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Gene expression dosage regulation in an allopolyploid fish.

Matos I, Machado MP, Schartl M, Coelho MM - PLoS ONE (2015)

Bottom Line: One outstanding example of successful allopolyploidy is the endemic Iberian cyprinid Squalius alburnoides.We found that 64% of transcripts in juveniles' samples and 44% in liver samples differed less than twofold between diploid and triploid hybrids (similar expression).Therefore, an exact functional diploidization of the triploid genome does not occur, but a significant down regulation of gene expression in triploids was observed.

View Article: PubMed Central - PubMed

Affiliation: CE3C-Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal; University of Würzburg, Biozentrum, Physiological Chemistry, Am Hubland, Würzburg, Germany.

ABSTRACT
How allopolyploids are able not only to cope but profit from their condition is a question that remains elusive, but is of great importance within the context of successful allopolyploid evolution. One outstanding example of successful allopolyploidy is the endemic Iberian cyprinid Squalius alburnoides. Previously, based on the evaluation of a few genes, it was reported that the transcription levels between diploid and triploid S. alburnoides were similar. If this phenomenon occurs on a full genomic scale, a wide functional ''diploidization'' could be related to the success of these polyploids. We generated RNA-seq data from whole juvenile fish and from adult livers, to perform the first comparative quantitative transcriptomic analysis between diploid and triploid individuals of a vertebrate allopolyploid. Together with an assay to estimate relative expression per cell, it was possible to infer the relative sizes of transcriptomes. This showed that diploid and triploid S. alburnoides hybrids have similar liver transcriptome sizes. This in turn made it valid to directly compare the S. alburnoides RNA-seq transcript data sets and obtain a profile of dosage responses across the S. alburnoides transcriptome. We found that 64% of transcripts in juveniles' samples and 44% in liver samples differed less than twofold between diploid and triploid hybrids (similar expression). Yet, respectively 29% and 15% of transcripts presented accurate dosage compensation (PAA/PA expression ratio of 1 instead of 1.5). Therefore, an exact functional diploidization of the triploid genome does not occur, but a significant down regulation of gene expression in triploids was observed. However, for those genes with similar expression levels between diploids and triploids, expression is not globally strictly proportional to gene dosage nor is it set to a perfect diploid level. This quantitative expression flexibility may be a strong contributor to overcome the genomic shock, and be an immediate evolutionary advantage of allopolyploids.

No MeSH data available.


Related in: MedlinePlus

Comparative gene expression profiles in adult liver between the most common forms of the S. alburnoides complex.Logarithmized ratios of expression for each mapped transcript ware orderly plotted producing a crescent curve where positive values indicate transcripts with higher expression and negative values transcripts with lower expression. Median is marked with a cross and indicates if most values are positive or negative. For all comparisons, the difference in the number of lower vs higher expressed transcripts is significant (χ-test, p<0.001).The percentages of positive and negative values in each comparison are indicated.
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pone.0116309.g003: Comparative gene expression profiles in adult liver between the most common forms of the S. alburnoides complex.Logarithmized ratios of expression for each mapped transcript ware orderly plotted producing a crescent curve where positive values indicate transcripts with higher expression and negative values transcripts with lower expression. Median is marked with a cross and indicates if most values are positive or negative. For all comparisons, the difference in the number of lower vs higher expressed transcripts is significant (χ-test, p<0.001).The percentages of positive and negative values in each comparison are indicated.

Mentions: As for the juveniles, the expression profiles for the liver were obtained per genomotype, and pairwise comparisons were performed (Fig. 3). The comparison between triploid and diploid levels showed in all cases a significant difference in the number of higher and lower represented transcripts (χ-test, p<0.001) (Fig. 3A-3C), indicating that globally, ploidy level affects the quantitative expression pattern. Despite the higher gene dosage in the triploid, there is a higher amount of lower represented transcripts in liv-PAA compared to both diploid liv-PA and liv-AA (Fig. 3A-3B). This was consistent with what was observed in the whole body juvenile data set (Fig. 2). Moreover, there is a substantially high amount of higher represented transcripts in liv-PAA when compared to liv-PP (Fig. 3C).


Gene expression dosage regulation in an allopolyploid fish.

Matos I, Machado MP, Schartl M, Coelho MM - PLoS ONE (2015)

Comparative gene expression profiles in adult liver between the most common forms of the S. alburnoides complex.Logarithmized ratios of expression for each mapped transcript ware orderly plotted producing a crescent curve where positive values indicate transcripts with higher expression and negative values transcripts with lower expression. Median is marked with a cross and indicates if most values are positive or negative. For all comparisons, the difference in the number of lower vs higher expressed transcripts is significant (χ-test, p<0.001).The percentages of positive and negative values in each comparison are indicated.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4366067&req=5

pone.0116309.g003: Comparative gene expression profiles in adult liver between the most common forms of the S. alburnoides complex.Logarithmized ratios of expression for each mapped transcript ware orderly plotted producing a crescent curve where positive values indicate transcripts with higher expression and negative values transcripts with lower expression. Median is marked with a cross and indicates if most values are positive or negative. For all comparisons, the difference in the number of lower vs higher expressed transcripts is significant (χ-test, p<0.001).The percentages of positive and negative values in each comparison are indicated.
Mentions: As for the juveniles, the expression profiles for the liver were obtained per genomotype, and pairwise comparisons were performed (Fig. 3). The comparison between triploid and diploid levels showed in all cases a significant difference in the number of higher and lower represented transcripts (χ-test, p<0.001) (Fig. 3A-3C), indicating that globally, ploidy level affects the quantitative expression pattern. Despite the higher gene dosage in the triploid, there is a higher amount of lower represented transcripts in liv-PAA compared to both diploid liv-PA and liv-AA (Fig. 3A-3B). This was consistent with what was observed in the whole body juvenile data set (Fig. 2). Moreover, there is a substantially high amount of higher represented transcripts in liv-PAA when compared to liv-PP (Fig. 3C).

Bottom Line: One outstanding example of successful allopolyploidy is the endemic Iberian cyprinid Squalius alburnoides.We found that 64% of transcripts in juveniles' samples and 44% in liver samples differed less than twofold between diploid and triploid hybrids (similar expression).Therefore, an exact functional diploidization of the triploid genome does not occur, but a significant down regulation of gene expression in triploids was observed.

View Article: PubMed Central - PubMed

Affiliation: CE3C-Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal; University of Würzburg, Biozentrum, Physiological Chemistry, Am Hubland, Würzburg, Germany.

ABSTRACT
How allopolyploids are able not only to cope but profit from their condition is a question that remains elusive, but is of great importance within the context of successful allopolyploid evolution. One outstanding example of successful allopolyploidy is the endemic Iberian cyprinid Squalius alburnoides. Previously, based on the evaluation of a few genes, it was reported that the transcription levels between diploid and triploid S. alburnoides were similar. If this phenomenon occurs on a full genomic scale, a wide functional ''diploidization'' could be related to the success of these polyploids. We generated RNA-seq data from whole juvenile fish and from adult livers, to perform the first comparative quantitative transcriptomic analysis between diploid and triploid individuals of a vertebrate allopolyploid. Together with an assay to estimate relative expression per cell, it was possible to infer the relative sizes of transcriptomes. This showed that diploid and triploid S. alburnoides hybrids have similar liver transcriptome sizes. This in turn made it valid to directly compare the S. alburnoides RNA-seq transcript data sets and obtain a profile of dosage responses across the S. alburnoides transcriptome. We found that 64% of transcripts in juveniles' samples and 44% in liver samples differed less than twofold between diploid and triploid hybrids (similar expression). Yet, respectively 29% and 15% of transcripts presented accurate dosage compensation (PAA/PA expression ratio of 1 instead of 1.5). Therefore, an exact functional diploidization of the triploid genome does not occur, but a significant down regulation of gene expression in triploids was observed. However, for those genes with similar expression levels between diploids and triploids, expression is not globally strictly proportional to gene dosage nor is it set to a perfect diploid level. This quantitative expression flexibility may be a strong contributor to overcome the genomic shock, and be an immediate evolutionary advantage of allopolyploids.

No MeSH data available.


Related in: MedlinePlus