Dataset Information

The Molecular Evolution and Functional Divergence of Lamprey Programmed Cell Death Genes.

ABSTRACT: The programmed cell death (PDCD) family plays a significant role in the regulation of cell survival and apoptotic cell death. However, the evolution, distribution and role of the PDCD family in lampreys have not been revealed. Thus, we identified the PDCD gene family in the lamprey genome and classified the genes into five subfamilies based on orthologs of the genes, conserved synteny, functional domains, phylogenetic tree, and conserved motifs. The distribution of the lamprey PDCD family and the immune response of the PDCD family in lampreys stimulated by different pathogens were also demonstrated. In addition, we investigated the molecular function of lamprey PDCD2, PDCD5, and PDCD10. Our studies showed that the recombinant lamprey PDCD5 protein and transfection of the L-PDCD5 gene induced cell apoptosis, upregulated the expression of the associated X protein (BAX) and TP53 and downregulated the expression of B cell lymphoma 2 (BCL-2) independent of Caspase 3. In contrast, lamprey PDCD10 suppressed apoptosis in response to cis-diaminedichloro-platinum (II) stimuli. Our phylogenetic and functional data not only provide a better understanding of the evolution of lamprey PDCD genes but also reveal the conservation of PDCD genes in apoptosis. Overall, our results provide a novel perspective on lamprey immune regulation mediated by the PDCD family.

SUBMITTER: Guan X

PROVIDER: S-EPMC6596451 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

The Molecular Evolution and Functional Divergence of Lamprey Programmed Cell Death Genes.

Guan Xin X Lu Jiali J Sun Feng F Li Qingwei Q Pang Yue Y

Frontiers in immunology 20190620

The programmed cell death (PDCD) family plays a significant role in the regulation of cell survival and apoptotic cell death. However, the evolution, distribution and role of the PDCD family in lampreys have not been revealed. Thus, we identified the PDCD gene family in the lamprey genome and classified the genes into five subfamilies based on orthologs of the genes, conserved synteny, functional domains, phylogenetic tree, and conserved motifs. The distribution of the lamprey PDCD family and th ...[more]

PMID: 31281315

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Project description:BACKGROUND: Starch is the main source of carbon storage in the Archaeplastida. The starch biosynthesis pathway (sbp) emerged from cytosolic glycogen metabolism shortly after plastid endosymbiosis and was redirected to the plastid stroma during the green lineage divergence. The SBP is a complex network of genes, most of which are members of large multigene families. While some gene duplications occurred in the Archaeplastida ancestor, most were generated during the sbp redirection process, and the remaining few paralogs were generated through compartmentalization or tissue specialization during the evolution of the land plants. In the present study, we tested models of duplicated gene evolution in order to understand the evolutionary forces that have led to the development of SBP in angiosperms. We combined phylogenetic analyses and tests on the rates of evolution along branches emerging from major duplication events in six gene families encoding sbp enzymes. RESULTS: We found evidence of positive selection along branches following cytosolic or plastidial specialization in two starch phosphorylases and identified numerous residues that exhibited changes in volume, polarity or charge. Starch synthases, branching and debranching enzymes functional specializations were also accompanied by accelerated evolution. However, none of the sites targeted by selection corresponded to known functional domains, catalytic or regulatory. Interestingly, among the 13 duplications tested, 7 exhibited evidence of positive selection in both branches emerging from the duplication, 2 in only one branch, and 4 in none of the branches. CONCLUSIONS: The majority of duplications were followed by accelerated evolution targeting specific residues along both branches. This pattern was consistent with the optimization of the two sub-functions originally fulfilled by the ancestral gene before duplication. Our results thereby provide strong support to the so-called "Escape from Adaptive Conflict" (EAC) model. Because none of the residues targeted by selection occurred in characterized functional domains, we propose that enzyme specialization has occurred through subtle changes in affinity, activity or interaction with other enzymes in complex formation, while the basic function defined by the catalytic domain has been maintained.

Project description:IgLON family is a subgroup of cell adhesion molecules which is known to have diverse roles in neuronal development. IgLONs are characterized by possessing 3 Ig-like C2 domains, which play a part in mediating various cellular interactions. Recently, IgLONs have been shown to be expressed at the blood-brain barrier (BBB). However, our understanding of the genetic divergence patterns and evolutionary rates of these proteins in relation to their functions, in general, and at the BBB, in particular, remains inadequate. In this study, 12 species were explored to shed more light on the phylogenetic origins, structure, functional specificity, and divergence of this family. A total of 40 IgLON genes were identified from vertebrates and invertebrates. The absence of IgLON family genes in Hydra vulgaris and Nematostella vectensis but not in Drosophila melanogaster suggests that this family appeared during the time of divergence of Arthropoda 455 Mya. In general, IgLON genes have been subject to strong positive selection in vertebrates. Our study, based on IgLONs' structural similarity, suggests that they may play a role in the evolutionary changes in the brain anatomy towards complexity including regulating neural growth and BBB permeability. IgLONs' functions seem to be performed through complex interactions on the level of motifs as well as single residues. We identified several IgLON motifs that could be influencing cellular migration and proliferation as well as BBB integrity through interactions with SH3 or integrin. Our motif analysis also revealed that NEGR1 might be involved in MAPK pathway as a form of a signal transmitting receptor through its motif (KKVRVVVNF). We found several residues that were both positively selected and with highly functional specificity. We also located functional divergent residues that could act as drug targets to regulate BBB permeability. Furthermore, we identified several putative metalloproteinase cleavage sites that support the ectodomain shedding hypothesis of the IgLONs. In conclusion, our results present a bridge between IgLONs' molecular evolution and their functions.

Dataset Information

The Molecular Evolution and Functional Divergence of Lamprey Programmed Cell Death Genes.

Publications

The Molecular Evolution and Functional Divergence of Lamprey Programmed Cell Death Genes.

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