Limits...
Duplications and functional divergence of ADP-glucose pyrophosphorylase genes in plants.

Georgelis N, Braun EL, Hannah LC - BMC Evol. Biol. (2008)

Bottom Line: We found that the first duplication in the AGPase large subunit family occurred early in the history of land plants, while the earliest small subunit duplication occurred after the divergence of monocots and eudicots.Instead, evolutionary constraints appear to be permanently relaxed for the large subunit relative to the small subunit.We discuss the phenotypes of mutants that alter some candidate sites and strategies for examining candidate sites of presently unknown function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Program in Plant Molecular and Cellular Biology and Horticultural Sciences, University of Florida, Gainesville, Florida 32610-0245, USA. gnick@ufl.edu

ABSTRACT

Background: ADP-glucose pyrophosphorylase (AGPase), which catalyses a rate limiting step in starch synthesis, is a heterotetramer comprised of two identical large and two identical small subunits in plants. Although the large and small subunits are equally sensitive to activity-altering amino acid changes when expressed in a bacterial system, the overall rate of non-synonymous evolution is approximately 2.7-fold greater for the large subunit than for the small subunit. Herein, we examine the basis for their different rates of evolution, the number of duplications in both large and small subunit genes and document changes in the patterns of AGPase evolution over time.

Results: We found that the first duplication in the AGPase large subunit family occurred early in the history of land plants, while the earliest small subunit duplication occurred after the divergence of monocots and eudicots. The large subunit also had a larger number of gene duplications than did the small subunit. The ancient duplications in the large subunit family raise concern about the saturation of synonymous substitutions, but estimates of the absolute rate of AGPase evolution were highly correlated with estimates of omega (the non-synonymous to synonymous rate ratio). Both subunits showed evidence for positive selection and relaxation of purifying selection after duplication, but these phenomena could not explain the different evolutionary rates of the two subunits. Instead, evolutionary constraints appear to be permanently relaxed for the large subunit relative to the small subunit. Both subunits exhibit branch-specific patterns of rate variation among sites.

Conclusion: These analyses indicate that the higher evolutionary rate of the plant AGPase large subunit reflects permanent relaxation of constraints relative to the small subunit and they show that the large subunit genes have undergone more gene duplications than small subunit genes. Candidate sites potentially responsible for functional divergence within each of the AGPase subunits were investigated by examining branch-specific patterns of rate variation. We discuss the phenotypes of mutants that alter some candidate sites and strategies for examining candidate sites of presently unknown function.

Show MeSH
Absolute rate of evolution of the large and the small subunit of AGPase from angiosperms (measured in aass MY-1). The blue bars indicate the average rates (amino acid substitutions per site per million years; aass MY-1) estimated from the most recent dated speciation events to present sequences of the trees shown in Figure 1B and 1C. The red bars indicate the average aass MY-1 estimated from the most recent dated speciation events to present sequences of the trees shown in Additional file 3A and 2B. The yellow bars indicate the average aass MY-1 estimated from all branches in Figure 3A and 3B. The green bars indicate the average aass MY-1 estimated from all branches in Additional file 4A and 3B. The error bars indicate 2× standard error.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2529307&req=5

Figure 2: Absolute rate of evolution of the large and the small subunit of AGPase from angiosperms (measured in aass MY-1). The blue bars indicate the average rates (amino acid substitutions per site per million years; aass MY-1) estimated from the most recent dated speciation events to present sequences of the trees shown in Figure 1B and 1C. The red bars indicate the average aass MY-1 estimated from the most recent dated speciation events to present sequences of the trees shown in Additional file 3A and 2B. The yellow bars indicate the average aass MY-1 estimated from all branches in Figure 3A and 3B. The green bars indicate the average aass MY-1 estimated from all branches in Additional file 4A and 3B. The error bars indicate 2× standard error.

Mentions: Absolute rates of amino acid evolution for AGPase subunits were estimated by examining terminal branch lengths for divergences that reflect speciation events with known divergence times (these divergence times are presented in Additional file 2). This approach is called the tip procedure since it involves only terminal branches (Methods), and it revealed that the average rate of evolution for the large subunit was 2.7-fold faster than that of the small subunit (Figure 2). This rate difference was both congruent with the difference in ML estimates of ω [2] and highly significant (P = 0.0006 by Student's unpaired t-test). Our conclusions were unchanged if we limited consideration to strongly supported duplication events (those retained when bootstrap support was considered; see Additional file 3).


Duplications and functional divergence of ADP-glucose pyrophosphorylase genes in plants.

Georgelis N, Braun EL, Hannah LC - BMC Evol. Biol. (2008)

Absolute rate of evolution of the large and the small subunit of AGPase from angiosperms (measured in aass MY-1). The blue bars indicate the average rates (amino acid substitutions per site per million years; aass MY-1) estimated from the most recent dated speciation events to present sequences of the trees shown in Figure 1B and 1C. The red bars indicate the average aass MY-1 estimated from the most recent dated speciation events to present sequences of the trees shown in Additional file 3A and 2B. The yellow bars indicate the average aass MY-1 estimated from all branches in Figure 3A and 3B. The green bars indicate the average aass MY-1 estimated from all branches in Additional file 4A and 3B. The error bars indicate 2× standard error.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2529307&req=5

Figure 2: Absolute rate of evolution of the large and the small subunit of AGPase from angiosperms (measured in aass MY-1). The blue bars indicate the average rates (amino acid substitutions per site per million years; aass MY-1) estimated from the most recent dated speciation events to present sequences of the trees shown in Figure 1B and 1C. The red bars indicate the average aass MY-1 estimated from the most recent dated speciation events to present sequences of the trees shown in Additional file 3A and 2B. The yellow bars indicate the average aass MY-1 estimated from all branches in Figure 3A and 3B. The green bars indicate the average aass MY-1 estimated from all branches in Additional file 4A and 3B. The error bars indicate 2× standard error.
Mentions: Absolute rates of amino acid evolution for AGPase subunits were estimated by examining terminal branch lengths for divergences that reflect speciation events with known divergence times (these divergence times are presented in Additional file 2). This approach is called the tip procedure since it involves only terminal branches (Methods), and it revealed that the average rate of evolution for the large subunit was 2.7-fold faster than that of the small subunit (Figure 2). This rate difference was both congruent with the difference in ML estimates of ω [2] and highly significant (P = 0.0006 by Student's unpaired t-test). Our conclusions were unchanged if we limited consideration to strongly supported duplication events (those retained when bootstrap support was considered; see Additional file 3).

Bottom Line: We found that the first duplication in the AGPase large subunit family occurred early in the history of land plants, while the earliest small subunit duplication occurred after the divergence of monocots and eudicots.Instead, evolutionary constraints appear to be permanently relaxed for the large subunit relative to the small subunit.We discuss the phenotypes of mutants that alter some candidate sites and strategies for examining candidate sites of presently unknown function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Program in Plant Molecular and Cellular Biology and Horticultural Sciences, University of Florida, Gainesville, Florida 32610-0245, USA. gnick@ufl.edu

ABSTRACT

Background: ADP-glucose pyrophosphorylase (AGPase), which catalyses a rate limiting step in starch synthesis, is a heterotetramer comprised of two identical large and two identical small subunits in plants. Although the large and small subunits are equally sensitive to activity-altering amino acid changes when expressed in a bacterial system, the overall rate of non-synonymous evolution is approximately 2.7-fold greater for the large subunit than for the small subunit. Herein, we examine the basis for their different rates of evolution, the number of duplications in both large and small subunit genes and document changes in the patterns of AGPase evolution over time.

Results: We found that the first duplication in the AGPase large subunit family occurred early in the history of land plants, while the earliest small subunit duplication occurred after the divergence of monocots and eudicots. The large subunit also had a larger number of gene duplications than did the small subunit. The ancient duplications in the large subunit family raise concern about the saturation of synonymous substitutions, but estimates of the absolute rate of AGPase evolution were highly correlated with estimates of omega (the non-synonymous to synonymous rate ratio). Both subunits showed evidence for positive selection and relaxation of purifying selection after duplication, but these phenomena could not explain the different evolutionary rates of the two subunits. Instead, evolutionary constraints appear to be permanently relaxed for the large subunit relative to the small subunit. Both subunits exhibit branch-specific patterns of rate variation among sites.

Conclusion: These analyses indicate that the higher evolutionary rate of the plant AGPase large subunit reflects permanent relaxation of constraints relative to the small subunit and they show that the large subunit genes have undergone more gene duplications than small subunit genes. Candidate sites potentially responsible for functional divergence within each of the AGPase subunits were investigated by examining branch-specific patterns of rate variation. We discuss the phenotypes of mutants that alter some candidate sites and strategies for examining candidate sites of presently unknown function.

Show MeSH