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Evidence for adaptive variation at the genes coding for cytosolic phosphoglucose isomerase (PGIC) in Festuca ovina L.

Li, Yuan LU (2015)
Abstract
The gene (Pgi) encoding the enzyme phosphoglucose isomerase (PGI) which plays a central role in the main pathways of carbon metabolism has been shown to be of adaptive significance in a wide range of different species. Earlier studies of enzyme electromorph variation in the grass Festuca ovina suggest that variation in cytosolic PGI (PGIC) may be involved in the adaptive response of F. ovina to the alvar grassland microhabitat variation on the Baltic island of Öland, Sweden. PGIC is encoded by two genes in F. ovina: PgiC1 is “native” to F. ovina, whereas the PgiC2 gene has been horizontally acquired from the genus Poa. In the present thesis, different selection tests identified two codon (amino acid) sites (173, 200) as candidates for... (More)
The gene (Pgi) encoding the enzyme phosphoglucose isomerase (PGI) which plays a central role in the main pathways of carbon metabolism has been shown to be of adaptive significance in a wide range of different species. Earlier studies of enzyme electromorph variation in the grass Festuca ovina suggest that variation in cytosolic PGI (PGIC) may be involved in the adaptive response of F. ovina to the alvar grassland microhabitat variation on the Baltic island of Öland, Sweden. PGIC is encoded by two genes in F. ovina: PgiC1 is “native” to F. ovina, whereas the PgiC2 gene has been horizontally acquired from the genus Poa. In the present thesis, different selection tests identified two codon (amino acid) sites (173, 200) as candidates for positive selection within the PgiC1 gene. Sites 173 and 200 being under positive selection is supported by the predicted PGI structural consequence of the observed amino acid changes at these two sites in F. ovina, and by the experimentally determined functional consequence of amino acid changes at several human PGI sites that have 3-D structural locations similar to those of the two selected sites in F. ovina. The fact that the single nucleotide polymorphism (SNP) and amino acid variation at the two selected sites is significantly associated with fine-scale microhabitat variation in the alvar grasslands provides further support for a scenario of positive selection on sites 173 and 200 in F. ovina. Weak balancing selection, possibly targeting codon sites 173 and 200 (located within the 5’ “portion” of PgiC1) may have contributed to the high level of polymorphism within this portion of the PgiC1 sequence, which is significantly more polymorphic than the 3’ portion of the sequence. The transgenic PgiC2 locus is not present in all F. ovina individuals, and the presence/absence of the functional version of this locus was also found to be associated with the fine-scale alvar grassland microhabitat variation. In summary, the present thesis represents the first study that has investigated the adaptive variation at more than one cytosolic Pgi gene within a single species, and makes F. ovina the most well-studied plant species for the Pgi adaptive variation in natural populations. (Less)
Abstract (Swedish)
Popular Abstract in English

Darwin’s masterpiece “On the origin of species” describes how populations (one group of individuals from the same species that can easily mate with each other and that occupy the same geographic area) evolve through the process of natural selection, which can be shortly abbreviated as the survival of the fittest. More specifically, the individuals within one population may vary significantly from each other, and much of the variation is heritable. In one environment, compared to the less fitted individuals, those fitted ones have a higher chance to survive, to reproduce and therefore to pass on their heritable, beneficial traits to the next generation. As a result of this natural selection... (More)
Popular Abstract in English

Darwin’s masterpiece “On the origin of species” describes how populations (one group of individuals from the same species that can easily mate with each other and that occupy the same geographic area) evolve through the process of natural selection, which can be shortly abbreviated as the survival of the fittest. More specifically, the individuals within one population may vary significantly from each other, and much of the variation is heritable. In one environment, compared to the less fitted individuals, those fitted ones have a higher chance to survive, to reproduce and therefore to pass on their heritable, beneficial traits to the next generation. As a result of this natural selection process, the fitted individuals’ heritable, beneficial traits will become more common in their favorable environment, which will lead to one of the typical signatures of natural selection: the associations between the heritable, beneficial traits and the favorable environment. The action of natural selection may also leave its signature on the genetic materials of DNA that underlies the heritable traits.

In the present thesis, I focus on one common grass species Festuca ovina L. (common name: sheep’s fescue) in the alvar grassland of Öland (Sweden). On Öland, sheep’s fescue is one of the few species that survive through the full range of alvar grassland that varies significantly in its environmental conditions.

Earlier field surveys of enzyme (product of the molecular unit of DNA, gene) variation in sheep’s fescue on Öland showed significant association between the variation at one cytosolic enzyme phosphoglucose isomerase (PGI) that is fundamental to almost all life and the environment variation, suggesting natural selection on PGI variation.

In the present thesis, we explored further the suggested selection on PGI variation and we found signatures of natural selection at two genes (PgiC1 and PgiC2( f )) that encode (determine) PGI in sheep’s fescue. PgiC1 is regarded to be native to sheep’s fescue while PgiC2( f ) is suggested to be acquired from other related species.

At the PgiC1 gene, analyses of the DNA variation revealed signatures of selection at two codons (encoding unit of DNA). The two codons being under selection is also suggested by the identified association between the variation at these two codons and the environment variation on Öland.

At the PgiC2( f ) gene that was only found in some sheep’s fescue individuals, we have also observed an association between the presence/absence of this gene and the environment variation on Öland, suggesting selection on PgiC2( f ).

In summary, we acquired a better understanding of the natural selection on the PGI variation in sheep’s fescue, and our study represents the first study that has clearly demonstrated the signature of natural selection at more than one cytosolic Pgi genes (two variants of which are PgiC1 and PgiC2( f )) within one single species. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Wheat, Christopher, Department of Zoology, Stockholm University, Stockholm, Sweden
organization
publishing date
type
Thesis
publication status
published
subject
keywords
3-D protein structure, purifying selection, positive selection, cDNA sequences, local adaptation, alvar grasslands, Festuca ovina, Phosphoglucose isomerase, PgiC loci, SNPs, nucleotide polymorphism, horizontal gene transfer
pages
170 pages
publisher
Department of Biology, Lund University
defense location
Blue Hall, Ecology Building, Sölvegatan 37, Lund
defense date
2015-05-29 13:00:00
ISBN
978-91-7623-344-3
language
English
LU publication?
yes
id
ba9ce000-9c7e-4c1d-9b01-b1308ca10787 (old id 5337325)
date added to LUP
2016-04-04 11:07:58
date last changed
2018-11-21 21:02:52
@phdthesis{ba9ce000-9c7e-4c1d-9b01-b1308ca10787,
  abstract     = {{The gene (Pgi) encoding the enzyme phosphoglucose isomerase (PGI) which plays a central role in the main pathways of carbon metabolism has been shown to be of adaptive significance in a wide range of different species. Earlier studies of enzyme electromorph variation in the grass Festuca ovina suggest that variation in cytosolic PGI (PGIC) may be involved in the adaptive response of F. ovina to the alvar grassland microhabitat variation on the Baltic island of Öland, Sweden. PGIC is encoded by two genes in F. ovina: PgiC1 is “native” to F. ovina, whereas the PgiC2 gene has been horizontally acquired from the genus Poa. In the present thesis, different selection tests identified two codon (amino acid) sites (173, 200) as candidates for positive selection within the PgiC1 gene. Sites 173 and 200 being under positive selection is supported by the predicted PGI structural consequence of the observed amino acid changes at these two sites in F. ovina, and by the experimentally determined functional consequence of amino acid changes at several human PGI sites that have 3-D structural locations similar to those of the two selected sites in F. ovina. The fact that the single nucleotide polymorphism (SNP) and amino acid variation at the two selected sites is significantly associated with fine-scale microhabitat variation in the alvar grasslands provides further support for a scenario of positive selection on sites 173 and 200 in F. ovina. Weak balancing selection, possibly targeting codon sites 173 and 200 (located within the 5’ “portion” of PgiC1) may have contributed to the high level of polymorphism within this portion of the PgiC1 sequence, which is significantly more polymorphic than the 3’ portion of the sequence. The transgenic PgiC2 locus is not present in all F. ovina individuals, and the presence/absence of the functional version of this locus was also found to be associated with the fine-scale alvar grassland microhabitat variation. In summary, the present thesis represents the first study that has investigated the adaptive variation at more than one cytosolic Pgi gene within a single species, and makes F. ovina the most well-studied plant species for the Pgi adaptive variation in natural populations.}},
  author       = {{Li, Yuan}},
  isbn         = {{978-91-7623-344-3}},
  keywords     = {{3-D protein structure; purifying selection; positive selection; cDNA sequences; local adaptation; alvar grasslands; Festuca ovina; Phosphoglucose isomerase; PgiC loci; SNPs; nucleotide polymorphism; horizontal gene transfer}},
  language     = {{eng}},
  publisher    = {{Department of Biology, Lund University}},
  school       = {{Lund University}},
  title        = {{Evidence for adaptive variation at the genes coding for cytosolic phosphoglucose isomerase (PGIC) in Festuca ovina L.}},
  year         = {{2015}},
}