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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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Current knowledge of light-induced stomatal opening and its regulation by CO2 and ABA.The color of the nodes represents their functional connectivity relative to the four signal nodes: CO2, red light, blue light, and ABA. CO2 and Ci are coloured grey. Nodes that can be activated by blue light alone are coloured blue. Nodes that can be activated by either red or blue light are coloured purple. Nodes are coloured yellow if they respond to the plant hormone ABA, and green if they are affected by both ABA and blue light. Nodes with no upstream effectors (called source nodes) are colored white, stomatal opening is coloured teal. We use a red shadow to indicate nodes that are characterized by three or more levelsin the dynamic model. To improve the visualization, multiple edges that originate from a single node may start together and bifurcate later toward their individual targets. Similarly, multiple positive edges that end at the same node may merge before reaching the target. Edge bifurcation or merging forms T-shaped junctions, while the crossing of two edges forms plus-shaped junctions. The full names of the network components denoted by abbreviated node names are: 14-3-3 proteinH-ATPase, 14-3-3 protein that binds to H+-ATPase; 14-3-3 proteinphot1, 14-3-3 protein that binds to phototropin 1; ABA, abscisic acid; ABI1, 2C-type protein phosphatase; acid. of apoplast, the acidification of the apoplast; AnionCh, anion efflux channels at the plasma membrane; AtABCB14, ABC transporter gene AtABCB14; Atnoa1, protein nitric oxide-associated 1; AtrbohD/F, NADPH oxidase D/F; AtSTP1, H-monosaccharide symporter gene AtSTP1; Ca-ATPase, Ca-ATPases and Ca2+/H+ antiporters responsible for Ca2+ efflux from the cytosol; CaIC, inward Ca2+ permeable channels; CaR, Ca2+ release from intracellular stores; carbon fixation, light-independent reactions of photosynthesis; CDPK, Ca2+-dependent protein kinases; CHL1, dual-affinity nitrate transporter gene AtNRT1.1; Ci, intercellular CO2 concentration; FFA, free fatty acids; H+-ATPase, the phosphorylated H-ATPase at the plasma membrane prior to the binding of the H+-ATPase 14-3-3 protein; H+-ATPasecomplex, 14-3-3 protein bound H+-ATPase; KEV, K+ efflux from vacuole to the cytosol; Kin, K+ inward channels at the plasma membrane; Kout, K+ outward channels at plasma membrane; LPL, lysophospholipids; NADPH, reduced form of nicotinamide adenine dinucleotide phosphate; NIA1, nitrate reductase; NO, nitric oxide; OST1, protein kinase open stomata 1; PA, phosphatidic acid; PEPC, phosphoenolpyruvate carboxylase; phot1, phototropin 1; phot1complex, 14-3-3 protein bound phototropin 1; phot2, phototropin 2; photophosphorylation, light-dependent reactions of photosynthesis; PIP2C, phosphatidylinositol 4,5-bisphosphate located in the cytosol; PIP2PM, phosphatidylinositol 4,5-bisphosphate located at the plasma membrane; PLA2β, phospholipase A2β; PLC, phospholipase C; PLD, phospholipase D; PMV, electric potential difference across the plasma membrane; PP1cn, the catalytic subunit of type 1 phosphatase located in the nucleus; PP1cc, the catalytic subunit of type 1 phosphatase located in the cytosol; protein kinase, a serine/threonine protein kinase that directly phosphorylates the plasma membrane H-ATPase; PRSL1, type 1 protein phosphatase regulatory subunit 2-like protein1; RIC7, ROP-interactive CRIB motif-containing protein 7; ROP2, small GTPase ROP2; ROS, reactive oxygen species; [Ca2+]c, cytosolic Ca2+ concentration; [Cl-]c/v, cytosolic/vacuolar Cl- concentration; [K+]c/v, cytosolic/vacuolar K+ concentration; [malate2-]a/c/v, apoplastic/cytosolic/vacuolar malate2- concentration; [NO3-]a/c/v, apoplastic/cytosolic/vacuolar nitrate concentration.
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pcbi-1003930-g001: Current knowledge of light-induced stomatal opening and its regulation by CO2 and ABA.The color of the nodes represents their functional connectivity relative to the four signal nodes: CO2, red light, blue light, and ABA. CO2 and Ci are coloured grey. Nodes that can be activated by blue light alone are coloured blue. Nodes that can be activated by either red or blue light are coloured purple. Nodes are coloured yellow if they respond to the plant hormone ABA, and green if they are affected by both ABA and blue light. Nodes with no upstream effectors (called source nodes) are colored white, stomatal opening is coloured teal. We use a red shadow to indicate nodes that are characterized by three or more levelsin the dynamic model. To improve the visualization, multiple edges that originate from a single node may start together and bifurcate later toward their individual targets. Similarly, multiple positive edges that end at the same node may merge before reaching the target. Edge bifurcation or merging forms T-shaped junctions, while the crossing of two edges forms plus-shaped junctions. The full names of the network components denoted by abbreviated node names are: 14-3-3 proteinH-ATPase, 14-3-3 protein that binds to H+-ATPase; 14-3-3 proteinphot1, 14-3-3 protein that binds to phototropin 1; ABA, abscisic acid; ABI1, 2C-type protein phosphatase; acid. of apoplast, the acidification of the apoplast; AnionCh, anion efflux channels at the plasma membrane; AtABCB14, ABC transporter gene AtABCB14; Atnoa1, protein nitric oxide-associated 1; AtrbohD/F, NADPH oxidase D/F; AtSTP1, H-monosaccharide symporter gene AtSTP1; Ca-ATPase, Ca-ATPases and Ca2+/H+ antiporters responsible for Ca2+ efflux from the cytosol; CaIC, inward Ca2+ permeable channels; CaR, Ca2+ release from intracellular stores; carbon fixation, light-independent reactions of photosynthesis; CDPK, Ca2+-dependent protein kinases; CHL1, dual-affinity nitrate transporter gene AtNRT1.1; Ci, intercellular CO2 concentration; FFA, free fatty acids; H+-ATPase, the phosphorylated H-ATPase at the plasma membrane prior to the binding of the H+-ATPase 14-3-3 protein; H+-ATPasecomplex, 14-3-3 protein bound H+-ATPase; KEV, K+ efflux from vacuole to the cytosol; Kin, K+ inward channels at the plasma membrane; Kout, K+ outward channels at plasma membrane; LPL, lysophospholipids; NADPH, reduced form of nicotinamide adenine dinucleotide phosphate; NIA1, nitrate reductase; NO, nitric oxide; OST1, protein kinase open stomata 1; PA, phosphatidic acid; PEPC, phosphoenolpyruvate carboxylase; phot1, phototropin 1; phot1complex, 14-3-3 protein bound phototropin 1; phot2, phototropin 2; photophosphorylation, light-dependent reactions of photosynthesis; PIP2C, phosphatidylinositol 4,5-bisphosphate located in the cytosol; PIP2PM, phosphatidylinositol 4,5-bisphosphate located at the plasma membrane; PLA2β, phospholipase A2β; PLC, phospholipase C; PLD, phospholipase D; PMV, electric potential difference across the plasma membrane; PP1cn, the catalytic subunit of type 1 phosphatase located in the nucleus; PP1cc, the catalytic subunit of type 1 phosphatase located in the cytosol; protein kinase, a serine/threonine protein kinase that directly phosphorylates the plasma membrane H-ATPase; PRSL1, type 1 protein phosphatase regulatory subunit 2-like protein1; RIC7, ROP-interactive CRIB motif-containing protein 7; ROP2, small GTPase ROP2; ROS, reactive oxygen species; [Ca2+]c, cytosolic Ca2+ concentration; [Cl-]c/v, cytosolic/vacuolar Cl- concentration; [K+]c/v, cytosolic/vacuolar K+ concentration; [malate2-]a/c/v, apoplastic/cytosolic/vacuolar malate2- concentration; [NO3-]a/c/v, apoplastic/cytosolic/vacuolar nitrate concentration.

Mentions: Figure 1 represents the resulting network of 70 nodes and 153 edges. The colour coding of the nodes signifies the functional connectivity of each node to the four signals, which is based on the existence of paths between a signal and the respective node but is also informed by the specific combinatorial regulation of the node (described in detail in the section “Elements of the dynamic model”). A brief description of the biology represented by the network is as follows; Text S3 provides a detailed description of the network. Both red and blue light activate guard cell photophosphorylation, providing adenosine triphosphate (ATP), the primary chemical energy transporter within the cell, for metabolic processes [33]. Subsequent carbon fixation provides sugars, primarily sucrose, as osmotica for guard cell swelling and stomatal opening [34], [35]. This pathway is formed by purple coloured nodes in the left side of the network. A blue light-specific pathway (blue coloured symbols) leads to the activation of the plasma membrane H+-ATPase [4], [36]. H+-ATPase activity hyperpolarizes the plasma membrane [4], with subsequent uptake of K+[37], [38] and accumulation of its counterions, Cl-, NO3-, and malate2-[13], [33]. These ions also function as osmotica during light-induced stomatal opening [6], [39], [40]. The stress hormone ABA initiates a signal transduction network (yellow nodes) which ultimately inhibits the plasma membrane H+-ATPase, inhibits malate synthesis, and induces malate breakdown and release [2], [41]–[45]. Thus the majority of the nodes in the network (the green-coloured nodes) are regulated by blue light and ABA. The twenty-three nodes that have more than two levels in our model are highlighted with a red shadow.


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)

Current knowledge of light-induced stomatal opening and its regulation by CO2 and ABA.The color of the nodes represents their functional connectivity relative to the four signal nodes: CO2, red light, blue light, and ABA. CO2 and Ci are coloured grey. Nodes that can be activated by blue light alone are coloured blue. Nodes that can be activated by either red or blue light are coloured purple. Nodes are coloured yellow if they respond to the plant hormone ABA, and green if they are affected by both ABA and blue light. Nodes with no upstream effectors (called source nodes) are colored white, stomatal opening is coloured teal. We use a red shadow to indicate nodes that are characterized by three or more levelsin the dynamic model. To improve the visualization, multiple edges that originate from a single node may start together and bifurcate later toward their individual targets. Similarly, multiple positive edges that end at the same node may merge before reaching the target. Edge bifurcation or merging forms T-shaped junctions, while the crossing of two edges forms plus-shaped junctions. The full names of the network components denoted by abbreviated node names are: 14-3-3 proteinH-ATPase, 14-3-3 protein that binds to H+-ATPase; 14-3-3 proteinphot1, 14-3-3 protein that binds to phototropin 1; ABA, abscisic acid; ABI1, 2C-type protein phosphatase; acid. of apoplast, the acidification of the apoplast; AnionCh, anion efflux channels at the plasma membrane; AtABCB14, ABC transporter gene AtABCB14; Atnoa1, protein nitric oxide-associated 1; AtrbohD/F, NADPH oxidase D/F; AtSTP1, H-monosaccharide symporter gene AtSTP1; Ca-ATPase, Ca-ATPases and Ca2+/H+ antiporters responsible for Ca2+ efflux from the cytosol; CaIC, inward Ca2+ permeable channels; CaR, Ca2+ release from intracellular stores; carbon fixation, light-independent reactions of photosynthesis; CDPK, Ca2+-dependent protein kinases; CHL1, dual-affinity nitrate transporter gene AtNRT1.1; Ci, intercellular CO2 concentration; FFA, free fatty acids; H+-ATPase, the phosphorylated H-ATPase at the plasma membrane prior to the binding of the H+-ATPase 14-3-3 protein; H+-ATPasecomplex, 14-3-3 protein bound H+-ATPase; KEV, K+ efflux from vacuole to the cytosol; Kin, K+ inward channels at the plasma membrane; Kout, K+ outward channels at plasma membrane; LPL, lysophospholipids; NADPH, reduced form of nicotinamide adenine dinucleotide phosphate; NIA1, nitrate reductase; NO, nitric oxide; OST1, protein kinase open stomata 1; PA, phosphatidic acid; PEPC, phosphoenolpyruvate carboxylase; phot1, phototropin 1; phot1complex, 14-3-3 protein bound phototropin 1; phot2, phototropin 2; photophosphorylation, light-dependent reactions of photosynthesis; PIP2C, phosphatidylinositol 4,5-bisphosphate located in the cytosol; PIP2PM, phosphatidylinositol 4,5-bisphosphate located at the plasma membrane; PLA2β, phospholipase A2β; PLC, phospholipase C; PLD, phospholipase D; PMV, electric potential difference across the plasma membrane; PP1cn, the catalytic subunit of type 1 phosphatase located in the nucleus; PP1cc, the catalytic subunit of type 1 phosphatase located in the cytosol; protein kinase, a serine/threonine protein kinase that directly phosphorylates the plasma membrane H-ATPase; PRSL1, type 1 protein phosphatase regulatory subunit 2-like protein1; RIC7, ROP-interactive CRIB motif-containing protein 7; ROP2, small GTPase ROP2; ROS, reactive oxygen species; [Ca2+]c, cytosolic Ca2+ concentration; [Cl-]c/v, cytosolic/vacuolar Cl- concentration; [K+]c/v, cytosolic/vacuolar K+ concentration; [malate2-]a/c/v, apoplastic/cytosolic/vacuolar malate2- concentration; [NO3-]a/c/v, apoplastic/cytosolic/vacuolar nitrate concentration.
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pcbi-1003930-g001: Current knowledge of light-induced stomatal opening and its regulation by CO2 and ABA.The color of the nodes represents their functional connectivity relative to the four signal nodes: CO2, red light, blue light, and ABA. CO2 and Ci are coloured grey. Nodes that can be activated by blue light alone are coloured blue. Nodes that can be activated by either red or blue light are coloured purple. Nodes are coloured yellow if they respond to the plant hormone ABA, and green if they are affected by both ABA and blue light. Nodes with no upstream effectors (called source nodes) are colored white, stomatal opening is coloured teal. We use a red shadow to indicate nodes that are characterized by three or more levelsin the dynamic model. To improve the visualization, multiple edges that originate from a single node may start together and bifurcate later toward their individual targets. Similarly, multiple positive edges that end at the same node may merge before reaching the target. Edge bifurcation or merging forms T-shaped junctions, while the crossing of two edges forms plus-shaped junctions. The full names of the network components denoted by abbreviated node names are: 14-3-3 proteinH-ATPase, 14-3-3 protein that binds to H+-ATPase; 14-3-3 proteinphot1, 14-3-3 protein that binds to phototropin 1; ABA, abscisic acid; ABI1, 2C-type protein phosphatase; acid. of apoplast, the acidification of the apoplast; AnionCh, anion efflux channels at the plasma membrane; AtABCB14, ABC transporter gene AtABCB14; Atnoa1, protein nitric oxide-associated 1; AtrbohD/F, NADPH oxidase D/F; AtSTP1, H-monosaccharide symporter gene AtSTP1; Ca-ATPase, Ca-ATPases and Ca2+/H+ antiporters responsible for Ca2+ efflux from the cytosol; CaIC, inward Ca2+ permeable channels; CaR, Ca2+ release from intracellular stores; carbon fixation, light-independent reactions of photosynthesis; CDPK, Ca2+-dependent protein kinases; CHL1, dual-affinity nitrate transporter gene AtNRT1.1; Ci, intercellular CO2 concentration; FFA, free fatty acids; H+-ATPase, the phosphorylated H-ATPase at the plasma membrane prior to the binding of the H+-ATPase 14-3-3 protein; H+-ATPasecomplex, 14-3-3 protein bound H+-ATPase; KEV, K+ efflux from vacuole to the cytosol; Kin, K+ inward channels at the plasma membrane; Kout, K+ outward channels at plasma membrane; LPL, lysophospholipids; NADPH, reduced form of nicotinamide adenine dinucleotide phosphate; NIA1, nitrate reductase; NO, nitric oxide; OST1, protein kinase open stomata 1; PA, phosphatidic acid; PEPC, phosphoenolpyruvate carboxylase; phot1, phototropin 1; phot1complex, 14-3-3 protein bound phototropin 1; phot2, phototropin 2; photophosphorylation, light-dependent reactions of photosynthesis; PIP2C, phosphatidylinositol 4,5-bisphosphate located in the cytosol; PIP2PM, phosphatidylinositol 4,5-bisphosphate located at the plasma membrane; PLA2β, phospholipase A2β; PLC, phospholipase C; PLD, phospholipase D; PMV, electric potential difference across the plasma membrane; PP1cn, the catalytic subunit of type 1 phosphatase located in the nucleus; PP1cc, the catalytic subunit of type 1 phosphatase located in the cytosol; protein kinase, a serine/threonine protein kinase that directly phosphorylates the plasma membrane H-ATPase; PRSL1, type 1 protein phosphatase regulatory subunit 2-like protein1; RIC7, ROP-interactive CRIB motif-containing protein 7; ROP2, small GTPase ROP2; ROS, reactive oxygen species; [Ca2+]c, cytosolic Ca2+ concentration; [Cl-]c/v, cytosolic/vacuolar Cl- concentration; [K+]c/v, cytosolic/vacuolar K+ concentration; [malate2-]a/c/v, apoplastic/cytosolic/vacuolar malate2- concentration; [NO3-]a/c/v, apoplastic/cytosolic/vacuolar nitrate concentration.
Mentions: Figure 1 represents the resulting network of 70 nodes and 153 edges. The colour coding of the nodes signifies the functional connectivity of each node to the four signals, which is based on the existence of paths between a signal and the respective node but is also informed by the specific combinatorial regulation of the node (described in detail in the section “Elements of the dynamic model”). A brief description of the biology represented by the network is as follows; Text S3 provides a detailed description of the network. Both red and blue light activate guard cell photophosphorylation, providing adenosine triphosphate (ATP), the primary chemical energy transporter within the cell, for metabolic processes [33]. Subsequent carbon fixation provides sugars, primarily sucrose, as osmotica for guard cell swelling and stomatal opening [34], [35]. This pathway is formed by purple coloured nodes in the left side of the network. A blue light-specific pathway (blue coloured symbols) leads to the activation of the plasma membrane H+-ATPase [4], [36]. H+-ATPase activity hyperpolarizes the plasma membrane [4], with subsequent uptake of K+[37], [38] and accumulation of its counterions, Cl-, NO3-, and malate2-[13], [33]. These ions also function as osmotica during light-induced stomatal opening [6], [39], [40]. The stress hormone ABA initiates a signal transduction network (yellow nodes) which ultimately inhibits the plasma membrane H+-ATPase, inhibits malate synthesis, and induces malate breakdown and release [2], [41]–[45]. Thus the majority of the nodes in the network (the green-coloured nodes) are regulated by blue light and ABA. The twenty-three nodes that have more than two levels in our model are highlighted with a red shadow.

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