It happened again: Convergent evolution of acylglucose specialized metabolism in black nightshade and wild tomato
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ABSTRACT:
SUBMITTER: Lou Y
PROVIDER: S-EPMC8580325 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Plants produce a myriad of taxonomically restricted specialized metabolites. This diversity-and our ability to correlate genotype with phenotype-makes the evolution of these ecologically and medicinally important compounds interesting and experimentally tractable. Trichomes of tomato and other nightshade family plants produce structurally diverse protective compounds termed acylsugars. While cultivated tomato (Solanum lycopersicum) strictly accumulates acylsucroses, the South American wild relative Solanum pennellii produces copious amounts of acylglucoses. Genetic, transgenic, and biochemical dissection of the S. pennellii acylglucose biosynthetic pathway identified a trichome gland cell-expressed invertase-like enzyme that hydrolyzes acylsucroses (Sopen03g040490). This enzyme acts on the pyranose ring-acylated acylsucroses found in the wild tomato but not on the furanose ring-decorated acylsucroses of cultivated tomato. These results show that modification of the core acylsucrose biosynthetic pathway leading to loss of furanose ring acylation set the stage for co-option of a general metabolic enzyme to produce a new class of protective compounds.
| S-EPMC6482016 | biostudies-literature
Project description:BackgroundThe Thecostraca are arguably the most morphologically and biologically variable group within the Crustacea, including both suspension feeders (Cirripedia: Thoracica and Acrothoracica) and parasitic forms (Cirripedia: Rhizocephala, Ascothoracida and Facetotecta). Similarities between the metamorphosis found in the Facetotecta and Rhizocephala suggests a common evolutionary origin, but until now no comprehensive study has looked at the basic evolution of these thecostracan groups.ResultsTo this end, we collected DNA sequences from three nuclear genes [18S rRNA (2,305), 28S rRNA (2,402), Histone H3 (328)] and 41 larval characters in seven facetotectans, five ascothoracidans, three acrothoracicans, 25 rhizocephalans and 39 thoracicans (ingroup) and 12 Malacostraca and 10 Copepoda (outgroup). Maximum parsimony, maximum likelihood and Bayesian analyses showed the Facetotecta, Ascothoracida and Cirripedia each as monophyletic. The better resolved and highly supported DNA maximum likelihood and morphological-DNA Bayesian analysis trees depicted the main phylogenetic relationships within the Thecostraca as (Facetotecta, (Ascothoracida, (Acrothoracica, (Rhizocephala, Thoracica)))).ConclusionOur analyses indicate a convergent evolution of the very similar and highly reduced slug-shaped stages found during metamorphosis of both the Rhizocephala and the Facetotecta. This provides a remarkable case of convergent evolution and implies that the advanced endoparasitic mode of life known from the Rhizocephala and strongly indicated for the Facetotecta had no common origin. Future analyses are needed to determine whether the most recent common ancestor of the Thecostraca was free-living or some primitive form of ectoparasite.
| S-EPMC2678073 | biostudies-literature
Project description:BackgroundGenome size and gene content in bacteria are associated with their lifestyles. Obligate intracellular bacteria (i.e., mutualists and parasites) have small genomes that derived from larger free-living bacterial ancestors; however, the different steps of bacterial specialization from free-living to intracellular lifestyle have not been studied comprehensively. The growing number of available sequenced genomes makes it possible to perform a statistical comparative analysis of 317 genomes from bacteria with different lifestyles.ResultsCompared to free-living bacteria, host-dependent bacteria exhibit fewer rRNA genes, more split rRNA operons and fewer transcriptional regulators, linked to slower growth rates. We found a function-dependent and non-random loss of the same 100 orthologous genes in all obligate intracellular bacteria. Thus, we showed that obligate intracellular bacteria from different phyla are converging according to their lifestyle. Their specialization is an irreversible phenomenon characterized by translation modification and massive gene loss, including the loss of transcriptional regulators. Although both mutualists and parasites converge by genome reduction, these obligate intracellular bacteria have lost distinct sets of genes in the context of their specific host associations: mutualists have significantly more genes that enable nutrient provisioning whereas parasites have genes that encode Types II, IV, and VI secretion pathways.ConclusionOur findings suggest that gene loss, rather than acquisition of virulence factors, has been a driving force in the adaptation of parasites to eukaryotic cells. This comparative genomic analysis helps to explore the strategies by which obligate intracellular genomes specialize to particular host-associations and contributes to advance our knowledge about the mechanisms of bacterial evolution.
| S-EPMC2688493 | biostudies-literature
Project description:The evolution of new traits in living organisms occurs via the processes of mutation, recombination, genetic drift, and selection. These processes that have resulted in the immense biological diversity on our planet are also being employed in metabolic engineering to optimize enzymes and pathways, create new-to-nature reactions, and synthesize complex natural products in heterologous systems. In this review, we discuss two evolution-aided strategies for metabolic engineering-directed evolution, which improves upon existing genetic templates using the evolutionary process, and combinatorial pathway reconstruction, which brings together genes evolved in different organisms into a single heterologous host. We discuss the general principles of these strategies, describe the technologies involved and the molecular traits they influence, provide examples of their use, and discuss the roadblocks that need to be addressed for their wider adoption. A better understanding of these strategies can provide an impetus to research on gene function discovery and biochemical evolution, which is foundational for improved metabolic engineering. These evolution-aided approaches thus have a substantial potential for improving our understanding of plant metabolism in general, for enhancing the production of plant metabolites, and in sustainable agriculture.
| S-EPMC9590541 | biostudies-literature
Project description:Specialized metabolic enzymes and metabolite diversity evolve through a variety of mechanisms including promiscuity, changes in substrate specificity, modifications of gene expression and gene duplication. For example, gene duplication and substrate binding site changes led to the evolution of the glucosinolate biosynthetic enzyme, AtIPMDH1, from a Leu biosynthetic enzyme. BAHD acyltransferases illustrate how enzymatic promiscuity leads to metabolite diversity. The examples 4-coumarate:CoA ligase and aromatic acid methyltransferases illustrate how promiscuity can potentiate the evolution of these specialized metabolic enzymes.
| S-EPMC5723210 | biostudies-literature
Project description:Closely related species are often assumed to be functionally similar. Phylogenetic information is thus widely used to infer functional diversity and assembly of communities. In contrast, evolutionary processes generating functional similarity of phylogenetically distinct taxa are rarely addressed in this context.To investigate the impact of convergent evolution on functional diversity (FD) and phylogenetic diversity (PD), we reconstructed the phylogenetic structure of carabid trophic groups. We then analyzed the mandible shapes using geometric morphometrics to link specialization in functional morphology with feeding specialization among herbivores, generalist carnivores, and specialized consumers of Collembola.Our results show that carabid feeding groups are paraphyletic. Herbivory evolved at least twice and specialization to Collembola predation at least three times. Species within feeding groups share a remarkably similar mandible morphology, which evolved convergently. While specialized mandibles of herbivores and collembolan specialists represent an adaptation to their main food source, the particular mandible morphologies do not necessarily reflect the degree of food specialization within feeding groups. Only a few species with a specialized herbivorous mandible may occasionally feed on animals, but the range of specific food resources in generalist carnivore species is large, despite an almost identical mandible shape.Thus, convergent evolution in specialized feeding groups reverses the relationship between PD and functional similarity compared with generalist carnivores. We conclude that phylogenetic relationship is a poor proxy of FD in carabids. Moreover, the inconsistencies between relatedness, morphological adaptation, and ecological function require caution in the characterization of functional groups. Rather than assuming general relationships between PD and FD, we suggest integrating the analysis of evolutionary processes into functional community analyses.
| S-EPMC7593144 | biostudies-literature
Project description:Black nightshade (Solanum nigrum) belongs to the Solanaceae family and is used as a medicinal herb with health benefits. It has been reported that the black nightshade plant contains various phytochemicals that are associated with antitumor activities. Here we employed a genetic approach to study the effects of overexpression of Arabidopsis thaliana production of anthocyanin pigment 1 (AtPAP1) in black nightshade. Ectopic expression of AtPAP1 resulted in enhanced accumulation of anthocyanin pigments in vegetative and reproductive tissues of the transgenic plants. Analysis of anthocyanin revealed that delphinidin 3-O-rutinoside-5-O-glucoside, delphinidin 3,5-O-diglucoside, delphinidin 3-O-rutinoside, petunidin 3-O-rutinoside (cis-p-coumaroyl)-5-O-glucoside, petunidin 3-(feruloyl)-rutinoside-5-glucoside, and malvidin 3-(feruloyl)-rutinoside-5-glucoside are highly induced in the leaves of AtPAP1 overexpression lines. Furthermore, ectopic expression of AtPAP1 evoked expression of early and late biosynthetic genes of the general phenylpropanoid and flavonoid pathways that include phenylalanine ammonia-lyase (PAL), cinnamate-4-hydroxylase (C4H), 4-coumarate CoA ligase (4CL), chalcone isomerase (CHI), and quinate hydroxycinnamoyl transferase (HCT), which suggests these genes might be transcriptional targets of AtPAP1 in black nightshade. Concomitantly, the total content of anthocyanin in the transgenic black nightshade plants was higher compared to the control plants, which supports phenotypic changes in color. Our data demonstrate that a major anthocyanin biosynthetic regulator, AtPAP1, can induce accumulation of anthocyanins in the heterologous system of black nightshade through the conserved flavonoid biosynthesis pathway in plants.
| S-EPMC7072430 | biostudies-literature
Project description:Specialized metabolites possess diverse interesting biological activities and some cardenolides- and monoterpene indole alkaloids- (MIAs) derived pharmaceuticals are currently used to treat human diseases such as cancers or hypertension. While these two families of biocompounds are produced by specific subfamilies of Apocynaceae, one member of this medicinal plant family, the succulent tree Pachypodium lamerei Drake (also known as Madagascar palm), does not produce such specialized metabolites. To explore the evolutionary paths that have led to the emergence and loss of cardenolide and MIA biosynthesis in Apocynaceae, we sequenced and assembled the P. lamerei genome by combining Oxford Nanopore Technologies long-reads and Illumina short-reads. Phylogenomics revealed that, among the Apocynaceae whose genomes have been sequenced, the Madagascar palm is so far the species closest to the common ancestor between MIA producers/non-MIA producers. Transposable elements, constituting 72.48% of the genome, emerge as potential key players in shaping genomic architecture and influencing specialized metabolic pathways. The absence of crucial MIA biosynthetic genes such as strictosidine synthase in P. lamerei and non-Rauvolfioideae species hints at a transposon-mediated mechanism behind gene loss. Phylogenetic analysis not only showcases the evolutionary divergence of specialized metabolite biosynthesis within Apocynaceae but also underscores the role of transposable elements in this intricate process. Moreover, we shed light on the low conservation of enzymes involved in the final stages of MIA biosynthesis in the distinct MIA-producing plant families, inferring independent gains of these specialized enzymes along the evolution of these medicinal plant clades. Overall, this study marks a leap forward in understanding the genomic dynamics underpinning the evolution of specialized metabolites biosynthesis in the Apocynaceae family, with transposons emerging as potential architects of genomics restructuring and gene loss.
| S-EPMC10963385 | biostudies-literature
Project description:Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260?Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.
| S-EPMC5711932 | biostudies-literature
Project description:The wild tomato species Solanum chilense and S. peruvianum are a valuable non-model system for studying plant adaptation since they grow in diverse environments facing many abiotic constraints. Here we investigate the sequence evolution of regulatory regions of drought and cold responsive genes and their expression regulation. The coding regions of these genes were previously shown to exhibit signatures of positive selection. Expression profiles and sequence evolution of regulatory regions of members of the Asr (ABA/water stress/ripening induced) gene family and the dehydrin gene pLC30-15 were analyzed in wild tomato populations from contrasting environments. For S. chilense, we found that Asr4 and pLC30-15 appear to respond much faster to drought conditions in accessions from very dry environments than accessions from more mesic locations. Sequence analysis suggests that the promoter of Asr2 and the downstream region of pLC30-15 are under positive selection in some local populations of S. chilense. By investigating gene expression differences at the population level we provide further support of our previous conclusions that Asr2, Asr4, and pLC30-15 are promising candidates for functional studies of adaptation. Our analysis also demonstrates the power of the candidate gene approach in evolutionary biology research and highlights the importance of wild Solanum species as a genetic resource for their cultivated relatives.
| S-EPMC3799731 | biostudies-literature