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Multi-level modeling of light-induced stomatal opening offers new insights into its regulation by drought.

Sun Z, Jin X, Albert R, Assmann SM - PLoS Comput. Biol. (2014)

Bottom Line: The dynamic model captured more than 10(31) distinct states for the system and yielded outcomes that were in qualitative agreement with a wide variety of previous experimental results.We found that under white light or blue light, over 60%, and under red light, over 90% of all simulated knockouts had similar opening responses as wild type, showing that the system is robust against single node loss.The model revealed an open question concerning the effect of ABA on red light-induced stomatal opening.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, The Pennsylvania State University, University Park, Pennsylvania, United States of America.

ABSTRACT
Plant guard cells gate CO2 uptake and transpirational water loss through stomatal pores. As a result of decades of experimental investigation, there is an abundance of information on the involvement of specific proteins and secondary messengers in the regulation of stomatal movements and on the pairwise relationships between guard cell components. We constructed a multi-level dynamic model of guard cell signal transduction during light-induced stomatal opening and of the effect of the plant hormone abscisic acid (ABA) on this process. The model integrates into a coherent network the direct and indirect biological evidence regarding the regulation of seventy components implicated in stomatal opening. Analysis of this signal transduction network identified robust cross-talk between blue light and ABA, in which [Ca2+]c plays a key role, and indicated an absence of cross-talk between red light and ABA. The dynamic model captured more than 10(31) distinct states for the system and yielded outcomes that were in qualitative agreement with a wide variety of previous experimental results. We obtained novel model predictions by simulating single component knockout phenotypes. We found that under white light or blue light, over 60%, and under red light, over 90% of all simulated knockouts had similar opening responses as wild type, showing that the system is robust against single node loss. The model revealed an open question concerning the effect of ABA on red light-induced stomatal opening. We experimentally showed that ABA is able to inhibit red light-induced stomatal opening, and our model offers possible hypotheses for the underlying mechanism, which point to potential future experiments. Our modelling methodology combines simplicity and flexibility with dynamic richness, making it well suited for a wide class of biological regulatory systems.

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Simulation of stomatal opening under different conditions of light quality in ambient air.(A) Mean stomatal opening levels as a function of time step from 2,000 simulations. Purple: dual beam (blue light = red light = 1, CO2 = 1); blue: blue light (blue light = 1, red light = 0, CO2 = 1); red: red light (blue light = 0, red light = 1, CO2 = 1). The standard error of the mean for the stomatal opening level is smaller than the symbols, and is consequently not shown. (B) Summary table of results for several simulated variables. The first three columns summarize the results shown in (A) indicating the maximum (steady-state) opening level, the number of time steps at which 50% of simulations reach 50% of the maximum level (t50%) and the number of time steps at which 95% of simulations reach 95% of the maximum level (t95%). The next two columns indicate the maximum malate levels and the maximum activation levels of the H+-ATPasecomplex. The two right-most columns present the contribution of different osmotica (ions vs. sucrose) to stomatal opening in response to different light qualities.
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pcbi-1003930-g004: Simulation of stomatal opening under different conditions of light quality in ambient air.(A) Mean stomatal opening levels as a function of time step from 2,000 simulations. Purple: dual beam (blue light = red light = 1, CO2 = 1); blue: blue light (blue light = 1, red light = 0, CO2 = 1); red: red light (blue light = 0, red light = 1, CO2 = 1). The standard error of the mean for the stomatal opening level is smaller than the symbols, and is consequently not shown. (B) Summary table of results for several simulated variables. The first three columns summarize the results shown in (A) indicating the maximum (steady-state) opening level, the number of time steps at which 50% of simulations reach 50% of the maximum level (t50%) and the number of time steps at which 95% of simulations reach 95% of the maximum level (t95%). The next two columns indicate the maximum malate levels and the maximum activation levels of the H+-ATPasecomplex. The two right-most columns present the contribution of different osmotica (ions vs. sucrose) to stomatal opening in response to different light qualities.

Mentions: We simulated wild type stomatal responses to sustained light in ambient air, as illustrated in Figure 4A. The specific combination of signals for each curve (blue light, red light, or dual beam) is initiated at time step 0 and maintained throughout the simulation. All three time courses of average stomatal opening levels (over the 2000 simulations) have similar sigmoidal shapes. We consistently observed sigmoidal timecourses for stomatal opening and other variables and in the following summarize them by three parameters (Figure 4B): the maximal (steady state) value of the mean level, the number of time steps at which 50% of simulations reach 50% of the maximal (steady state) level (t50%), and the number of time steps at which 95% of all simulations reach 95% of the maximal level (t95%). In the presence of both blue and red light, the average stomatal opening level reaches a maximum of ∼11.28 in ∼10 steps, whereas red light alone only generates an opening level of 1.00. Notably, blue light, with an opening level of 4.15, is more effective than red light in inducing opening, which is consistent with experimental observations of stomatal apertures [3], [5]. A synergistic action of red and blue light on stomatal opening, which has been observed experimentally [5], [9], [39], [57], is reproduced in Figure 4A: the stomatal opening level under both blue and red light (dual beam) is larger than the sum of opening levels under each type of light alone.


Multi-level modeling of light-induced stomatal opening offers new insights into its regulation by drought.

Sun Z, Jin X, Albert R, Assmann SM - PLoS Comput. Biol. (2014)

Simulation of stomatal opening under different conditions of light quality in ambient air.(A) Mean stomatal opening levels as a function of time step from 2,000 simulations. Purple: dual beam (blue light = red light = 1, CO2 = 1); blue: blue light (blue light = 1, red light = 0, CO2 = 1); red: red light (blue light = 0, red light = 1, CO2 = 1). The standard error of the mean for the stomatal opening level is smaller than the symbols, and is consequently not shown. (B) Summary table of results for several simulated variables. The first three columns summarize the results shown in (A) indicating the maximum (steady-state) opening level, the number of time steps at which 50% of simulations reach 50% of the maximum level (t50%) and the number of time steps at which 95% of simulations reach 95% of the maximum level (t95%). The next two columns indicate the maximum malate levels and the maximum activation levels of the H+-ATPasecomplex. The two right-most columns present the contribution of different osmotica (ions vs. sucrose) to stomatal opening in response to different light qualities.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230748&req=5

pcbi-1003930-g004: Simulation of stomatal opening under different conditions of light quality in ambient air.(A) Mean stomatal opening levels as a function of time step from 2,000 simulations. Purple: dual beam (blue light = red light = 1, CO2 = 1); blue: blue light (blue light = 1, red light = 0, CO2 = 1); red: red light (blue light = 0, red light = 1, CO2 = 1). The standard error of the mean for the stomatal opening level is smaller than the symbols, and is consequently not shown. (B) Summary table of results for several simulated variables. The first three columns summarize the results shown in (A) indicating the maximum (steady-state) opening level, the number of time steps at which 50% of simulations reach 50% of the maximum level (t50%) and the number of time steps at which 95% of simulations reach 95% of the maximum level (t95%). The next two columns indicate the maximum malate levels and the maximum activation levels of the H+-ATPasecomplex. The two right-most columns present the contribution of different osmotica (ions vs. sucrose) to stomatal opening in response to different light qualities.
Mentions: We simulated wild type stomatal responses to sustained light in ambient air, as illustrated in Figure 4A. The specific combination of signals for each curve (blue light, red light, or dual beam) is initiated at time step 0 and maintained throughout the simulation. All three time courses of average stomatal opening levels (over the 2000 simulations) have similar sigmoidal shapes. We consistently observed sigmoidal timecourses for stomatal opening and other variables and in the following summarize them by three parameters (Figure 4B): the maximal (steady state) value of the mean level, the number of time steps at which 50% of simulations reach 50% of the maximal (steady state) level (t50%), and the number of time steps at which 95% of all simulations reach 95% of the maximal level (t95%). In the presence of both blue and red light, the average stomatal opening level reaches a maximum of ∼11.28 in ∼10 steps, whereas red light alone only generates an opening level of 1.00. Notably, blue light, with an opening level of 4.15, is more effective than red light in inducing opening, which is consistent with experimental observations of stomatal apertures [3], [5]. A synergistic action of red and blue light on stomatal opening, which has been observed experimentally [5], [9], [39], [57], is reproduced in Figure 4A: the stomatal opening level under both blue and red light (dual beam) is larger than the sum of opening levels under each type of light alone.

Bottom Line: The dynamic model captured more than 10(31) distinct states for the system and yielded outcomes that were in qualitative agreement with a wide variety of previous experimental results.We found that under white light or blue light, over 60%, and under red light, over 90% of all simulated knockouts had similar opening responses as wild type, showing that the system is robust against single node loss.The model revealed an open question concerning the effect of ABA on red light-induced stomatal opening.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, The Pennsylvania State University, University Park, Pennsylvania, United States of America.

ABSTRACT
Plant guard cells gate CO2 uptake and transpirational water loss through stomatal pores. As a result of decades of experimental investigation, there is an abundance of information on the involvement of specific proteins and secondary messengers in the regulation of stomatal movements and on the pairwise relationships between guard cell components. We constructed a multi-level dynamic model of guard cell signal transduction during light-induced stomatal opening and of the effect of the plant hormone abscisic acid (ABA) on this process. The model integrates into a coherent network the direct and indirect biological evidence regarding the regulation of seventy components implicated in stomatal opening. Analysis of this signal transduction network identified robust cross-talk between blue light and ABA, in which [Ca2+]c plays a key role, and indicated an absence of cross-talk between red light and ABA. The dynamic model captured more than 10(31) distinct states for the system and yielded outcomes that were in qualitative agreement with a wide variety of previous experimental results. We obtained novel model predictions by simulating single component knockout phenotypes. We found that under white light or blue light, over 60%, and under red light, over 90% of all simulated knockouts had similar opening responses as wild type, showing that the system is robust against single node loss. The model revealed an open question concerning the effect of ABA on red light-induced stomatal opening. We experimentally showed that ABA is able to inhibit red light-induced stomatal opening, and our model offers possible hypotheses for the underlying mechanism, which point to potential future experiments. Our modelling methodology combines simplicity and flexibility with dynamic richness, making it well suited for a wide class of biological regulatory systems.

Show MeSH
Related in: MedlinePlus