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Evaluating the adaptive evolutionary convergence of carnivorous plant taxa through functional genomics.

ABSTRACT: Carnivorous plants are striking examples of evolutionary convergence, displaying complex and often highly similar adaptations despite lack of shared ancestry. Using available carnivorous plant genomes along with non-carnivorous reference taxa, this study examines the convergence of functional overrepresentation of genes previously implicated in plant carnivory. Gene Ontology (GO) coding was used to quantitatively score functional representation in these taxa, in terms of proportion of carnivory-associated functions relative to all functional sequence. Statistical analysis revealed that, in carnivorous plants as a group, only two of the 24 functions tested showed a signal of substantial overrepresentation. However, when the four carnivorous taxa were analyzed individually, 11 functions were found to be significant in at least one taxon. Though carnivorous plants collectively may show overrepresentation in functions from the predicted set, the specific functions that are overrepresented vary substantially from taxon to taxon. While it is possible that some functions serve a similar practical purpose such that one taxon does not need to utilize both to achieve the same result, it appears that there are multiple approaches for the evolution of carnivorous function in plant genomes. Our approach could be applied to tests of functional convergence in other systems provided on the availability of genomes and annotation data for a group.

SUBMITTER: Wheeler GL

PROVIDER: S-EPMC5797450 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Evaluating the adaptive evolutionary convergence of carnivorous plant taxa through functional genomics.

Wheeler Gregory L GL Carstens Bryan C BC

PeerJ 20180131

Carnivorous plants are striking examples of evolutionary convergence, displaying complex and often highly similar adaptations despite lack of shared ancestry. Using available carnivorous plant genomes along with non-carnivorous reference taxa, this study examines the convergence of functional overrepresentation of genes previously implicated in plant carnivory. Gene Ontology (GO) coding was used to quantitatively score functional representation in these taxa, in terms of proportion of carnivory- ...[more]

PMID: 29404217

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Project description:BackgroundThe 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.ResultsHere 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.ConclusionThe 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.

Project description:The carnivorous plants of the family Lentibulariaceae have attained recent attention not only because of their interesting lifestyle, but also because of their dynamic nuclear genome size. Lentibulariaceae genomes span an order of magnitude and include species with the smallest genomes in angiosperms, making them a powerful system to study the mechanisms of genome expansion and contraction. However, little is known about mitochondrial DNA (mtDNA) sequences of this family, and the evolutionary forces that shape this organellar genome. Here we report the sequencing and assembly of the complete mtDNA from the endemic terrestrial Brazilian species Utricularia reniformis. The 857,234bp master circle mitochondrial genome encodes 70 transcriptionaly active genes (42 protein-coding, 25 tRNAs and 3 rRNAs), covering up to 7% of the mtDNA. A ltrA-like protein related to splicing and mobility and a LAGLIDADG homing endonuclease have been identified in intronic regions, suggesting particular mechanisms of genome maintenance. RNA-seq analysis identified properties with putative diverse and important roles in genome regulation and evolution: 1) 672kbp (78%) of the mtDNA is covered by full-length reads; 2) most of the 243kbp intergenic regions exhibit transcripts; and 3) at least 69 novel RNA editing sites in the protein-coding genes. Additional genomic features are hypothetical ORFs (48%), chloroplast insertions, including truncated plastid genes that have been lost from the chloroplast DNA (5%), repeats (5%), relics of transposable elements mostly related to LTR retrotransposons (5%), and truncated mitovirus sequences (0.4%). Phylogenetic analysis based on 32 different Lamiales mitochondrial genomes corroborate that Lentibulariaceae is a monophyletic group. In summary, the U. reniformis mtDNA represents the eighth largest plant mtDNA described to date, shedding light on the genomic trends and evolutionary characteristics and phylogenetic history of the family Lentibulariaceae.

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Evaluating the adaptive evolutionary convergence of carnivorous plant taxa through functional genomics.

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Evaluating the adaptive evolutionary convergence of carnivorous plant taxa through functional genomics.

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