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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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The effect of CO2-free air on light-induced stomatal opening and H+-ATPase activity.Simulations of (A) maximum stomatal opening level, and (B) maximum H+-ATPase activity level in air with moderate CO2 concentration (+CO2) compared to CO2-free air (-CO2) under different light conditions. Red colour indicates red light, blue colour indicates blue light, purple colour indicates dual beam. Darker colours represent air with moderate CO2, and lighter colours represent CO2-free air. (A) Stomatal opening is significantly enhanced by CO2-free air under all light conditions. (B) The H+-ATPase activity pattern parallels that of stomatal opening levels in having higher levels in the absence of CO2.
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pcbi-1003930-g005: The effect of CO2-free air on light-induced stomatal opening and H+-ATPase activity.Simulations of (A) maximum stomatal opening level, and (B) maximum H+-ATPase activity level in air with moderate CO2 concentration (+CO2) compared to CO2-free air (-CO2) under different light conditions. Red colour indicates red light, blue colour indicates blue light, purple colour indicates dual beam. Darker colours represent air with moderate CO2, and lighter colours represent CO2-free air. (A) Stomatal opening is significantly enhanced by CO2-free air under all light conditions. (B) The H+-ATPase activity pattern parallels that of stomatal opening levels in having higher levels in the absence of CO2.

Mentions: We investigated the effect that different levels of CO2, another input signal to our model, has on stomatal opening induced by different qualities of light. The CO2 content in the ambient atmosphere affects light-induced stomatal opening. Air with lower CO2 concentration or CO2-free air was shown to promote white light-induced stomatal opening [1], blue light-induced stomatal opening [5], [58], and red light-induced stomatal opening [40]. Our model captures the enhancement of stomatal opening levels by low CO2 under all light conditions (Figure 5A). Our simulations also indicate that the pattern of the maximal H+-ATPase activity in response to different light and CO2 conditions parallels that of stomatal opening (Figure 5B). Our model thus predicts that the H+-ATPase activity level is promoted by CO2-free air compared to ambient air under all light conditions, and suggests that the promotion of H+-ATPase activity level may contribute to the enhancement of stomatal opening levels by CO2-free air.


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)

The effect of CO2-free air on light-induced stomatal opening and H+-ATPase activity.Simulations of (A) maximum stomatal opening level, and (B) maximum H+-ATPase activity level in air with moderate CO2 concentration (+CO2) compared to CO2-free air (-CO2) under different light conditions. Red colour indicates red light, blue colour indicates blue light, purple colour indicates dual beam. Darker colours represent air with moderate CO2, and lighter colours represent CO2-free air. (A) Stomatal opening is significantly enhanced by CO2-free air under all light conditions. (B) The H+-ATPase activity pattern parallels that of stomatal opening levels in having higher levels in the absence of CO2.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003930-g005: The effect of CO2-free air on light-induced stomatal opening and H+-ATPase activity.Simulations of (A) maximum stomatal opening level, and (B) maximum H+-ATPase activity level in air with moderate CO2 concentration (+CO2) compared to CO2-free air (-CO2) under different light conditions. Red colour indicates red light, blue colour indicates blue light, purple colour indicates dual beam. Darker colours represent air with moderate CO2, and lighter colours represent CO2-free air. (A) Stomatal opening is significantly enhanced by CO2-free air under all light conditions. (B) The H+-ATPase activity pattern parallels that of stomatal opening levels in having higher levels in the absence of CO2.
Mentions: We investigated the effect that different levels of CO2, another input signal to our model, has on stomatal opening induced by different qualities of light. The CO2 content in the ambient atmosphere affects light-induced stomatal opening. Air with lower CO2 concentration or CO2-free air was shown to promote white light-induced stomatal opening [1], blue light-induced stomatal opening [5], [58], and red light-induced stomatal opening [40]. Our model captures the enhancement of stomatal opening levels by low CO2 under all light conditions (Figure 5A). Our simulations also indicate that the pattern of the maximal H+-ATPase activity in response to different light and CO2 conditions parallels that of stomatal opening (Figure 5B). Our model thus predicts that the H+-ATPase activity level is promoted by CO2-free air compared to ambient air under all light conditions, and suggests that the promotion of H+-ATPase activity level may contribute to the enhancement of stomatal opening levels by CO2-free air.

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