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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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GO enrichment. The enrichment of particular GO categories (in % of total GO categories) in the subsets of orthologous pairs between U. vulgaris and U. gibba with ascending sequence similarity. GO:0048193 Golgi vesicle transport; GO:0009853 Photorespiration GO: 0007264 Small GTPase mediated signal transduction; GO: 00022626 Cytosolic ribosomes; GO:0005856 Cytoskeleton; GO: 0005746 Mitochondrial respiratory chain.
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Fig6: GO enrichment. The enrichment of particular GO categories (in % of total GO categories) in the subsets of orthologous pairs between U. vulgaris and U. gibba with ascending sequence similarity. GO:0048193 Golgi vesicle transport; GO:0009853 Photorespiration GO: 0007264 Small GTPase mediated signal transduction; GO: 00022626 Cytosolic ribosomes; GO:0005856 Cytoskeleton; GO: 0005746 Mitochondrial respiratory chain.

Mentions: Because the overall sequence similarity of putative U. vulgaris-U. gibba orthologs was rather low (median 87%), we investigated which GO categories were enriched among the most conserved orthologous pairs. GO enrichment (AgriGo) [29] analysis of the most conserved orthologs (with similarity higher than 93%) against all orthologs identified 36 significantly enriched GO categories (Additional file 5). They belonged to the genes encoding proteins conserved across all angiosperms (ribosomal proteins, tubulins, small GTP-binding proteins, mitochondrial respiratory chain proteins, etc.). Their proportion in respective similarity classes of putative orthologs increased with increasing sequence similarity (Figure 6). Detailed inspection of GO categories enriched among highly conserved orthologs between U. gibba and U. vulgaris revealed genes which were less similar to their Arabidopsis counterparts than the rest of the highly conserved orthologs, namely MYOSIN XI B (homolog of At1g04160) and TIP GROWTH DEFECTIVE 1 (TIP1) (a homolog of At5g20350). Interestingly, both genes play a role in root hair development in Arabidopsis. As neither U. gibba nor U. vulgaris produce roots, it is probable that the two genes have gained a novel or modified functions in Utricularia, explaining why their sequences are highly similar between both Utricularia species, but less similar to Arabidopsis homologs.Figure 6


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)

GO enrichment. The enrichment of particular GO categories (in % of total GO categories) in the subsets of orthologous pairs between U. vulgaris and U. gibba with ascending sequence similarity. GO:0048193 Golgi vesicle transport; GO:0009853 Photorespiration GO: 0007264 Small GTPase mediated signal transduction; GO: 00022626 Cytosolic ribosomes; GO:0005856 Cytoskeleton; GO: 0005746 Mitochondrial respiratory chain.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: GO enrichment. The enrichment of particular GO categories (in % of total GO categories) in the subsets of orthologous pairs between U. vulgaris and U. gibba with ascending sequence similarity. GO:0048193 Golgi vesicle transport; GO:0009853 Photorespiration GO: 0007264 Small GTPase mediated signal transduction; GO: 00022626 Cytosolic ribosomes; GO:0005856 Cytoskeleton; GO: 0005746 Mitochondrial respiratory chain.
Mentions: Because the overall sequence similarity of putative U. vulgaris-U. gibba orthologs was rather low (median 87%), we investigated which GO categories were enriched among the most conserved orthologous pairs. GO enrichment (AgriGo) [29] analysis of the most conserved orthologs (with similarity higher than 93%) against all orthologs identified 36 significantly enriched GO categories (Additional file 5). They belonged to the genes encoding proteins conserved across all angiosperms (ribosomal proteins, tubulins, small GTP-binding proteins, mitochondrial respiratory chain proteins, etc.). Their proportion in respective similarity classes of putative orthologs increased with increasing sequence similarity (Figure 6). Detailed inspection of GO categories enriched among highly conserved orthologs between U. gibba and U. vulgaris revealed genes which were less similar to their Arabidopsis counterparts than the rest of the highly conserved orthologs, namely MYOSIN XI B (homolog of At1g04160) and TIP GROWTH DEFECTIVE 1 (TIP1) (a homolog of At5g20350). Interestingly, both genes play a role in root hair development in Arabidopsis. As neither U. gibba nor U. vulgaris produce roots, it is probable that the two genes have gained a novel or modified functions in Utricularia, explaining why their sequences are highly similar between both Utricularia species, but less similar to Arabidopsis homologs.Figure 6

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