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Flux Control in a Defense Pathway in Arabidopsis thaliana Is Robust to Environmental Perturbations and Controls Variation in Adaptive Traits.

Olson-Manning CF, Strock CF, Mitchell-Olds T - G3 (Bethesda) (2015)

Bottom Line: Uncovering the general properties of biochemical pathways that influence ecologically important traits is an effective way to understand these connections.We also find that a generalist herbivore, Trichoplusia ni, modifies its feeding behavior depending on the flux through the glucosinolate pathway.The influence over herbivore behavior combined with the consistency of flux control suggests that genes controlling flux might be repeatedly targeted by natural selection in diverse environments and species.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, University of Chicago, Illinois 60637 colsonmanning@uchicago.edu.

No MeSH data available.


The aliphatic and indolic glucosinolate pathways in Arabidopsis thaliana. Aliphatic glucosinolates are synthesized by enzymatic reactions on the left pathway (yellow) beginning with chain-elongated methionine (MET) (Sønderby et al. 2010). Indolic glucosinolates are synthesized from tryptophan (TRP) by the right (blue) side of the pathway. Both pathways use the enzymes SUR1 and UGT74B1 found in the green intersection of the pathways. Black circles depict metabolites and are labeled in gray italics where necessary. Black lines connecting metabolites signify enzymatic reactions. Underlined enzymes were those manipulated in this study.
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fig1: The aliphatic and indolic glucosinolate pathways in Arabidopsis thaliana. Aliphatic glucosinolates are synthesized by enzymatic reactions on the left pathway (yellow) beginning with chain-elongated methionine (MET) (Sønderby et al. 2010). Indolic glucosinolates are synthesized from tryptophan (TRP) by the right (blue) side of the pathway. Both pathways use the enzymes SUR1 and UGT74B1 found in the green intersection of the pathways. Black circles depict metabolites and are labeled in gray italics where necessary. Black lines connecting metabolites signify enzymatic reactions. Underlined enzymes were those manipulated in this study.

Mentions: However, the observation that enzymes with significant pathway flux control often are encoded by genes with sequence signatures of adaptive evolution supports a functional connection between metabolic variation and whole-organism traits (Flowers et al. 2007; Olson-Manning et al. 2013; Lavington et al. 2014). Genetic studies of Drosophila found that enzymes with presumed flux control in glycolysis alter adult flight performance (Eanes et al. 2006) and clines in gene frequency are concentrated in glycolytic and pentose shunt enzymes thought to influence flux balance in response to temperature and climate (Lavington et al. 2014). For glucosinolates in Arabidopsis, the first biosynthetic step leading to short-chain aliphatic glucosinolates (CYP79F1, Figure 1) has primary flux control and is encoded by the only pathway gene showing clear evidence of non-neutral evolution in that study (Olson-Manning et al. 2013). In closely related Boechera stricta, the orthologous locus shows accelerated biochemical evolution and controls variation for herbivore damage and plant fitness in nature (Prasad et al. 2012). These concordant results across 15 million years of evolutionary divergence (Rushworth et al. 2011) support the hypothesis that genes controlling pathway flux might be repeated targets of natural selection due to consistent physiological effects in diverse environments and species.


Flux Control in a Defense Pathway in Arabidopsis thaliana Is Robust to Environmental Perturbations and Controls Variation in Adaptive Traits.

Olson-Manning CF, Strock CF, Mitchell-Olds T - G3 (Bethesda) (2015)

The aliphatic and indolic glucosinolate pathways in Arabidopsis thaliana. Aliphatic glucosinolates are synthesized by enzymatic reactions on the left pathway (yellow) beginning with chain-elongated methionine (MET) (Sønderby et al. 2010). Indolic glucosinolates are synthesized from tryptophan (TRP) by the right (blue) side of the pathway. Both pathways use the enzymes SUR1 and UGT74B1 found in the green intersection of the pathways. Black circles depict metabolites and are labeled in gray italics where necessary. Black lines connecting metabolites signify enzymatic reactions. Underlined enzymes were those manipulated in this study.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4632061&req=5

fig1: The aliphatic and indolic glucosinolate pathways in Arabidopsis thaliana. Aliphatic glucosinolates are synthesized by enzymatic reactions on the left pathway (yellow) beginning with chain-elongated methionine (MET) (Sønderby et al. 2010). Indolic glucosinolates are synthesized from tryptophan (TRP) by the right (blue) side of the pathway. Both pathways use the enzymes SUR1 and UGT74B1 found in the green intersection of the pathways. Black circles depict metabolites and are labeled in gray italics where necessary. Black lines connecting metabolites signify enzymatic reactions. Underlined enzymes were those manipulated in this study.
Mentions: However, the observation that enzymes with significant pathway flux control often are encoded by genes with sequence signatures of adaptive evolution supports a functional connection between metabolic variation and whole-organism traits (Flowers et al. 2007; Olson-Manning et al. 2013; Lavington et al. 2014). Genetic studies of Drosophila found that enzymes with presumed flux control in glycolysis alter adult flight performance (Eanes et al. 2006) and clines in gene frequency are concentrated in glycolytic and pentose shunt enzymes thought to influence flux balance in response to temperature and climate (Lavington et al. 2014). For glucosinolates in Arabidopsis, the first biosynthetic step leading to short-chain aliphatic glucosinolates (CYP79F1, Figure 1) has primary flux control and is encoded by the only pathway gene showing clear evidence of non-neutral evolution in that study (Olson-Manning et al. 2013). In closely related Boechera stricta, the orthologous locus shows accelerated biochemical evolution and controls variation for herbivore damage and plant fitness in nature (Prasad et al. 2012). These concordant results across 15 million years of evolutionary divergence (Rushworth et al. 2011) support the hypothesis that genes controlling pathway flux might be repeated targets of natural selection due to consistent physiological effects in diverse environments and species.

Bottom Line: Uncovering the general properties of biochemical pathways that influence ecologically important traits is an effective way to understand these connections.We also find that a generalist herbivore, Trichoplusia ni, modifies its feeding behavior depending on the flux through the glucosinolate pathway.The influence over herbivore behavior combined with the consistency of flux control suggests that genes controlling flux might be repeatedly targeted by natural selection in diverse environments and species.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, University of Chicago, Illinois 60637 colsonmanning@uchicago.edu.

No MeSH data available.