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Recurrent loss of specific introns during angiosperm evolution.

Wang H, Devos KM, Bennetzen JL - PLoS Genet. (2014)

Bottom Line: The two larger genomes, maize and sorghum, were found to have a higher rate of both recurrent loss and overall loss and/or gain than foxtail millet, rice or Brachypodium.Adjacent introns and small introns were found to be preferentially lost.This last result suggests that epigenetic status, as evidenced by a loss of methylated CG dinucleotides, may play a role in the process of intron loss.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, Georgia, United States of America.

ABSTRACT
Numerous instances of presence/absence variations for introns have been documented in eukaryotes, and some cases of recurrent loss of the same intron have been suggested. However, there has been no comprehensive or phylogenetically deep analysis of recurrent intron loss. Of 883 cases of intron presence/absence variation that we detected in five sequenced grass genomes, 93 were confirmed as recurrent losses and the rest could be explained by single losses (652) or single gains (118). No case of recurrent intron gain was observed. Deep phylogenetic analysis often indicated that apparent intron gains were actually numerous independent losses of the same intron. Recurrent loss exhibited extreme non-randomness, in that some introns were removed independently in many lineages. The two larger genomes, maize and sorghum, were found to have a higher rate of both recurrent loss and overall loss and/or gain than foxtail millet, rice or Brachypodium. Adjacent introns and small introns were found to be preferentially lost. Intron loss genes exhibited a high frequency of germ line or early embryogenesis expression. In addition, flanking exon A+T-richness and intron TG/CG ratios were higher in retained introns. This last result suggests that epigenetic status, as evidenced by a loss of methylated CG dinucleotides, may play a role in the process of intron loss. This study provides the first comprehensive analysis of recurrent intron loss, makes a series of novel findings on the patterns of recurrent intron loss during the evolution of the grass family, and provides insight into the molecular mechanism(s) underlying intron loss.

No MeSH data available.


Related in: MedlinePlus

Intron turnover frequencies and rates of (a) recurrent loss, (b) all loss and (c) single gain in five grass genomes.Branches of species tree represent evolutionary time. Frequency is defined as the number of events divided by the branch length and the unit branch length is million years (MY). Rate in a terminal node is measured by the number of events per intron per year. Rates are shown to the right of the vertical line and in the same line with the corresponding species codes. The 4-letter genome codes used are Zmay: Zea mays; Sbic: Sorghum bicolor; Sita: Setaria italica; Bdis: Brachypodium distachyon; Osat: Oryza sativa; Atha: Arabidopsis thaliana.
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pgen-1004843-g002: Intron turnover frequencies and rates of (a) recurrent loss, (b) all loss and (c) single gain in five grass genomes.Branches of species tree represent evolutionary time. Frequency is defined as the number of events divided by the branch length and the unit branch length is million years (MY). Rate in a terminal node is measured by the number of events per intron per year. Rates are shown to the right of the vertical line and in the same line with the corresponding species codes. The 4-letter genome codes used are Zmay: Zea mays; Sbic: Sorghum bicolor; Sita: Setaria italica; Bdis: Brachypodium distachyon; Osat: Oryza sativa; Atha: Arabidopsis thaliana.

Mentions: We identified 1026 intron loss and/or gain events in the 883 resolved PA intron groups, including 879 loss and 147 gain events. The number of events in the 93 recurrent loss groups was 206, or ∼20% of all events. We investigated lineage differentiation of the average frequency of intron loss (measured by the number of events/branch length) in the grass family and our results (Fig. 2 and Figure S6) revealed that (1) single loss occurred at a higher frequency than recurrent loss in all branches (counts/time are tested; log-linear model with time as offset, p-value <0.0001); (2) sorghum and maize had significantly (counts/time are tested; log-linear model with time as offset, p-value <0.0001) higher frequency of intron loss than foxtail millet, rice or Brachypodium in both single loss and recurrent loss groups; and (3) in the BEP clade, Brachypodium had a higher (not significant, p-value  = 0.22) frequency than rice.


Recurrent loss of specific introns during angiosperm evolution.

Wang H, Devos KM, Bennetzen JL - PLoS Genet. (2014)

Intron turnover frequencies and rates of (a) recurrent loss, (b) all loss and (c) single gain in five grass genomes.Branches of species tree represent evolutionary time. Frequency is defined as the number of events divided by the branch length and the unit branch length is million years (MY). Rate in a terminal node is measured by the number of events per intron per year. Rates are shown to the right of the vertical line and in the same line with the corresponding species codes. The 4-letter genome codes used are Zmay: Zea mays; Sbic: Sorghum bicolor; Sita: Setaria italica; Bdis: Brachypodium distachyon; Osat: Oryza sativa; Atha: Arabidopsis thaliana.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4256211&req=5

pgen-1004843-g002: Intron turnover frequencies and rates of (a) recurrent loss, (b) all loss and (c) single gain in five grass genomes.Branches of species tree represent evolutionary time. Frequency is defined as the number of events divided by the branch length and the unit branch length is million years (MY). Rate in a terminal node is measured by the number of events per intron per year. Rates are shown to the right of the vertical line and in the same line with the corresponding species codes. The 4-letter genome codes used are Zmay: Zea mays; Sbic: Sorghum bicolor; Sita: Setaria italica; Bdis: Brachypodium distachyon; Osat: Oryza sativa; Atha: Arabidopsis thaliana.
Mentions: We identified 1026 intron loss and/or gain events in the 883 resolved PA intron groups, including 879 loss and 147 gain events. The number of events in the 93 recurrent loss groups was 206, or ∼20% of all events. We investigated lineage differentiation of the average frequency of intron loss (measured by the number of events/branch length) in the grass family and our results (Fig. 2 and Figure S6) revealed that (1) single loss occurred at a higher frequency than recurrent loss in all branches (counts/time are tested; log-linear model with time as offset, p-value <0.0001); (2) sorghum and maize had significantly (counts/time are tested; log-linear model with time as offset, p-value <0.0001) higher frequency of intron loss than foxtail millet, rice or Brachypodium in both single loss and recurrent loss groups; and (3) in the BEP clade, Brachypodium had a higher (not significant, p-value  = 0.22) frequency than rice.

Bottom Line: The two larger genomes, maize and sorghum, were found to have a higher rate of both recurrent loss and overall loss and/or gain than foxtail millet, rice or Brachypodium.Adjacent introns and small introns were found to be preferentially lost.This last result suggests that epigenetic status, as evidenced by a loss of methylated CG dinucleotides, may play a role in the process of intron loss.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, Georgia, United States of America.

ABSTRACT
Numerous instances of presence/absence variations for introns have been documented in eukaryotes, and some cases of recurrent loss of the same intron have been suggested. However, there has been no comprehensive or phylogenetically deep analysis of recurrent intron loss. Of 883 cases of intron presence/absence variation that we detected in five sequenced grass genomes, 93 were confirmed as recurrent losses and the rest could be explained by single losses (652) or single gains (118). No case of recurrent intron gain was observed. Deep phylogenetic analysis often indicated that apparent intron gains were actually numerous independent losses of the same intron. Recurrent loss exhibited extreme non-randomness, in that some introns were removed independently in many lineages. The two larger genomes, maize and sorghum, were found to have a higher rate of both recurrent loss and overall loss and/or gain than foxtail millet, rice or Brachypodium. Adjacent introns and small introns were found to be preferentially lost. Intron loss genes exhibited a high frequency of germ line or early embryogenesis expression. In addition, flanking exon A+T-richness and intron TG/CG ratios were higher in retained introns. This last result suggests that epigenetic status, as evidenced by a loss of methylated CG dinucleotides, may play a role in the process of intron loss. This study provides the first comprehensive analysis of recurrent intron loss, makes a series of novel findings on the patterns of recurrent intron loss during the evolution of the grass family, and provides insight into the molecular mechanism(s) underlying intron loss.

No MeSH data available.


Related in: MedlinePlus