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Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome.

Ibarra-Laclette E, Albert VA, Pérez-Torres CA, Zamudio-Hernández F, Ortega-Estrada Mde J, Herrera-Estrella A, Herrera-Estrella L - BMC Plant Biol. (2011)

Bottom Line: Long contigs of plastid and mitochondrial genomes, as well as sequences for 100 individual nuclear genes, were compared with those of other plants to better establish information on molecular evolutionary rates.Expression of DNA repair and ROS detoxification enzymes may be indicative of a response to increased respiration.Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of organellar genomes and multiple nuclear genes supports the hypothesis that increased nucleotide substitution rates throughout the plant may be due to the mutagenic action of amplified ROS production.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Guanajuato, México.

ABSTRACT

Background: The carnivorous plant Utricularia gibba (bladderwort) is remarkable in having a minute genome, which at ca. 80 megabases is approximately half that of Arabidopsis. Bladderworts show an incredible diversity of forms surrounding a defined theme: tiny, bladder-like suction traps on terrestrial, epiphytic, or aquatic plants with a diversity of unusual vegetative forms. Utricularia plants, which are rootless, are also anomalous in physiological features (respiration and carbon distribution), and highly enhanced molecular evolutionary rates in chloroplast, mitochondrial and nuclear ribosomal sequences. Despite great interest in the genus, no genomic resources exist for Utricularia, and the substitution rate increase has received limited study.

Results: Here we describe the sequencing and analysis of the Utricularia gibba transcriptome. Three different organs were surveyed, the traps, the vegetative shoot bodies, and the inflorescence stems. We also examined the bladderwort transcriptome under diverse stress conditions. We detail aspects of functional classification, tissue similarity, nitrogen and phosphorus metabolism, respiration, DNA repair, and detoxification of reactive oxygen species (ROS). Long contigs of plastid and mitochondrial genomes, as well as sequences for 100 individual nuclear genes, were compared with those of other plants to better establish information on molecular evolutionary rates.

Conclusion: The Utricularia transcriptome provides a detailed genomic window into processes occurring in a carnivorous plant. It contains a deep representation of the complex metabolic pathways that characterize a putative minimal plant genome, permitting its use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the genus. Vegetative shoots and traps are the most similar organs by functional classification of their transcriptome, the traps expressing hydrolytic enzymes for prey digestion that were previously thought to be encoded by bacteria. Supporting physiological data, global gene expression analysis shows that traps significantly over-express genes involved in respiration and that phosphate uptake might occur mainly in traps, whereas nitrogen uptake could in part take place in vegetative parts. Expression of DNA repair and ROS detoxification enzymes may be indicative of a response to increased respiration. Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of organellar genomes and multiple nuclear genes supports the hypothesis that increased nucleotide substitution rates throughout the plant may be due to the mutagenic action of amplified ROS production.

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Functional annotation. Proportion of KEGG categories (Kyoto Encyclopedia of Genes and Genomes) found in the U. gibba unique transcripts (UT) compared with plants genome annotations [(Arabidopsis thaliana, Populus trichocarpa, Ricinus communis, Vitis vinifera (dicotyledon plants), Oryza sativa, Sorghum bicolor (monocotyledon plants), Physomitrella patens (moss), Chlamydomonas reinhardtii, and Ostreococcus Lucimarinuas (green algae's)].
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Figure 1: Functional annotation. Proportion of KEGG categories (Kyoto Encyclopedia of Genes and Genomes) found in the U. gibba unique transcripts (UT) compared with plants genome annotations [(Arabidopsis thaliana, Populus trichocarpa, Ricinus communis, Vitis vinifera (dicotyledon plants), Oryza sativa, Sorghum bicolor (monocotyledon plants), Physomitrella patens (moss), Chlamydomonas reinhardtii, and Ostreococcus Lucimarinuas (green algae's)].

Mentions: The Kyoto Encyclopedia of Genes and Genomes (KEGG) classifications [28] from best-hit plant proteins were associated to U. gibba UT in order to identify proteins with a known function. Proportions of best hits in each KEGG category are shown in Figure 1. Additionally, using the KEGG Atlas resource [29] we created a global metabolism map combining 119 existing pathways, corresponding to 16,595 genes referenced to in the KEGG database for Arabidopsis, Populus, Vitis, Ricinus, Oryza, Sorghum, Physcomitrella, Chlamydomonas and Ostreococcus. This global metabolism map was compared to the global map created for the U. gibba UT, for which 117 distinct metabolic pathways could be assigned (Additional file 2, Figure S1) out of 119 plant metabolic pathways annotated in the KEGG Atlas. These results indicate that the U. gibba UT comprise a deep representation of the complex metabolic pathways that characterize a plant genome, permitting their use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the Lentibulariaceae.


Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome.

Ibarra-Laclette E, Albert VA, Pérez-Torres CA, Zamudio-Hernández F, Ortega-Estrada Mde J, Herrera-Estrella A, Herrera-Estrella L - BMC Plant Biol. (2011)

Functional annotation. Proportion of KEGG categories (Kyoto Encyclopedia of Genes and Genomes) found in the U. gibba unique transcripts (UT) compared with plants genome annotations [(Arabidopsis thaliana, Populus trichocarpa, Ricinus communis, Vitis vinifera (dicotyledon plants), Oryza sativa, Sorghum bicolor (monocotyledon plants), Physomitrella patens (moss), Chlamydomonas reinhardtii, and Ostreococcus Lucimarinuas (green algae's)].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3141634&req=5

Figure 1: Functional annotation. Proportion of KEGG categories (Kyoto Encyclopedia of Genes and Genomes) found in the U. gibba unique transcripts (UT) compared with plants genome annotations [(Arabidopsis thaliana, Populus trichocarpa, Ricinus communis, Vitis vinifera (dicotyledon plants), Oryza sativa, Sorghum bicolor (monocotyledon plants), Physomitrella patens (moss), Chlamydomonas reinhardtii, and Ostreococcus Lucimarinuas (green algae's)].
Mentions: The Kyoto Encyclopedia of Genes and Genomes (KEGG) classifications [28] from best-hit plant proteins were associated to U. gibba UT in order to identify proteins with a known function. Proportions of best hits in each KEGG category are shown in Figure 1. Additionally, using the KEGG Atlas resource [29] we created a global metabolism map combining 119 existing pathways, corresponding to 16,595 genes referenced to in the KEGG database for Arabidopsis, Populus, Vitis, Ricinus, Oryza, Sorghum, Physcomitrella, Chlamydomonas and Ostreococcus. This global metabolism map was compared to the global map created for the U. gibba UT, for which 117 distinct metabolic pathways could be assigned (Additional file 2, Figure S1) out of 119 plant metabolic pathways annotated in the KEGG Atlas. These results indicate that the U. gibba UT comprise a deep representation of the complex metabolic pathways that characterize a plant genome, permitting their use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the Lentibulariaceae.

Bottom Line: Long contigs of plastid and mitochondrial genomes, as well as sequences for 100 individual nuclear genes, were compared with those of other plants to better establish information on molecular evolutionary rates.Expression of DNA repair and ROS detoxification enzymes may be indicative of a response to increased respiration.Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of organellar genomes and multiple nuclear genes supports the hypothesis that increased nucleotide substitution rates throughout the plant may be due to the mutagenic action of amplified ROS production.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Guanajuato, México.

ABSTRACT

Background: The carnivorous plant Utricularia gibba (bladderwort) is remarkable in having a minute genome, which at ca. 80 megabases is approximately half that of Arabidopsis. Bladderworts show an incredible diversity of forms surrounding a defined theme: tiny, bladder-like suction traps on terrestrial, epiphytic, or aquatic plants with a diversity of unusual vegetative forms. Utricularia plants, which are rootless, are also anomalous in physiological features (respiration and carbon distribution), and highly enhanced molecular evolutionary rates in chloroplast, mitochondrial and nuclear ribosomal sequences. Despite great interest in the genus, no genomic resources exist for Utricularia, and the substitution rate increase has received limited study.

Results: Here we describe the sequencing and analysis of the Utricularia gibba transcriptome. Three different organs were surveyed, the traps, the vegetative shoot bodies, and the inflorescence stems. We also examined the bladderwort transcriptome under diverse stress conditions. We detail aspects of functional classification, tissue similarity, nitrogen and phosphorus metabolism, respiration, DNA repair, and detoxification of reactive oxygen species (ROS). Long contigs of plastid and mitochondrial genomes, as well as sequences for 100 individual nuclear genes, were compared with those of other plants to better establish information on molecular evolutionary rates.

Conclusion: The Utricularia transcriptome provides a detailed genomic window into processes occurring in a carnivorous plant. It contains a deep representation of the complex metabolic pathways that characterize a putative minimal plant genome, permitting its use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the genus. Vegetative shoots and traps are the most similar organs by functional classification of their transcriptome, the traps expressing hydrolytic enzymes for prey digestion that were previously thought to be encoded by bacteria. Supporting physiological data, global gene expression analysis shows that traps significantly over-express genes involved in respiration and that phosphate uptake might occur mainly in traps, whereas nitrogen uptake could in part take place in vegetative parts. Expression of DNA repair and ROS detoxification enzymes may be indicative of a response to increased respiration. Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of organellar genomes and multiple nuclear genes supports the hypothesis that increased nucleotide substitution rates throughout the plant may be due to the mutagenic action of amplified ROS production.

Show MeSH
Related in: MedlinePlus