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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 locations in genes from five grass genomes: (a) all introns, (b) recurrent loss introns and (c) PA introns.The CDS lengths in genes are normalized to 1 and the positions of introns are calculated as (length from translation start)/(total size of CDS). The normalized gene is partitioned into 10 intervals (X-axis) and Y-axis values are the percentage of introns in these intervals. Error bars in (b) and (c) represent one sd from interval mean values (circle), where mean and sd are calculated by resampling with replacement (1000 times) from the entire intron set.
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pgen-1004843-g003: Intron locations in genes from five grass genomes: (a) all introns, (b) recurrent loss introns and (c) PA introns.The CDS lengths in genes are normalized to 1 and the positions of introns are calculated as (length from translation start)/(total size of CDS). The normalized gene is partitioned into 10 intervals (X-axis) and Y-axis values are the percentage of introns in these intervals. Error bars in (b) and (c) represent one sd from interval mean values (circle), where mean and sd are calculated by resampling with replacement (1000 times) from the entire intron set.

Mentions: We normalized for gene size and investigated the distribution of intron loss or gain along each gene (Fig. 3 and Figure S8). The locations of all introns in all gene models of the six genomes showed a relatively even distribution, with the two termini, i.e. (0, 0.1) and (0.9, 1.0) of the total length of a gene when calculating from the 5′ end, exhibiting lower values (Fig. 3a). Under-representation of intron loss and/or gain at the gene termini was also observed in recurrent (Fig. 3b) and PA intron groups (Fig, 3c): the percentage of recurrently lost and PA introns located at (0, 0.1) and PA introns at (0.9, 1.0) was lower than expected based on the mean and sd from 1000 resamplings from all introns. In the all loss (recurrent + single) groups, we observed (0.2, 0.3) had a percentage higher than expected based on the resampling results (Figure S8).


Recurrent loss of specific introns during angiosperm evolution.

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

Intron locations in genes from five grass genomes: (a) all introns, (b) recurrent loss introns and (c) PA introns.The CDS lengths in genes are normalized to 1 and the positions of introns are calculated as (length from translation start)/(total size of CDS). The normalized gene is partitioned into 10 intervals (X-axis) and Y-axis values are the percentage of introns in these intervals. Error bars in (b) and (c) represent one sd from interval mean values (circle), where mean and sd are calculated by resampling with replacement (1000 times) from the entire intron set.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256211&req=5

pgen-1004843-g003: Intron locations in genes from five grass genomes: (a) all introns, (b) recurrent loss introns and (c) PA introns.The CDS lengths in genes are normalized to 1 and the positions of introns are calculated as (length from translation start)/(total size of CDS). The normalized gene is partitioned into 10 intervals (X-axis) and Y-axis values are the percentage of introns in these intervals. Error bars in (b) and (c) represent one sd from interval mean values (circle), where mean and sd are calculated by resampling with replacement (1000 times) from the entire intron set.
Mentions: We normalized for gene size and investigated the distribution of intron loss or gain along each gene (Fig. 3 and Figure S8). The locations of all introns in all gene models of the six genomes showed a relatively even distribution, with the two termini, i.e. (0, 0.1) and (0.9, 1.0) of the total length of a gene when calculating from the 5′ end, exhibiting lower values (Fig. 3a). Under-representation of intron loss and/or gain at the gene termini was also observed in recurrent (Fig. 3b) and PA intron groups (Fig, 3c): the percentage of recurrently lost and PA introns located at (0, 0.1) and PA introns at (0.9, 1.0) was lower than expected based on the mean and sd from 1000 resamplings from all introns. In the all loss (recurrent + single) groups, we observed (0.2, 0.3) had a percentage higher than expected based on the resampling results (Figure S8).

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