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Beyond Trees: Regulons and Regulatory Motif Characterization.

ABSTRACT: Trees and their seeds regulate their germination, growth, and reproduction in response to environmental stimuli. These stimuli, through signal transduction, trigger transcription factors that alter the expression of various genes leading to the unfolding of the genetic program. A regulon is conceptually defined as a set of target genes regulated by a transcription factor by physically binding to regulatory motifs to accomplish a specific biological function, such as the CO-FT regulon for flowering timing and fall growth cessation in trees. Only with a clear characterization of regulatory motifs, can candidate target genes be experimentally validated, but motif characterization represents the weakest feature of regulon research, especially in tree genetics. I review here relevant experimental and bioinformatics approaches in characterizing transcription factors and their binding sites, outline problems in tree regulon research, and demonstrate how transcription factor databases can be effectively used to aid the characterization of tree regulons.

SUBMITTER: Xia X

PROVIDER: S-EPMC7564462 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Beyond Trees: Regulons and Regulatory Motif Characterization.

Xia Xuhua X

Genes 20200825 9

Trees and their seeds regulate their germination, growth, and reproduction in response to environmental stimuli. These stimuli, through signal transduction, trigger transcription factors that alter the expression of various genes leading to the unfolding of the genetic program. A regulon is conceptually defined as a set of target genes regulated by a transcription factor by physically binding to regulatory motifs to accomplish a specific biological function, such as the CO-FT regulon for floweri ...[more]

PMID: 32854400

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Project description:BackgroundSequencing projects have allowed diverse retroviruses and LTR retrotransposons from different eukaryotic organisms to be characterized. It is known that retroviruses and other retro-transcribing viruses evolve from LTR retrotransposons and that this whole system clusters into five families: Ty3/Gypsy, Retroviridae, Ty1/Copia, Bel/Pao and Caulimoviridae. Phylogenetic analyses usually show that these split into multiple distinct lineages but what is yet to be understood is how deep evolution occurred in this system.ResultsWe combined phylogenetic and graph analyses to investigate the history of LTR retroelements both as a tree and as a network. We used 268 non-redundant LTR retroelements, many of them introduced for the first time in this work, to elucidate all possible LTR retroelement phylogenetic patterns. These were superimposed over the tree of eukaryotes to investigate the dynamics of the system, at distinct evolutionary times. Next, we investigated phenotypic features such as duplication and variability of amino acid motifs, and several differences in genomic ORF organization. Using this information we characterized eight reticulate evolution markers to construct phenotypic network models.ConclusionThe evolutionary history of LTR retroelements can be traced as a time-evolving network that depends on phylogenetic patterns, epigenetic host-factors and phenotypic plasticity. The Ty1/Copia and the Ty3/Gypsy families represent the oldest patterns in this network that we found mimics eukaryotic macroevolution. The emergence of the Bel/Pao, Retroviridae and Caulimoviridae families in this network can be related with distinct inflations of the Ty3/Gypsy family, at distinct evolutionary times. This suggests that Ty3/Gypsy ancestors diversified much more than their Ty1/Copia counterparts, at distinct geological eras. Consistent with the principle of preferential attachment, the connectivities among phenotypic markers, taken as network-represented combinations, are power-law distributed. This evidences an inflationary mode of evolution where the system diversity; 1) expands continuously alternating vertical and gradual processes of phylogenetic divergence with episodes of modular, saltatory and reticulate evolution; 2) is governed by the intrinsic capability of distinct LTR retroelement host-communities to self-organize their phenotypes according to emergent laws characteristic of complex systems.ReviewersThis article was reviewed by Eugene V. Koonin, Eric Bapteste, and Enmanuelle Lerat (nominated by King Jordan).

Project description:In silico comparative genomics approaches have been efficiently used for functional prediction and reconstruction of metabolic and regulatory networks. Riboswitches are metabolite-sensing structures often found in bacterial mRNA leaders controlling gene expression on transcriptional or translational levels.An increasing number of riboswitches and other cis-regulatory RNAs have been recently classified into numerous RNA families in the Rfam database. High conservation of these RNA motifs provides a unique advantage for their genomic identification and comparative analysis.A comparative genomics approach implemented in the RegPredict tool was used for reconstruction and functional annotation of regulons controlled by RNAs from 43 Rfam families in diverse taxonomic groups of Bacteria. The inferred regulons include ~5200 cis-regulatory RNAs and more than 12000 target genes in 255 microbial genomes. All predicted RNA-regulated genes were classified into specific and overall functional categories. Analysis of taxonomic distribution of these categories allowed us to establish major functional preferences for each analyzed cis-regulatory RNA motif family. Overall, most RNA motif regulons showed predictable functional content in accordance with their experimentally established effector ligands. Our results suggest that some RNA motifs (including thiamin pyrophosphate and cobalamin riboswitches that control the cofactor metabolism) are widespread and likely originated from the last common ancestor of all bacteria. However, many more analyzed RNA motifs are restricted to a narrow taxonomic group of bacteria and likely represent more recent evolutionary innovations.The reconstructed regulatory networks for major known RNA motifs substantially expand the existing knowledge of transcriptional regulation in bacteria. The inferred regulons can be used for genetic experiments, functional annotations of genes, metabolic reconstruction and evolutionary analysis. The obtained genome-wide collection of reference RNA motif regulons is available in the RegPrecise database (http://regprecise.lbl.gov/).

Project description:Two methods were developed for the generation of cisgenic apples. Both have been successfully applied producing trees. The first method avoids the use of any foreign selectable marker genes; only the gene-of-interest is integrated between the T-DNA border sequences. The second method makes use of recombinase-based marker excision. For the first method we used the MdMYB10 gene from a red-fleshed apple coding for a transcription factor involved in regulating anthocyanin biosynthesis. Red plantlets were obtained and presence of the cisgene was confirmed. Plantlets were grafted and grown in a greenhouse. After 3 years, the first flowers appeared, showing red petals. Pollination led to production of red-fleshed cisgenic apples. The second method used the pM(arker)F(ree) vector system, introducing the scab resistance gene Rvi6, derived from apple. Agrobacterium-mediated transformation, followed by selection on kanamycin, produced genetically modified apple lines. Next, leaves from in vitro material were treated to activate the recombinase leading to excision of selection genes. Subsequently, the leaf explants were subjected to negative selection for marker-free plantlets by inducing regeneration on medium containing 5-fluorocytosine. After verification of the marker-free nature, the obtained plants were grafted onto rootstocks. Young trees from four cisgenic lines and one intragenic line, all containing Rvi6, were planted in an orchard. Appropriate controls were incorporated in this trial. We scored scab incidence for three consecutive years on leaves after inoculations with Rvi6-avirulent strains. One cisgenic line and the intragenic line performed as well as the resistant control. In 2014 trees started to overcome their juvenile character and formed flowers and fruits. The first results of scoring scab symptoms on apple fruits were obtained. Apple fruits from susceptible controls showed scab symptoms, while fruits from cisgenic and intragenic lines were free of scab.

Dataset Information

Beyond Trees: Regulons and Regulatory Motif Characterization.

Publications

Beyond Trees: Regulons and Regulatory Motif Characterization.

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