting auxin and ROS homeostasis in plant development and provide useful tools to study auxin-type herbicides.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
APICAL HOOK DEVELOPMENT, ROOT HAIR DEVELOPMENT, ARABIDOPSIS-THALIANA, SEEDLINGS, ETHYLENE BIOSYNTHESIS, SHOOT GRAVITROPISM, CELL ELONGATION, ABIOTIC STRESS, ABSCISIC-ACID, PLANT-GROWTH, GENE FAMILY, Arabidopsis, auxin homeostasis, chemical genetics, ethylene signaling, herbicide, quinoline carboxamide, reactive oxygen species, triple, response
journal title
JOURNAL OF EXPERIMENTAL BOTANY
J. Exp. Bot.
volume
68
issue
15
pages
4185 - 4203
Web of Science type
Article
Web of Science id
000410245700017
ISSN
0022-0957
1460-2431
DOI
10.1093/jxb/erx242
language
English
UGent publication?
yes
classification
A1
additional info
the first two authors contributed equally to this work
copyright statement
Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
id
8533289
handle
http://hdl.handle.net/1854/LU-8533289
date created
2017-10-05 12:43:25
date last changed
2017-11-16 14:29:36
@article{8533289,
  abstract     = {The volatile two-carbon hormone ethylene acts in concert with an array of signals to affect etiolated seedling development. From a chemical screen, we isolated a quinoline carboxamide designated ACCERBATIN (AEX) that exacerbates the 1-aminocyclopropane-1-carboxylic acid-induced triple response, typical for ethylene-treated seedlings in darkness. Phenotypic analyses revealed distinct AEX effects including inhibition of root hair development and shortening of the root meristem. Mutant analysis and reporter studies further suggested that AEX most probably acts in parallel to ethylene signaling. We demonstrated that AEX functions at the intersection of auxin metabolism and reactive oxygen species (ROS) homeostasis. AEX inhibited auxin efflux in BY-2 cells and promoted indole-3-acetic acid (IAA) oxidation in the shoot apical meristem and cotyledons of etiolated seedlings. Gene expression studies and superoxide/hydrogen peroxide staining further revealed that the disrupted auxin homeostasis was accompanied by oxidative stress. Interestingly, in light conditions, AEX exhibited properties reminiscent of the quinoline carboxylate-type auxin-like herbicides. We propose that AEX interferes with auxin transport from its major biosynthesis sites, either as a direct consequence of poor basipetal transport from the shoot meristematic region, or indirectly, through excessive IAA oxidation and ROS accumulation. Further investigation of AEX can provide new insights into the mechanisms connecting auxin and ROS homeostasis in plant development and provide useful tools to study auxin-type herbicides.},
  author       = {Hu, Yuming and Depaepe, Thomas and Smet, Dajo and Hoyerova, Klara and Klima, Petr and Cuypers, Ann and Cutler, Sean and Buyst, Dieter and Morreel, Kris and Boerjan, Wout and Martins, Jos{\'e} and Petrasek, Jan and Vandenbussche, Filip and Van Der Straeten, Dominique},
  issn         = {0022-0957},
  journal      = {JOURNAL OF EXPERIMENTAL BOTANY},
  keyword      = {APICAL HOOK DEVELOPMENT,ROOT HAIR DEVELOPMENT,ARABIDOPSIS-THALIANA,SEEDLINGS,ETHYLENE BIOSYNTHESIS,SHOOT GRAVITROPISM,CELL ELONGATION,ABIOTIC STRESS,ABSCISIC-ACID,PLANT-GROWTH,GENE FAMILY,Arabidopsis,auxin homeostasis,chemical genetics,ethylene signaling,herbicide,quinoline carboxamide,reactive oxygen species,triple,response},
  language     = {eng},
  number       = {15},
  pages        = {4185--4203},
  title        = {ACCERBATIN, a small molecule at the intersection of auxin and reactive oxygen species homeostasis with herbicidal properties},
  url          = {http://dx.doi.org/10.1093/jxb/erx242},
  volume       = {68},
  year         = {2017},
}

Chicago
Hu, Yuming, Thomas Depaepe, Dajo Smet, Klara Hoyerova, Petr Klima, Ann Cuypers, Sean Cutler, et al. 2017. “ACCERBATIN, a Small Molecule at the Intersection of Auxin and Reactive Oxygen Species Homeostasis with Herbicidal Properties.” Journal of Experimental Botany 68 (15): 4185–4203.
APA
Hu, Yuming, Depaepe, T., Smet, D., Hoyerova, K., Klima, P., Cuypers, A., Cutler, S., et al. (2017). ACCERBATIN, a small molecule at the intersection of auxin and reactive oxygen species homeostasis with herbicidal properties. JOURNAL OF EXPERIMENTAL BOTANY, 68(15), 4185–4203.
Vancouver
1.
Hu Y, Depaepe T, Smet D, Hoyerova K, Klima P, Cuypers A, et al. ACCERBATIN, a small molecule at the intersection of auxin and reactive oxygen species homeostasis with herbicidal properties. JOURNAL OF EXPERIMENTAL BOTANY. 2017;68(15):4185–203.
MLA
Hu, Yuming, Thomas Depaepe, Dajo Smet, et al. “ACCERBATIN, a Small Molecule at the Intersection of Auxin and Reactive Oxygen Species Homeostasis with Herbicidal Properties.” JOURNAL OF EXPERIMENTAL BOTANY 68.15 (2017): 4185–4203. Print.