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The transcriptome of Utricularia vulgaris, a rootless plant with minimalist genome, reveals extreme alternative splicing and only moderate sequence similarity with Utricularia gibba.

Bárta J, Stone JD, Pech J, Sirová D, Adamec L, Campbell MA, Štorchová H - BMC Plant Biol. (2015)

Bottom Line: We also found a strong correspondence in the presence or absence of root-associated genes between the U. vulgaris transcriptome and U. gibba genome, which indicated that the loss of some root-specific genes had occurred before the divergence of the two rootless species.The species-rich genus Utricularia offers a unique opportunity to study adaptations related to the environment and carnivorous habit and also evolutionary processes responsible for considerable genome reduction.Our study is the first comparison of two global sequence data sets in Utricularia.

View Article: PubMed Central - PubMed

ABSTRACT

Background: The species of Utricularia attract attention not only owing to their carnivorous lifestyle, but also due to an elevated substitution rate and a dynamic evolution of genome size leading to its dramatic reduction. To better understand the evolutionary dynamics of genome size and content as well as the great physiological plasticity in this mostly aquatic carnivorous genus, we analyzed the transcriptome of Utricularia vulgaris, a temperate species with well characterized physiology and ecology. We compared its transcriptome, namely gene content and overall transcript profile, with a previously described transcriptome of Utricularia gibba, a congener possessing one of the smallest angiosperm genomes.

Results: We sequenced a normalized cDNA library prepared from total RNA extracted from shoots of U. vulgaris including leaves and traps, cultivated under sterile or outdoor conditions. 454 pyrosequencing resulted in more than 1,400,000 reads which were assembled into 41,407 isotigs in 19,522 isogroups. We observed high transcript variation in several isogroups explained by multiple loci and/or alternative splicing. The comparison of U. vulgaris and U. gibba transcriptomes revealed a similar distribution of GO categories among expressed genes, despite the differences in transcriptome preparation. We also found a strong correspondence in the presence or absence of root-associated genes between the U. vulgaris transcriptome and U. gibba genome, which indicated that the loss of some root-specific genes had occurred before the divergence of the two rootless species.

Conclusions: The species-rich genus Utricularia offers a unique opportunity to study adaptations related to the environment and carnivorous habit and also evolutionary processes responsible for considerable genome reduction. We show that a transcriptome may approximate the genome for gene content or gene duplication estimation. Our study is the first comparison of two global sequence data sets in Utricularia.

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Taxonomic assignment. Dendrogram showing number of MEGAN assigned U. vulgaris(A) and U. gibba(B) isotigs.
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Fig2: Taxonomic assignment. Dendrogram showing number of MEGAN assigned U. vulgaris(A) and U. gibba(B) isotigs.

Mentions: More than 99% of the isotigs with significant hits were assigned by MEGAN to plants (Streptophytes) in both U. vulgaris and U. gibba. All remaining isotigs (38 in U. vulgaris and 87 in U. gibba) belonged to Fungi, Metazoa, unicellular eukaryotes, and prokaryotes (Figure 2). The taxonomic diversity of singletons was much higher: 5.3% and 10.6% of singletons with significant hits were assigned outside the Streptophytes in U. vulgaris, and U. gibba, respectively (Additional file 1). The non-plant sequences were mostly derived from microbial commensals, as well as a minor fraction from animal (fish, worm) RNA contamination. The very low proportion of prokaryotic sequences was due to the polyA+ RNA used to prepare cDNA. As prokaryotic mRNAs rarely contain polyA+ tails, they were mostly eliminated. The proportion of non-plant transcripts is probably higher among singletons, because many of them may not have produced statistically significant hits due to incomplete microbial records in public databases. The abundance of microbe-derived transcripts was higher in the U. gibba transcriptome prepared only from plants grown under natural conditions and colonized with microbes. In contrast, the U. vulgaris transcriptome was constructed from a pooled RNA sample prepared from the plants cultivated under both sterile and non-sterile conditions.Figure 2


The transcriptome of Utricularia vulgaris, a rootless plant with minimalist genome, reveals extreme alternative splicing and only moderate sequence similarity with Utricularia gibba.

Bárta J, Stone JD, Pech J, Sirová D, Adamec L, Campbell MA, Štorchová H - BMC Plant Biol. (2015)

Taxonomic assignment. Dendrogram showing number of MEGAN assigned U. vulgaris(A) and U. gibba(B) isotigs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4358910&req=5

Fig2: Taxonomic assignment. Dendrogram showing number of MEGAN assigned U. vulgaris(A) and U. gibba(B) isotigs.
Mentions: More than 99% of the isotigs with significant hits were assigned by MEGAN to plants (Streptophytes) in both U. vulgaris and U. gibba. All remaining isotigs (38 in U. vulgaris and 87 in U. gibba) belonged to Fungi, Metazoa, unicellular eukaryotes, and prokaryotes (Figure 2). The taxonomic diversity of singletons was much higher: 5.3% and 10.6% of singletons with significant hits were assigned outside the Streptophytes in U. vulgaris, and U. gibba, respectively (Additional file 1). The non-plant sequences were mostly derived from microbial commensals, as well as a minor fraction from animal (fish, worm) RNA contamination. The very low proportion of prokaryotic sequences was due to the polyA+ RNA used to prepare cDNA. As prokaryotic mRNAs rarely contain polyA+ tails, they were mostly eliminated. The proportion of non-plant transcripts is probably higher among singletons, because many of them may not have produced statistically significant hits due to incomplete microbial records in public databases. The abundance of microbe-derived transcripts was higher in the U. gibba transcriptome prepared only from plants grown under natural conditions and colonized with microbes. In contrast, the U. vulgaris transcriptome was constructed from a pooled RNA sample prepared from the plants cultivated under both sterile and non-sterile conditions.Figure 2

Bottom Line: We also found a strong correspondence in the presence or absence of root-associated genes between the U. vulgaris transcriptome and U. gibba genome, which indicated that the loss of some root-specific genes had occurred before the divergence of the two rootless species.The species-rich genus Utricularia offers a unique opportunity to study adaptations related to the environment and carnivorous habit and also evolutionary processes responsible for considerable genome reduction.Our study is the first comparison of two global sequence data sets in Utricularia.

View Article: PubMed Central - PubMed

ABSTRACT

Background: The species of Utricularia attract attention not only owing to their carnivorous lifestyle, but also due to an elevated substitution rate and a dynamic evolution of genome size leading to its dramatic reduction. To better understand the evolutionary dynamics of genome size and content as well as the great physiological plasticity in this mostly aquatic carnivorous genus, we analyzed the transcriptome of Utricularia vulgaris, a temperate species with well characterized physiology and ecology. We compared its transcriptome, namely gene content and overall transcript profile, with a previously described transcriptome of Utricularia gibba, a congener possessing one of the smallest angiosperm genomes.

Results: We sequenced a normalized cDNA library prepared from total RNA extracted from shoots of U. vulgaris including leaves and traps, cultivated under sterile or outdoor conditions. 454 pyrosequencing resulted in more than 1,400,000 reads which were assembled into 41,407 isotigs in 19,522 isogroups. We observed high transcript variation in several isogroups explained by multiple loci and/or alternative splicing. The comparison of U. vulgaris and U. gibba transcriptomes revealed a similar distribution of GO categories among expressed genes, despite the differences in transcriptome preparation. We also found a strong correspondence in the presence or absence of root-associated genes between the U. vulgaris transcriptome and U. gibba genome, which indicated that the loss of some root-specific genes had occurred before the divergence of the two rootless species.

Conclusions: The species-rich genus Utricularia offers a unique opportunity to study adaptations related to the environment and carnivorous habit and also evolutionary processes responsible for considerable genome reduction. We show that a transcriptome may approximate the genome for gene content or gene duplication estimation. Our study is the first comparison of two global sequence data sets in Utricularia.

Show MeSH
Related in: MedlinePlus