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Transcriptomic Responses of the Heart and Brain to Anoxia in the Western Painted Turtle.

Keenan SW, Hill CA, Kandoth C, Buck LT, Warren DE - PLoS ONE (2015)

Bottom Line: Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle.The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression).Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Saint Louis University, St. Louis, Missouri, United States of America.

ABSTRACT
Painted turtles are the most anoxia-tolerant tetrapods known, capable of surviving without oxygen for more than four months at 3°C and 30 hours at 20°C. To investigate the transcriptomic basis of this ability, we used RNA-seq to quantify mRNA expression in the painted turtle ventricle and telencephalon after 24 hours of anoxia at 19°C. Reads were obtained from 22,174 different genes, 13,236 of which were compared statistically between treatments for each tissue. Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle. The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression). When treatment effects were compared between anoxic and normoxic conditions in the two tissue types, 31 genes were increased (≥ 2x change) and 2 were decreased (≤ 0.5x change). Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest. No genes related to ion channels, synaptic transmission, cardiac contractility or excitation-contraction coupling changed. The generalized expression pattern in telencephalon and across tissues, but not in ventricle, correlated with the predicted metabolic cost of transcription, with the shortest genes and those with the fewest exons showing the largest increases in expression.

No MeSH data available.


Related in: MedlinePlus

Sequence length as a predictor of increased gene abundance.(A) In telencephalon, longer genes show smaller changes in FPKM. The inset shows the linear regression analysis comparing the ln (delta FPKM) vs. ln (sequence length). (B) In ventricle, there is no significant relationship between delta FPKM and sequence length (regression not shown). The arrow indicates the expression value and sequence length of a GLUT isoform (Slc2a1,3,14). Excluding that point did not decrease the P-value appreciably. (C) When genes from all tissues were compared between treatments (treatment effects), sequence length is a significant predictor of delta FPKM. The values in parentheses indicate P-values and R2 values if the GLUT isoform (indicated by the arrowhead) is excluded from the linear regression analysis. Note: Although sequence length is the independent variable, it is shown on the y-axis to be consistent with reference [33]. The regression analyses (see insets in A and C) were conducted with ln (sequence length) as the independent variable. All significantly upregulated genes were included, regardless of fold-change.
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pone.0131669.g005: Sequence length as a predictor of increased gene abundance.(A) In telencephalon, longer genes show smaller changes in FPKM. The inset shows the linear regression analysis comparing the ln (delta FPKM) vs. ln (sequence length). (B) In ventricle, there is no significant relationship between delta FPKM and sequence length (regression not shown). The arrow indicates the expression value and sequence length of a GLUT isoform (Slc2a1,3,14). Excluding that point did not decrease the P-value appreciably. (C) When genes from all tissues were compared between treatments (treatment effects), sequence length is a significant predictor of delta FPKM. The values in parentheses indicate P-values and R2 values if the GLUT isoform (indicated by the arrowhead) is excluded from the linear regression analysis. Note: Although sequence length is the independent variable, it is shown on the y-axis to be consistent with reference [33]. The regression analyses (see insets in A and C) were conducted with ln (sequence length) as the independent variable. All significantly upregulated genes were included, regardless of fold-change.

Mentions: Transcriptional costs are directly related to gene length and splicing. When the absolute change in FPKM values for each elevated transcript was compared to their sequence length (Fig 5), longer genes had the smallest change in FPKM values in telencephalon (Fig 5A) and between treatment values across tissues (Fig 5C). A similar relationship between exon density, a predictor of splicing requirement, and change in FPKM was also observed for telencephalon (Fig 6A), but not for ventricle (Fig 6B) or between the treatments of the two tissues (Fig 6C). Additionally, genes that significantly decreased expression during anoxia, across treatments, contained a significantly (t-test, P-value = 0.007, t = 2.848, df = 46) greater number of exons (mean = 10.1 ± 2.7) compared to increased genes (mean = 4.8 ± 0.56) (Fig 7).


Transcriptomic Responses of the Heart and Brain to Anoxia in the Western Painted Turtle.

Keenan SW, Hill CA, Kandoth C, Buck LT, Warren DE - PLoS ONE (2015)

Sequence length as a predictor of increased gene abundance.(A) In telencephalon, longer genes show smaller changes in FPKM. The inset shows the linear regression analysis comparing the ln (delta FPKM) vs. ln (sequence length). (B) In ventricle, there is no significant relationship between delta FPKM and sequence length (regression not shown). The arrow indicates the expression value and sequence length of a GLUT isoform (Slc2a1,3,14). Excluding that point did not decrease the P-value appreciably. (C) When genes from all tissues were compared between treatments (treatment effects), sequence length is a significant predictor of delta FPKM. The values in parentheses indicate P-values and R2 values if the GLUT isoform (indicated by the arrowhead) is excluded from the linear regression analysis. Note: Although sequence length is the independent variable, it is shown on the y-axis to be consistent with reference [33]. The regression analyses (see insets in A and C) were conducted with ln (sequence length) as the independent variable. All significantly upregulated genes were included, regardless of fold-change.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4493013&req=5

pone.0131669.g005: Sequence length as a predictor of increased gene abundance.(A) In telencephalon, longer genes show smaller changes in FPKM. The inset shows the linear regression analysis comparing the ln (delta FPKM) vs. ln (sequence length). (B) In ventricle, there is no significant relationship between delta FPKM and sequence length (regression not shown). The arrow indicates the expression value and sequence length of a GLUT isoform (Slc2a1,3,14). Excluding that point did not decrease the P-value appreciably. (C) When genes from all tissues were compared between treatments (treatment effects), sequence length is a significant predictor of delta FPKM. The values in parentheses indicate P-values and R2 values if the GLUT isoform (indicated by the arrowhead) is excluded from the linear regression analysis. Note: Although sequence length is the independent variable, it is shown on the y-axis to be consistent with reference [33]. The regression analyses (see insets in A and C) were conducted with ln (sequence length) as the independent variable. All significantly upregulated genes were included, regardless of fold-change.
Mentions: Transcriptional costs are directly related to gene length and splicing. When the absolute change in FPKM values for each elevated transcript was compared to their sequence length (Fig 5), longer genes had the smallest change in FPKM values in telencephalon (Fig 5A) and between treatment values across tissues (Fig 5C). A similar relationship between exon density, a predictor of splicing requirement, and change in FPKM was also observed for telencephalon (Fig 6A), but not for ventricle (Fig 6B) or between the treatments of the two tissues (Fig 6C). Additionally, genes that significantly decreased expression during anoxia, across treatments, contained a significantly (t-test, P-value = 0.007, t = 2.848, df = 46) greater number of exons (mean = 10.1 ± 2.7) compared to increased genes (mean = 4.8 ± 0.56) (Fig 7).

Bottom Line: Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle.The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression).Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Saint Louis University, St. Louis, Missouri, United States of America.

ABSTRACT
Painted turtles are the most anoxia-tolerant tetrapods known, capable of surviving without oxygen for more than four months at 3°C and 30 hours at 20°C. To investigate the transcriptomic basis of this ability, we used RNA-seq to quantify mRNA expression in the painted turtle ventricle and telencephalon after 24 hours of anoxia at 19°C. Reads were obtained from 22,174 different genes, 13,236 of which were compared statistically between treatments for each tissue. Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle. The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression). When treatment effects were compared between anoxic and normoxic conditions in the two tissue types, 31 genes were increased (≥ 2x change) and 2 were decreased (≤ 0.5x change). Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest. No genes related to ion channels, synaptic transmission, cardiac contractility or excitation-contraction coupling changed. The generalized expression pattern in telencephalon and across tissues, but not in ventricle, correlated with the predicted metabolic cost of transcription, with the shortest genes and those with the fewest exons showing the largest increases in expression.

No MeSH data available.


Related in: MedlinePlus