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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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Structural analysis of the signalling network.(A) Compressed representation of the network that shows the four signals (input nodes) of the network, two composite nodes that represent SCC1 (which contains 31 nodes) and SCC2 (which contains 3 nodes), as well as photophosphorylation, sucrose, and the output node of the network, stomatal opening. The nodes not shown do not affect the network's connectivity and are contracted into the edges shown in black. Five paths do not cross SCC1; they start from blue light, red light, or CO2, pass through photophosphorylation, merge at SCC2, reach sucrose, and lead to stomatal opening. Signal-specific edges are coloured blue (for blue light), red (for red light), grey (for CO2); the edges shared by both blue and red light are purple. (B) The 4 edges whose removal results in the highest node loss from SCC1. The unperturbed SCC1 contains 31 nodes, which is the basis for the percentage calculation. (C) Sub-structure of SCC1. Group 1 contains 12 nodes, and group 2 contains 17 nodes.
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pcbi-1003930-g002: Structural analysis of the signalling network.(A) Compressed representation of the network that shows the four signals (input nodes) of the network, two composite nodes that represent SCC1 (which contains 31 nodes) and SCC2 (which contains 3 nodes), as well as photophosphorylation, sucrose, and the output node of the network, stomatal opening. The nodes not shown do not affect the network's connectivity and are contracted into the edges shown in black. Five paths do not cross SCC1; they start from blue light, red light, or CO2, pass through photophosphorylation, merge at SCC2, reach sucrose, and lead to stomatal opening. Signal-specific edges are coloured blue (for blue light), red (for red light), grey (for CO2); the edges shared by both blue and red light are purple. (B) The 4 edges whose removal results in the highest node loss from SCC1. The unperturbed SCC1 contains 31 nodes, which is the basis for the percentage calculation. (C) Sub-structure of SCC1. Group 1 contains 12 nodes, and group 2 contains 17 nodes.

Mentions: Next, we identified the strongly connected components of the system. A strongly connected component is a group of nodes wherein any node is reachable from any other node through a path (a series of consecutive nodes and edges). Intuitively, a strongly connected component is a closely-knit group of nodes with interwoven feedback that usually forms an important functional module of a network. The stomatal opening network contains three strongly connected components (SCCs), comprising 31 nodes (SCC1), 3 nodes (SCC2) and 2 nodes (SCC3), respectively (Figure 2A). The 3-node SCC2 represents the interplay amongst Ci and carbon fixation processes in guard cells and mesophyll cells: Ci is required by photosynthesis and photosynthesis lowers Ci in turn. The 2-node SCC3 represents the two directions of transport between apoplastic and cytosolic NO3-. The largest SCC signifies the crosstalk between the different signals of the system, since all four signals of our model connect to it. Eight of the thirteen high-degree nodes listed in Table 1 are in the largest SCC. Most of the remaining high degree nodes have only outgoing or incoming edges and thus cannot be strongly connected. Twenty-seven nodes, including the nodes of SCC2, can reach the nodes of SCC1 through directed paths. Eleven nodes, including SCC3, can be reached from SCC1 through directed paths. Only a single node, CHL1, is not connected to SCC1 by a directed path.


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)

Structural analysis of the signalling network.(A) Compressed representation of the network that shows the four signals (input nodes) of the network, two composite nodes that represent SCC1 (which contains 31 nodes) and SCC2 (which contains 3 nodes), as well as photophosphorylation, sucrose, and the output node of the network, stomatal opening. The nodes not shown do not affect the network's connectivity and are contracted into the edges shown in black. Five paths do not cross SCC1; they start from blue light, red light, or CO2, pass through photophosphorylation, merge at SCC2, reach sucrose, and lead to stomatal opening. Signal-specific edges are coloured blue (for blue light), red (for red light), grey (for CO2); the edges shared by both blue and red light are purple. (B) The 4 edges whose removal results in the highest node loss from SCC1. The unperturbed SCC1 contains 31 nodes, which is the basis for the percentage calculation. (C) Sub-structure of SCC1. Group 1 contains 12 nodes, and group 2 contains 17 nodes.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003930-g002: Structural analysis of the signalling network.(A) Compressed representation of the network that shows the four signals (input nodes) of the network, two composite nodes that represent SCC1 (which contains 31 nodes) and SCC2 (which contains 3 nodes), as well as photophosphorylation, sucrose, and the output node of the network, stomatal opening. The nodes not shown do not affect the network's connectivity and are contracted into the edges shown in black. Five paths do not cross SCC1; they start from blue light, red light, or CO2, pass through photophosphorylation, merge at SCC2, reach sucrose, and lead to stomatal opening. Signal-specific edges are coloured blue (for blue light), red (for red light), grey (for CO2); the edges shared by both blue and red light are purple. (B) The 4 edges whose removal results in the highest node loss from SCC1. The unperturbed SCC1 contains 31 nodes, which is the basis for the percentage calculation. (C) Sub-structure of SCC1. Group 1 contains 12 nodes, and group 2 contains 17 nodes.
Mentions: Next, we identified the strongly connected components of the system. A strongly connected component is a group of nodes wherein any node is reachable from any other node through a path (a series of consecutive nodes and edges). Intuitively, a strongly connected component is a closely-knit group of nodes with interwoven feedback that usually forms an important functional module of a network. The stomatal opening network contains three strongly connected components (SCCs), comprising 31 nodes (SCC1), 3 nodes (SCC2) and 2 nodes (SCC3), respectively (Figure 2A). The 3-node SCC2 represents the interplay amongst Ci and carbon fixation processes in guard cells and mesophyll cells: Ci is required by photosynthesis and photosynthesis lowers Ci in turn. The 2-node SCC3 represents the two directions of transport between apoplastic and cytosolic NO3-. The largest SCC signifies the crosstalk between the different signals of the system, since all four signals of our model connect to it. Eight of the thirteen high-degree nodes listed in Table 1 are in the largest SCC. Most of the remaining high degree nodes have only outgoing or incoming edges and thus cannot be strongly connected. Twenty-seven nodes, including the nodes of SCC2, can reach the nodes of SCC1 through directed paths. Eleven nodes, including SCC3, can be reached from SCC1 through directed paths. Only a single node, CHL1, is not connected to SCC1 by a directed path.

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