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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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Related in: MedlinePlus

The effect of ABA and DCMU on red light-induced stomatal opening.(A) Experimental measurement of stomatal apertures in isolated epidermal peels of Vicia faba under different conditions. Qualitatively, the apertures can be categorized into two opening levels: red light yields a high opening level, and opening levels under all other conditions can be considered as low. (B) Simulated stomatal opening levels. In the original model, stomatal opening levels under red light and red light + ABA treatments are high (level 1); all other treatments yield low (level 0) opening levels. If the model is modified by adding an inhibition of sucrose accumulation by ABA, red light is the only condition that yields a high opening level; all other conditions have low opening levels. This is in qualitative agreement with the experimental results shown in (A).
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pcbi-1003930-g006: The effect of ABA and DCMU on red light-induced stomatal opening.(A) Experimental measurement of stomatal apertures in isolated epidermal peels of Vicia faba under different conditions. Qualitatively, the apertures can be categorized into two opening levels: red light yields a high opening level, and opening levels under all other conditions can be considered as low. (B) Simulated stomatal opening levels. In the original model, stomatal opening levels under red light and red light + ABA treatments are high (level 1); all other treatments yield low (level 0) opening levels. If the model is modified by adding an inhibition of sucrose accumulation by ABA, red light is the only condition that yields a high opening level; all other conditions have low opening levels. This is in qualitative agreement with the experimental results shown in (A).

Mentions: Accordingly, we experimentally assessed the effect of ABA on red light-induced stomatal opening in Vicia faba epidermal peels (see Materials and Methods). Significant inhibition by ABA of red light-induced stomatal opening was found (Figure 6A). We also observed inhibition of stomatal opening by the photosynthetic inhibitor, DCMU, consistent with a previous report [3].


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 ABA and DCMU on red light-induced stomatal opening.(A) Experimental measurement of stomatal apertures in isolated epidermal peels of Vicia faba under different conditions. Qualitatively, the apertures can be categorized into two opening levels: red light yields a high opening level, and opening levels under all other conditions can be considered as low. (B) Simulated stomatal opening levels. In the original model, stomatal opening levels under red light and red light + ABA treatments are high (level 1); all other treatments yield low (level 0) opening levels. If the model is modified by adding an inhibition of sucrose accumulation by ABA, red light is the only condition that yields a high opening level; all other conditions have low opening levels. This is in qualitative agreement with the experimental results shown in (A).
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003930-g006: The effect of ABA and DCMU on red light-induced stomatal opening.(A) Experimental measurement of stomatal apertures in isolated epidermal peels of Vicia faba under different conditions. Qualitatively, the apertures can be categorized into two opening levels: red light yields a high opening level, and opening levels under all other conditions can be considered as low. (B) Simulated stomatal opening levels. In the original model, stomatal opening levels under red light and red light + ABA treatments are high (level 1); all other treatments yield low (level 0) opening levels. If the model is modified by adding an inhibition of sucrose accumulation by ABA, red light is the only condition that yields a high opening level; all other conditions have low opening levels. This is in qualitative agreement with the experimental results shown in (A).
Mentions: Accordingly, we experimentally assessed the effect of ABA on red light-induced stomatal opening in Vicia faba epidermal peels (see Materials and Methods). Significant inhibition by ABA of red light-induced stomatal opening was found (Figure 6A). We also observed inhibition of stomatal opening by the photosynthetic inhibitor, DCMU, consistent with a previous report [3].

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