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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 level in response to a sequence of light conditions.The arrows with corresponding colours and directions signify the imposition (upward) or removal (downward) of a specific light signal. The system is in darkness at time step 0; a red light signal is added at step 4; a blue light signal is turned on at step 15 and off at step 24. The blue light signal induces a sharp increase in the stomatal opening level. The stomatal opening level gradually returns to the red light-induced steady state level after the blue light pulse.
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pcbi-1003930-g003: Simulation of stomatal opening level in response to a sequence of light conditions.The arrows with corresponding colours and directions signify the imposition (upward) or removal (downward) of a specific light signal. The system is in darkness at time step 0; a red light signal is added at step 4; a blue light signal is turned on at step 15 and off at step 24. The blue light signal induces a sharp increase in the stomatal opening level. The stomatal opening level gradually returns to the red light-induced steady state level after the blue light pulse.

Mentions: We started by comparing the model's results to experiments under different qualities of light in ambient air. In signature experiments that investigated the roles of red and blue light in stimulating stomatal opening, leaves were illuminated with constant background red light upon which a short blue light pulse was superimposed. The stomatal conductance increased slightly in response to the red light, then displayed dramatic transient increase in response to the blue light pulse [5], [9], [57], [58]. As depicted in Figure 3, our model successfully reproduces this temporal pattern of stomatal opening.


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 level in response to a sequence of light conditions.The arrows with corresponding colours and directions signify the imposition (upward) or removal (downward) of a specific light signal. The system is in darkness at time step 0; a red light signal is added at step 4; a blue light signal is turned on at step 15 and off at step 24. The blue light signal induces a sharp increase in the stomatal opening level. The stomatal opening level gradually returns to the red light-induced steady state level after the blue light pulse.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003930-g003: Simulation of stomatal opening level in response to a sequence of light conditions.The arrows with corresponding colours and directions signify the imposition (upward) or removal (downward) of a specific light signal. The system is in darkness at time step 0; a red light signal is added at step 4; a blue light signal is turned on at step 15 and off at step 24. The blue light signal induces a sharp increase in the stomatal opening level. The stomatal opening level gradually returns to the red light-induced steady state level after the blue light pulse.
Mentions: We started by comparing the model's results to experiments under different qualities of light in ambient air. In signature experiments that investigated the roles of red and blue light in stimulating stomatal opening, leaves were illuminated with constant background red light upon which a short blue light pulse was superimposed. The stomatal conductance increased slightly in response to the red light, then displayed dramatic transient increase in response to the blue light pulse [5], [9], [57], [58]. As depicted in Figure 3, our model successfully reproduces this temporal pattern of stomatal opening.

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