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PMID:19057671

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Citation

Fucile, G, Falconer, S and Christendat, D (2008) Evolutionary diversification of plant shikimate kinase gene duplicates. PLoS Genet. 4:e1000292

Abstract

Shikimate kinase (SK; EC 2.7.1.71) catalyzes the fifth reaction of the shikimate pathway, which directs carbon from the central metabolism pool to a broad range of secondary metabolites involved in plant development, growth, and stress responses. In this study, we demonstrate the role of plant SK gene duplicate evolution in the diversification of metabolic regulation and the acquisition of novel and physiologically essential function. Phylogenetic analysis of plant SK homologs resolves an orthologous cluster of plant SKs and two functionally distinct orthologous clusters. These previously undescribed genes, shikimate kinase-like 1 (SKL1) and -2 (SKL2), do not encode SK activity, are present in all major plant lineages, and apparently evolved under positive selection following SK gene duplication over 400 MYA. This is supported by functional assays using recombinant SK, SKL1, and SKL2 from Arabidopsis thaliana (At) and evolutionary analyses of the diversification of SK-catalytic and -substrate binding sites based on theoretical structure models. AtSKL1 mutants yield albino and novel variegated phenotypes, which indicate SKL1 is required for chloroplast biogenesis. Extant SKL2 sequences show a strong genetic signature of positive selection, which is enriched in a protein-protein interaction module not found in other SK homologs. We also report the first kinetic characterization of plant SKs and show that gene expression diversification among the AtSK inparalogs is correlated with developmental processes and stress responses. This study examines the functional diversification of ancient and recent plant SK gene duplicates and highlights the utility of SKs as scaffolds for functional innovation.

Links

PubMed PMC2593004 Online version:10.1371/journal.pgen.1000292

Keywords

Amino Acid Sequence; Chloroplasts/chemistry; Chloroplasts/enzymology; Chloroplasts/genetics; Evolution, Molecular; Gene Duplication; Molecular Sequence Data; Mutation; Phosphotransferases (Alcohol Group Acceptor)/chemistry; Phosphotransferases (Alcohol Group Acceptor)/genetics; Phosphotransferases (Alcohol Group Acceptor)/metabolism; Phylogeny; Plant Proteins/chemistry; Plant Proteins/genetics; Plant Proteins/metabolism; Plants/chemistry; Plants/classification; Plants/enzymology; Plants/genetics; Protein Structure, Tertiary; Selection, Genetic

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

ARATH:F4IIJ2

involved_in

GO:0019632: shikimate metabolic process

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:F4IIJ2

located_in

GO:0009507: chloroplast

ECO:0000304: author statement supported by traceable reference used in manual assertion

C

Seeded From UniProt

complete

ARATH:F4IIJ2

enables

GO:0004765: shikimate kinase activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ARATH:F4JW33

involved_in

GO:0019632: shikimate metabolic process

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:F4JW33

located_in

GO:0009507: chloroplast

ECO:0000304: author statement supported by traceable reference used in manual assertion

C

Seeded From UniProt

complete

ARATH:F4JW33

enables

GO:0004765: shikimate kinase activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ARATH:SKL2

NOT|enables

GO:0004765: shikimate kinase activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ARATH:SK2

involved_in

GO:0019632: shikimate metabolic process

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:SK2

enables

GO:0004765: shikimate kinase activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ARATH:SKL1

involved_in

GO:0010027: thylakoid membrane organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:SKL1

involved_in

GO:0009658: chloroplast organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:SKL1

NOT|enables

GO:0004765: shikimate kinase activity

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete


See also

References

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