Multi-level modeling of light-induced stomatal opening offers new insights into its regulation by drought.
by Sun Z., Jin X., Albert R., Assmann S. M. (2014)
in PLoS Comp. Biol.10:e1003930. – doi: 10.1371/journal.pcbi.1003930 –
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+]cplays a key role, and indicated an absence of cross-talk between red light and ABA.
The dynamic model captured more than 1031 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.
Stomata are microscopic pores surrounded and regulated by pairs of guard cells located on the surface of plant leaves. Stomata participate in CO2 uptake, O2 release and water vapor loss. Blue and red light induce stomatal opening (enlargement of the pores), which allows the uptake of CO2, providing the raw material for photosynthesis, and the release of O2 into the atmosphere. The stress hormone abscisic acid induces minimization of pore width, decreasing water loss through transpiration. During drought conditions these counteracting stimuli jointly determine the overall stomatal movement through an integrated guard cell signalling cascade. We synthesized this interaction network between blue light, red light, and abscisic acid by aggregating and interpreting the abundant biological evidence that has been accumulated to date. We used the resulting network as the basis of a multi-level dynamic model of stomatal opening regulation in response to multiple stimuli. The model is validated by comparing its results to a large number of published experimental observations. Our model, and our experiments inspired by it, reveal an unexplored facet of the interplay between light and abscisic acid in guard cell signalling. The model directs future experiments, and its methodology can readily be applied to other systems.