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Modelling and experimental analysis of hormonal crosstalk in Arabidopsis.

Liu J, Mehdi S, Topping J, Tarkowski P, Lindsey K - Mol. Syst. Biol. (2010)

Bottom Line: Modelling correctly predicts experimental results for the effect of the pls gene mutation on endogenous cytokinin concentration.Modelling further reveals that a bell-shaped dose-response relationship between endogenous auxin and root length is established via PLS.This combined modelling and experimental analysis provides new insights into the integration of hormonal signals in plants.

View Article: PubMed Central - PubMed

Affiliation: The Integrative Cell Biology Laboratory and The Biophysical Sciences Institute, School of Biological and Biomedical Sciences, Durham University, Durham, UK. junli.liu@durham.ac.uk

ABSTRACT
An important question in plant biology is how genes influence the crosstalk between hormones to regulate growth. In this study, we model POLARIS (PLS) gene function and crosstalk between auxin, ethylene and cytokinin in Arabidopsis. Experimental evidence suggests that PLS acts on or close to the ethylene receptor ETR1, and a mathematical model describing possible PLS-ethylene pathway interactions is developed, and used to make quantitative predictions about PLS-hormone interactions. Modelling correctly predicts experimental results for the effect of the pls gene mutation on endogenous cytokinin concentration. Modelling also reveals a role for PLS in auxin biosynthesis in addition to a role in auxin transport. The model reproduces available mutants, and with new experimental data provides new insights into how PLS regulates auxin concentration, by controlling the relative contribution of auxin transport and biosynthesis and by integrating auxin, ethylene and cytokinin signalling. Modelling further reveals that a bell-shaped dose-response relationship between endogenous auxin and root length is established via PLS. This combined modelling and experimental analysis provides new insights into the integration of hormonal signals in plants.

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PLS-mediated control of auxin concentration. (A) Effects of both PLS transcription and interaction of ethylene with its receptor on auxin concentration; (B) effects of both exogenous ACC and PLS transcription on auxin concentration. In pls mutant, auxin concentration decreases from 0.14 to 0.12 μM as exogenous ACC concentration increases from 0 to 10 μM. (C) Effects of both exogenous ACC and PLS transcription on auxin transport and biosynthesis; (D) effects of both PLS transcription and interaction of ethylene with its receptor on auxin transport and biosynthesis; (E) effects of PLS transcription on endogenous ethylene concentration; (F) filled bar: modelling results; unfilled bar: experimental measurements (Chilley et al, 2006). wt: k6=0.3 s−1; k11=5 μM−1 s−1; pls: k6=0.0 s−1; k11=5 μM−1 s−1. pls etr1-1: k6=0.0 s−1; k11=0.03 μM−1 s−1. PLSox: k6=1.0 s−1; k11=5 μM−1 s−1. PLSox ETR1-1ox: k6=0.45 s−1; k11=10 μM−1 s−1. PLSox etr1-1: k6=0.45 s−1; k11=0.03 μM−1 s−1. (G) Analysis of the effects of both CTR1 and PLS transcription. Auxin concentration for total CTR1 concentration to be 0.3 μM (wt) is also included for comparison.
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f5: PLS-mediated control of auxin concentration. (A) Effects of both PLS transcription and interaction of ethylene with its receptor on auxin concentration; (B) effects of both exogenous ACC and PLS transcription on auxin concentration. In pls mutant, auxin concentration decreases from 0.14 to 0.12 μM as exogenous ACC concentration increases from 0 to 10 μM. (C) Effects of both exogenous ACC and PLS transcription on auxin transport and biosynthesis; (D) effects of both PLS transcription and interaction of ethylene with its receptor on auxin transport and biosynthesis; (E) effects of PLS transcription on endogenous ethylene concentration; (F) filled bar: modelling results; unfilled bar: experimental measurements (Chilley et al, 2006). wt: k6=0.3 s−1; k11=5 μM−1 s−1; pls: k6=0.0 s−1; k11=5 μM−1 s−1. pls etr1-1: k6=0.0 s−1; k11=0.03 μM−1 s−1. PLSox: k6=1.0 s−1; k11=5 μM−1 s−1. PLSox ETR1-1ox: k6=0.45 s−1; k11=10 μM−1 s−1. PLSox etr1-1: k6=0.45 s−1; k11=0.03 μM−1 s−1. (G) Analysis of the effects of both CTR1 and PLS transcription. Auxin concentration for total CTR1 concentration to be 0.3 μM (wt) is also included for comparison.

Mentions: In Figure 5A, we model the effects of both PLS transcription, k6, and the ethylene response through its receptor-signalling pathway, k11. k11 can be reduced experimentally by genetic or pharmacological inhibition of ethylene signalling (Chilley et al, 2006). Model analysis predicts that interaction of the PLS peptide with the ethylene signalling pathway can flexibly regulate auxin concentration and response. If PLS is not expressed (pls), the regulation of auxin concentration and its response by the interaction between ethylene and its receptors is less flexible. When k11 changes in the range of 0.1–10 μM−1 s−1 (for wt, k11=5 μM−1 s−1), the change in auxin concentration is less than 0.1% (Figure 5A). To change the auxin concentration markedly, k11 needs to be reduced to 0.01 μM−1 s−1. However, the prediction described in Figure 5A is that if PLS is expressed (in wild type or PLSox seedlings), changing k11 provides more flexibility in the regulation of auxin concentration/response. In addition, the interaction between PLS and ethylene signalling provides the system with an enhanced capability to regulate auxin concentration, by changing either PLS expression, ethylene signalling or both.


Modelling and experimental analysis of hormonal crosstalk in Arabidopsis.

Liu J, Mehdi S, Topping J, Tarkowski P, Lindsey K - Mol. Syst. Biol. (2010)

PLS-mediated control of auxin concentration. (A) Effects of both PLS transcription and interaction of ethylene with its receptor on auxin concentration; (B) effects of both exogenous ACC and PLS transcription on auxin concentration. In pls mutant, auxin concentration decreases from 0.14 to 0.12 μM as exogenous ACC concentration increases from 0 to 10 μM. (C) Effects of both exogenous ACC and PLS transcription on auxin transport and biosynthesis; (D) effects of both PLS transcription and interaction of ethylene with its receptor on auxin transport and biosynthesis; (E) effects of PLS transcription on endogenous ethylene concentration; (F) filled bar: modelling results; unfilled bar: experimental measurements (Chilley et al, 2006). wt: k6=0.3 s−1; k11=5 μM−1 s−1; pls: k6=0.0 s−1; k11=5 μM−1 s−1. pls etr1-1: k6=0.0 s−1; k11=0.03 μM−1 s−1. PLSox: k6=1.0 s−1; k11=5 μM−1 s−1. PLSox ETR1-1ox: k6=0.45 s−1; k11=10 μM−1 s−1. PLSox etr1-1: k6=0.45 s−1; k11=0.03 μM−1 s−1. (G) Analysis of the effects of both CTR1 and PLS transcription. Auxin concentration for total CTR1 concentration to be 0.3 μM (wt) is also included for comparison.
© Copyright Policy - open-access
Related In: Results  -  Collection

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f5: PLS-mediated control of auxin concentration. (A) Effects of both PLS transcription and interaction of ethylene with its receptor on auxin concentration; (B) effects of both exogenous ACC and PLS transcription on auxin concentration. In pls mutant, auxin concentration decreases from 0.14 to 0.12 μM as exogenous ACC concentration increases from 0 to 10 μM. (C) Effects of both exogenous ACC and PLS transcription on auxin transport and biosynthesis; (D) effects of both PLS transcription and interaction of ethylene with its receptor on auxin transport and biosynthesis; (E) effects of PLS transcription on endogenous ethylene concentration; (F) filled bar: modelling results; unfilled bar: experimental measurements (Chilley et al, 2006). wt: k6=0.3 s−1; k11=5 μM−1 s−1; pls: k6=0.0 s−1; k11=5 μM−1 s−1. pls etr1-1: k6=0.0 s−1; k11=0.03 μM−1 s−1. PLSox: k6=1.0 s−1; k11=5 μM−1 s−1. PLSox ETR1-1ox: k6=0.45 s−1; k11=10 μM−1 s−1. PLSox etr1-1: k6=0.45 s−1; k11=0.03 μM−1 s−1. (G) Analysis of the effects of both CTR1 and PLS transcription. Auxin concentration for total CTR1 concentration to be 0.3 μM (wt) is also included for comparison.
Mentions: In Figure 5A, we model the effects of both PLS transcription, k6, and the ethylene response through its receptor-signalling pathway, k11. k11 can be reduced experimentally by genetic or pharmacological inhibition of ethylene signalling (Chilley et al, 2006). Model analysis predicts that interaction of the PLS peptide with the ethylene signalling pathway can flexibly regulate auxin concentration and response. If PLS is not expressed (pls), the regulation of auxin concentration and its response by the interaction between ethylene and its receptors is less flexible. When k11 changes in the range of 0.1–10 μM−1 s−1 (for wt, k11=5 μM−1 s−1), the change in auxin concentration is less than 0.1% (Figure 5A). To change the auxin concentration markedly, k11 needs to be reduced to 0.01 μM−1 s−1. However, the prediction described in Figure 5A is that if PLS is expressed (in wild type or PLSox seedlings), changing k11 provides more flexibility in the regulation of auxin concentration/response. In addition, the interaction between PLS and ethylene signalling provides the system with an enhanced capability to regulate auxin concentration, by changing either PLS expression, ethylene signalling or both.

Bottom Line: Modelling correctly predicts experimental results for the effect of the pls gene mutation on endogenous cytokinin concentration.Modelling further reveals that a bell-shaped dose-response relationship between endogenous auxin and root length is established via PLS.This combined modelling and experimental analysis provides new insights into the integration of hormonal signals in plants.

View Article: PubMed Central - PubMed

Affiliation: The Integrative Cell Biology Laboratory and The Biophysical Sciences Institute, School of Biological and Biomedical Sciences, Durham University, Durham, UK. junli.liu@durham.ac.uk

ABSTRACT
An important question in plant biology is how genes influence the crosstalk between hormones to regulate growth. In this study, we model POLARIS (PLS) gene function and crosstalk between auxin, ethylene and cytokinin in Arabidopsis. Experimental evidence suggests that PLS acts on or close to the ethylene receptor ETR1, and a mathematical model describing possible PLS-ethylene pathway interactions is developed, and used to make quantitative predictions about PLS-hormone interactions. Modelling correctly predicts experimental results for the effect of the pls gene mutation on endogenous cytokinin concentration. Modelling also reveals a role for PLS in auxin biosynthesis in addition to a role in auxin transport. The model reproduces available mutants, and with new experimental data provides new insights into how PLS regulates auxin concentration, by controlling the relative contribution of auxin transport and biosynthesis and by integrating auxin, ethylene and cytokinin signalling. Modelling further reveals that a bell-shaped dose-response relationship between endogenous auxin and root length is established via PLS. This combined modelling and experimental analysis provides new insights into the integration of hormonal signals in plants.

Show MeSH
Related in: MedlinePlus