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. 2012 Aug 17:13:406.
doi: 10.1186/1471-2164-13-406.

Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective

Aureliano Bombarely  1 , Kieron D Edwards, Juan Sanchez-Tamburrino, Lukas A Mueller
Affiliations

Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective

Aureliano Bombarely et al. BMC Genomics. .

Abstract

Background: Polyploidization is an important mechanism in plant evolution. By analyzing the leaf transcriptomes taken from the allotetraploid Nicotiana tabacum (tobacco) and parental genome donors, N. sylvesteris (S-Genome) and N. tomentosiformis (T-Genome), a phylogenomic approach was taken to map the fate of homeologous gene pairs in this plant.

Results: A comparison between the genes present in the leaf transcriptomes of N. tabacum and modern day representatives of its progenitor species demonstrated that only 33% of assembled transcripts could be distinguished based on their sequences. A large majority of the genes (83.6% of the non parent distinguishable and 87.2% of the phylogenetic topology analyzed clusters) expressed above background level (more than 5 reads) showed similar overall expression levels. Homeologous sequences could be identified for 968 gene clusters, and 90% (6% of all genes) of the set maintained expression of only one of the tobacco homeologs. When both homeologs were expressed, only 15% (0.5% of the total) showed evidence of differential expression, providing limited evidence of subfunctionalization. Comparing the rate of synonymous nucleotide substitution (Ks) and non-synonymous nucleotide substitution (Kn) provided limited evidence for positive selection during the evolution of tobacco since the polyploidization event took place.

Conclusions: Polyploidization is a powerful mechanism for plant speciation that can occur during one generation; however millions of generations may be necessary for duplicate genes to acquire a new function. Analysis of the tobacco leaf transcriptome reveals that polyploidization, even in a young tetraploid such as tobacco, can lead to complex changes in gene expression. Gene loss and gene silencing, or subfunctionalization may explain why both homeologs are not expressed by the associated genes. With Whole Genome Duplication (WGD) events, polyploid genomes usually maintain a high percentage of gene duplicates. The data provided little evidence of preferential maintenance of gene expression from either the T- or S-genome. Additionally there was little evidence of neofunctionalization in Nicotiana tabacum suggesting it occurs at a low frequency in young polyploidy.

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Figures

Figure 1
Figure 1
Nicotiana EST assemblies. Chart showing the number of contigs in EST assemblies generated with GsAssembler using minimum overlap identity levels between 75 and 99% (see Methods). Assemblies were carried out from four data sets; N. sylvesteris (green), N. tomentosiformis (blue), N. tabacum (red) and a hybrid set of N. sylvesteris and N. tomentosiformis (brown) sequences.
Figure 2
Figure 2
Phylogenomic analysis of Nicotiana gene clusters. Bar chart showing the number of Nicotiana genes that were present in a set of pre-defined phylogenetic tree topologies. Genes from the N. tabacum, N. sylvesteris and N. tomentosiformis assemblies were clustered and phylogenetic trees for each cluster were generated by Maximum Likelihood (ML; black bars) and Neighbour Joining (NJ; open bars) methods using S. lycopersicum as an out-group. The different tree topologies are shown along the x-axis with N. tabacum (A; Ntab) N. sylvesteris (B; Nsyl), N. tomentosiformis (C; Ntom) and S. lycopersicum (Slyc) genes represented in text and/or dendrogram form.
Figure 3
Figure 3
Gene Ontology analysis of Nicotiana gene clusters. Plot showing the percentage of Nicotiana gene clusters annotated with level 2 (A) and level 3 (B) Biological Process Gene Ontology terms for all gene clusters and each of the main phylogenetic tree topologies (AB_AC, AB_C, AC_B and BC_A). Bars are coloured according to topology group (see inset key for identification).
Figure 4
Figure 4
Expression level of Nicotiana gene pairs. Scatter plot showing the expression level (RPKM) for the N. sylvesteris / S genome gene (x-axis) versus N. tomentosiformis / T genome gene (y-axis) for homologous gene pairs (open red circles) and homeologous N. tabacum gene pairs (closed black circles). Solid black line across diagonal represents no difference in gene expression level between species.
Figure 5
Figure 5
Nucleotide substitution rates in Nicotiana genes. Frequency histograms showing the rate of synonymous nucleotide substitutions (Ks) in orthologous genes between N. tabacum and S. lycopersicum (A), N. sylvesteris and N. tomentosiformis (B), N. tabacum and N. sylvesteris (C) and N. tabacum and N. tomentosiformis (D).
Figure 6
Figure 6
Evolutionary rates in Nicotiana genes from different Gene Ontology groups. Non-synonymous: synonymous nucleotide subtraction ratio (ω) values for Nicotiana genes separated according to their Level 2 (A) and Level 3 (B) Biological Process, Level 2 (C) and Level 4 (D) Cellular Component and Level 2 (E) and Level 3 (F) Molecular Function Gene Ontology annotations. Omega values for comparisons between homologous N. sylvesteris and N. tomentosiformis gene pairs (black circles), N. tabacum and N. sylvesteris gene pairs (green circles) and N. tabacum and N. tomentosiformis gene pairs (red circles) are shown.
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