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The landscape of nucleotide polymorphism among 13,500 genes of the conifer picea glauca, relationships with functions, and comparison with medicago truncatula.

Pavy N, Deschênes A, Blais S, Lavigne P, Beaulieu J, Isabel N, Mackay J, Bousquet J - Genome Biol Evol (2013)

Bottom Line: Conifer-specific sequences were also generally associated with the highest A/S ratios.These patterns confirm that the breadth of gene expression is a contributing factor to the evolution of nucleotide polymorphism.However, a number of families with high A/S ratios were found specific to P. glauca, suggesting cases of divergent evolution at the functional level.

View Article: PubMed Central - PubMed

Affiliation: Canada Research Chair in Forest and Environmental Genomics, Centre for Forest Research and Institute for Systems and Integrative Biology, Université Laval, Québec, Canada.

ABSTRACT
Gene families differ in composition, expression, and chromosomal organization between conifers and angiosperms, but little is known regarding nucleotide polymorphism. Using various sequencing strategies, an atlas of 212k high-confidence single nucleotide polymorphisms (SNPs) with a validation rate of more than 92% was developed for the conifer white spruce (Picea glauca). Nonsynonymous and synonymous SNPs were annotated over the corresponding 13,498 white spruce genes representative of 2,457 known gene families. Patterns of nucleotide polymorphisms were analyzed by estimating the ratio of nonsynonymous to synonymous numbers of substitutions per site (A/S). A general excess of synonymous SNPs was expected and observed. However, the analysis from several perspectives enabled to identify groups of genes harboring an excess of nonsynonymous SNPs, thus potentially under positive selection. Four known gene families harbored such an excess: dehydrins, ankyrin-repeats, AP2/DREB, and leucine-rich repeat. Conifer-specific sequences were also generally associated with the highest A/S ratios. A/S values were also distributed asymmetrically across genes specifically expressed in megagametophytes, roots, or in both, harboring on average an excess of nonsynonymous SNPs. These patterns confirm that the breadth of gene expression is a contributing factor to the evolution of nucleotide polymorphism. The A/S ratios of Medicago truncatula genes were also analyzed: several gene families shared between P. glauca and M. truncatula data sets had similar excess of synonymous or nonsynonymous SNPs. However, a number of families with high A/S ratios were found specific to P. glauca, suggesting cases of divergent evolution at the functional level.

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Relationship between co-expressed genes and their imbalance in A/S ratios in Picea glauca. (a) Expression profiles of genes more represented among sequences with the lowest A/S values. The pictures represent the expression patterns in buds (B), needles (N), mature (Mx) or juvenile (Jx) xylem, phloem (P), roots (R), megagametophytes (M), and embryogenic cells (E). Due to space limitation, only four examples are showed out of the eight expression clusters encompassing genes with low A/S values. (b) The histogram illustrates the 12 co-expression clusters with a significant overrepresentation among genes with the highest or lowest A/S values (gene set enrichment analysis, Fisher’s exact test, two-tailed, adjusted Ps < 0.01). (c) Expression profiles of the genes from the four co-expression clusters of genes with the highest A/S values.
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evt143-F6: Relationship between co-expressed genes and their imbalance in A/S ratios in Picea glauca. (a) Expression profiles of genes more represented among sequences with the lowest A/S values. The pictures represent the expression patterns in buds (B), needles (N), mature (Mx) or juvenile (Jx) xylem, phloem (P), roots (R), megagametophytes (M), and embryogenic cells (E). Due to space limitation, only four examples are showed out of the eight expression clusters encompassing genes with low A/S values. (b) The histogram illustrates the 12 co-expression clusters with a significant overrepresentation among genes with the highest or lowest A/S values (gene set enrichment analysis, Fisher’s exact test, two-tailed, adjusted Ps < 0.01). (c) Expression profiles of the genes from the four co-expression clusters of genes with the highest A/S values.

Mentions: We identified 12 different co-expression clusters that had a significant abundance of genes with the highest or lowest A/S ratios (gene set enrichment analysis; Fisher’s exact test, two-tailed, adjusted Ps < 0.01) (fig. 6b). Those co-expression clusters (8 out 12) with the lowest A/S values were overpopulated by genes with high expression levels in several organs (fig. 6a). For example, the 727 genes in cluster 26 were highly expressed in seven tissues but weakly expressed in embryogenic cells; this cluster had 5.5% of its genes with the lowest A/S values (average 0.31) and 1.8% of its genes with the highest A/S values (average 2.12) (fig. 6a). Also, the 737 genes in cluster 23 were highly expressed in buds, roots, megagametophytes, embryogenic cells but weakly to moderately expressed in needles, xylem, and phelloderm; they included more than 12% of genes with the lowest A/S ratios with an average A/S of 0.08 (fig. 6a). On the other hand, the four other clusters had, on average, genes with higher A/S ratios, and they were overpopulated by genes expressed in a single organ (mostly root, needle, or megagametophyte) or in two organs (root and megagametophyte) (fig. 6c). For example, genes in cluster 15 (fig. 6c) were mainly expressed in roots and included 73 genes classified among those with the highest A/S ratios with an average of 1.98, which would be indicative of positive selection (fig. 6b). Sequence similarity searches conducted on this subset of 73 genes resulted in putative functions for only 15 sequences, a fraction (20.5%) which is well below the expected proportion (63.8%) (χ2 = 55.4, adjusted P value <0.01). We identified a defensin sequence with a close homolog expressed in Scots pine roots that was shown to have antimicrobial properties (Kovaleva et al. 2009) and two other sequences related to defense mechanisms (an LRR and a MAP kinase kinase), whereas all the other sequences did not show obvious functional annotations, which suggests that some of these are likely to be conifer-specific genes.Fig. 6.—


The landscape of nucleotide polymorphism among 13,500 genes of the conifer picea glauca, relationships with functions, and comparison with medicago truncatula.

Pavy N, Deschênes A, Blais S, Lavigne P, Beaulieu J, Isabel N, Mackay J, Bousquet J - Genome Biol Evol (2013)

Relationship between co-expressed genes and their imbalance in A/S ratios in Picea glauca. (a) Expression profiles of genes more represented among sequences with the lowest A/S values. The pictures represent the expression patterns in buds (B), needles (N), mature (Mx) or juvenile (Jx) xylem, phloem (P), roots (R), megagametophytes (M), and embryogenic cells (E). Due to space limitation, only four examples are showed out of the eight expression clusters encompassing genes with low A/S values. (b) The histogram illustrates the 12 co-expression clusters with a significant overrepresentation among genes with the highest or lowest A/S values (gene set enrichment analysis, Fisher’s exact test, two-tailed, adjusted Ps < 0.01). (c) Expression profiles of the genes from the four co-expression clusters of genes with the highest A/S values.
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Related In: Results  -  Collection

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evt143-F6: Relationship between co-expressed genes and their imbalance in A/S ratios in Picea glauca. (a) Expression profiles of genes more represented among sequences with the lowest A/S values. The pictures represent the expression patterns in buds (B), needles (N), mature (Mx) or juvenile (Jx) xylem, phloem (P), roots (R), megagametophytes (M), and embryogenic cells (E). Due to space limitation, only four examples are showed out of the eight expression clusters encompassing genes with low A/S values. (b) The histogram illustrates the 12 co-expression clusters with a significant overrepresentation among genes with the highest or lowest A/S values (gene set enrichment analysis, Fisher’s exact test, two-tailed, adjusted Ps < 0.01). (c) Expression profiles of the genes from the four co-expression clusters of genes with the highest A/S values.
Mentions: We identified 12 different co-expression clusters that had a significant abundance of genes with the highest or lowest A/S ratios (gene set enrichment analysis; Fisher’s exact test, two-tailed, adjusted Ps < 0.01) (fig. 6b). Those co-expression clusters (8 out 12) with the lowest A/S values were overpopulated by genes with high expression levels in several organs (fig. 6a). For example, the 727 genes in cluster 26 were highly expressed in seven tissues but weakly expressed in embryogenic cells; this cluster had 5.5% of its genes with the lowest A/S values (average 0.31) and 1.8% of its genes with the highest A/S values (average 2.12) (fig. 6a). Also, the 737 genes in cluster 23 were highly expressed in buds, roots, megagametophytes, embryogenic cells but weakly to moderately expressed in needles, xylem, and phelloderm; they included more than 12% of genes with the lowest A/S ratios with an average A/S of 0.08 (fig. 6a). On the other hand, the four other clusters had, on average, genes with higher A/S ratios, and they were overpopulated by genes expressed in a single organ (mostly root, needle, or megagametophyte) or in two organs (root and megagametophyte) (fig. 6c). For example, genes in cluster 15 (fig. 6c) were mainly expressed in roots and included 73 genes classified among those with the highest A/S ratios with an average of 1.98, which would be indicative of positive selection (fig. 6b). Sequence similarity searches conducted on this subset of 73 genes resulted in putative functions for only 15 sequences, a fraction (20.5%) which is well below the expected proportion (63.8%) (χ2 = 55.4, adjusted P value <0.01). We identified a defensin sequence with a close homolog expressed in Scots pine roots that was shown to have antimicrobial properties (Kovaleva et al. 2009) and two other sequences related to defense mechanisms (an LRR and a MAP kinase kinase), whereas all the other sequences did not show obvious functional annotations, which suggests that some of these are likely to be conifer-specific genes.Fig. 6.—

Bottom Line: Conifer-specific sequences were also generally associated with the highest A/S ratios.These patterns confirm that the breadth of gene expression is a contributing factor to the evolution of nucleotide polymorphism.However, a number of families with high A/S ratios were found specific to P. glauca, suggesting cases of divergent evolution at the functional level.

View Article: PubMed Central - PubMed

Affiliation: Canada Research Chair in Forest and Environmental Genomics, Centre for Forest Research and Institute for Systems and Integrative Biology, Université Laval, Québec, Canada.

ABSTRACT
Gene families differ in composition, expression, and chromosomal organization between conifers and angiosperms, but little is known regarding nucleotide polymorphism. Using various sequencing strategies, an atlas of 212k high-confidence single nucleotide polymorphisms (SNPs) with a validation rate of more than 92% was developed for the conifer white spruce (Picea glauca). Nonsynonymous and synonymous SNPs were annotated over the corresponding 13,498 white spruce genes representative of 2,457 known gene families. Patterns of nucleotide polymorphisms were analyzed by estimating the ratio of nonsynonymous to synonymous numbers of substitutions per site (A/S). A general excess of synonymous SNPs was expected and observed. However, the analysis from several perspectives enabled to identify groups of genes harboring an excess of nonsynonymous SNPs, thus potentially under positive selection. Four known gene families harbored such an excess: dehydrins, ankyrin-repeats, AP2/DREB, and leucine-rich repeat. Conifer-specific sequences were also generally associated with the highest A/S ratios. A/S values were also distributed asymmetrically across genes specifically expressed in megagametophytes, roots, or in both, harboring on average an excess of nonsynonymous SNPs. These patterns confirm that the breadth of gene expression is a contributing factor to the evolution of nucleotide polymorphism. The A/S ratios of Medicago truncatula genes were also analyzed: several gene families shared between P. glauca and M. truncatula data sets had similar excess of synonymous or nonsynonymous SNPs. However, a number of families with high A/S ratios were found specific to P. glauca, suggesting cases of divergent evolution at the functional level.

Show MeSH
Related in: MedlinePlus