Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling
Plants release chemicals to deter attackers. Arabidopsis thaliana relies on multiple defense compounds, including indol-3-ylmethyl glucosinolate (I3G), which upon hydrolysis initiated by myrosinase enzymes releases a multitude of bioactive compounds, among others, indole-3-acetonitrile and indole-3-...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-04-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2018.00550/full |
| _version_ | 1819030878719836160 |
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| author | Daniel Vik Namiko Mitarai Nikolai Wulff Barbara A. Halkier Meike Burow |
| author_facet | Daniel Vik Namiko Mitarai Nikolai Wulff Barbara A. Halkier Meike Burow |
| author_sort | Daniel Vik |
| collection | DOAJ |
| description | Plants release chemicals to deter attackers. Arabidopsis thaliana relies on multiple defense compounds, including indol-3-ylmethyl glucosinolate (I3G), which upon hydrolysis initiated by myrosinase enzymes releases a multitude of bioactive compounds, among others, indole-3-acetonitrile and indole-3-acetoisothiocyanate. The highly unstable isothiocyanate rapidly reacts with other molecules. One of the products, indole-3-carbinol, was reported to inhibit auxin signaling through binding to the TIR1 auxin receptor. On the contrary, the nitrile product of I3G hydrolysis can be converted by nitrilase enzymes to form the primary auxin molecule, indole-3-acetic acid, which activates TIR1. This suggests that auxin signaling is subject to both antagonistic and protagonistic effects of I3G hydrolysis upon attack. We hypothesize that I3G hydrolysis and auxin signaling form an incoherent feedforward loop and we build a mathematical model to examine the regulatory network dynamics. We use molecular docking to investigate the possible antagonistic properties of different I3G hydrolysis products by competitive binding to the TIR1 receptor. Our simulations reveal an uncoupling of auxin concentration and signaling, and we determine that enzyme activity and antagonist binding affinity are key parameters for this uncoupling. The molecular docking predicts that several I3G hydrolysis products strongly antagonize auxin signaling. By comparing a tissue disrupting attack – e.g., by chewing insects or necrotrophic pathogens that causes rapid release of I3G hydrolysis products – to sustained cell-autonomous I3G hydrolysis, e.g., upon infection by biotrophic pathogens, we find that each scenario gives rise to distinct auxin signaling dynamics. This suggests that plants have different defense versus growth strategies depending on the nature of the attack. |
| first_indexed | 2024-12-21T06:37:09Z |
| format | Article |
| id | doaj.art-5795b3250f5749268b638c89f666b87f |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-21T06:37:09Z |
| publishDate | 2018-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-5795b3250f5749268b638c89f666b87f2022-12-21T19:12:49ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-04-01910.3389/fpls.2018.00550330180Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin SignalingDaniel Vik0Namiko Mitarai1Nikolai Wulff2Barbara A. Halkier3Meike Burow4DynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkCenter for Models of Life, Niels Bohr Institute, University of Copenhagen, Copenhagen, DenmarkDynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkDynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkDynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkPlants release chemicals to deter attackers. Arabidopsis thaliana relies on multiple defense compounds, including indol-3-ylmethyl glucosinolate (I3G), which upon hydrolysis initiated by myrosinase enzymes releases a multitude of bioactive compounds, among others, indole-3-acetonitrile and indole-3-acetoisothiocyanate. The highly unstable isothiocyanate rapidly reacts with other molecules. One of the products, indole-3-carbinol, was reported to inhibit auxin signaling through binding to the TIR1 auxin receptor. On the contrary, the nitrile product of I3G hydrolysis can be converted by nitrilase enzymes to form the primary auxin molecule, indole-3-acetic acid, which activates TIR1. This suggests that auxin signaling is subject to both antagonistic and protagonistic effects of I3G hydrolysis upon attack. We hypothesize that I3G hydrolysis and auxin signaling form an incoherent feedforward loop and we build a mathematical model to examine the regulatory network dynamics. We use molecular docking to investigate the possible antagonistic properties of different I3G hydrolysis products by competitive binding to the TIR1 receptor. Our simulations reveal an uncoupling of auxin concentration and signaling, and we determine that enzyme activity and antagonist binding affinity are key parameters for this uncoupling. The molecular docking predicts that several I3G hydrolysis products strongly antagonize auxin signaling. By comparing a tissue disrupting attack – e.g., by chewing insects or necrotrophic pathogens that causes rapid release of I3G hydrolysis products – to sustained cell-autonomous I3G hydrolysis, e.g., upon infection by biotrophic pathogens, we find that each scenario gives rise to distinct auxin signaling dynamics. This suggests that plants have different defense versus growth strategies depending on the nature of the attack.http://journal.frontiersin.org/article/10.3389/fpls.2018.00550/fullmathematical modelingindole glucosinolate hydrolysisauxin signalingmyrosinasesspecifier proteinnitrilase |
| spellingShingle | Daniel Vik Namiko Mitarai Nikolai Wulff Barbara A. Halkier Meike Burow Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling Frontiers in Plant Science mathematical modeling indole glucosinolate hydrolysis auxin signaling myrosinases specifier protein nitrilase |
| title | Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling |
| title_full | Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling |
| title_fullStr | Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling |
| title_full_unstemmed | Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling |
| title_short | Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling |
| title_sort | dynamic modeling of indole glucosinolate hydrolysis and its impact on auxin signaling |
| topic | mathematical modeling indole glucosinolate hydrolysis auxin signaling myrosinases specifier protein nitrilase |
| url | http://journal.frontiersin.org/article/10.3389/fpls.2018.00550/full |
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