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. 2025 Jan 29;2025:10.17912/micropub.biology.001026. doi: 10.17912/micropub.biology.001026

Gene model for the ortholog of eIF4E1 in Drosophila ananassae

McKenzie Chamberlain 1, Ali Christie 2, Jeremy Girard 3, Hannah M Shaver 2, Lindsey J Long 2, James J Youngblom 3, Chinmay P Rele 1, Laura K Reed 1,§
Reviewed by: Anonymous
PMCID: PMC11822467  PMID: 39950091

Abstract

Gene model for the ortholog of eukaryotic translation initiation factor 4E1 ( eIF4E1 ) in the May 2011 (Agencourt dana_caf1/DanaCAF1) Genome Assembly (GenBank Accession: GCA_000005115.1 ) of Drosophila ananassae . This ortholog was characterized as part of a developing dataset to study the evolution of the Insulin/insulin-like growth factor signaling pathway (IIS) across the genus Drosophila using the Genomics Education Partnership gene annotation protocol for Course-based Undergraduate Research Experiences.

Figure 1. Genomic neighborhood and gene model for eIF4E1 in Drosophila ananassae .

Figure 1. Genomic neighborhood and gene model for eIF4E1 in Drosophila ananassae

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(A) Synteny comparison of the genomic neighborhoods for eIF4E1 in Drosophila melanogaster and D. ananassae . Thin underlying arrows indicate the DNA strand within which the gene– eIF4E1 –is located in D. melanogaster (top) and D. ananassae (bottom) genomes. Thin arrows pointing to the left indicate that eIF4E1 is on the negative (-) strand in D. ananassae and D. melanogaster . The wide gene arrows pointing in the same direction as eIF4E1 are on the same strand relative to the thin underlying arrows, while wide gene arrows pointing in the opposite direction of eIF4E1 are on the opposite strand relative to the thin underlying arrows. White gene arrows in D. ananassae indicate orthology to the corresponding gene in D. melanogaster . Gene symbols given in the D. ananassae gene arrows indicate the orthologous gene in D. melanogaster , while the locus identifiers are specific to D. ananassae . (B) Gene Model in GEP UCSC Track Data Hub (Raney et al., 2014). The coding-regions of eIF4E1 in D. ananassae are displayed in the User Supplied Track (black); coding CDSs are depicted by thick rectangles and introns by thin lines with arrows indicating the direction of transcription. Subsequent evidence tracks include BLAT Alignments of NCBI RefSeq Genes (dark blue, alignment of Ref-Seq genes for D. ananassae ), Spaln of D. melanogaster Proteins (purple, alignment of Ref-Seq proteins from D. melanogaster ), Transcripts and Coding Regions Predicted by TransDecoder (dark green), RNA-Seq from Adult Females, Adult Males and Embryos (red, light blue, and dark pink, respectively; alignment of Illumina RNA-Seq reads from D. ananassae ), and Splice Junctions Predicted by regtools using D. ananassae RNA-Seq (SRP006203; SRP007906). Splice junctions shown have a minimum read-depth of 10 with 100-499 and >1000 supporting reads in light pink and red, respectively. (C) Dot Plot of eIF4E1-RB in D. melanogaster ( x -axis) vs. the orthologous peptide in D. ananassae ( y -axis). Amino acid number is indicated along the left and bottom; coding-CDS number is indicated along the top and right, and CDSs are also highlighted with alternating colors. The purple boxes labeled I, II, and III contain regions where an insertion or deletion of base pairs has occurred. The green boxes labeled IV and V outline regions that have a lack of sequence similarity between eIF4E1-RB in D. melanogaster and eIF4E1-RB in D. ananassae . (D) The protein alignment between D. melanogaster eIF4E1-PB and its putative ortholog in D. ananassae . The alternating colored rectangles represent adjacent CDSs. The symbols in the match line denote the level of similarity between the aligned residues. An asterisk (*) indicates that the aligned residues are identical. A colon (:) indicates the aligned residues have highly similar chemical properties—roughly equivalent to scoring > 0.5 in the Gonnet PAM 250 matrix (Gonnet et al., 1992). A period (.) indicates that the aligned residues have weakly similar chemically properties—roughly equivalent to scoring > 0 and ≤ 0.5 in the Gonnet PAM 250 matrix. A space indicates a gap or mismatch when the aligned residues have a complete lack of similarity—roughly equivalent to scoring ≤ 0 in the Gonnet PAM 250 matrix. The purple boxes labeled I, II and III outline regions where an insertion or deletion of base pairs has occurred. The green boxes labeled IV and V outline regions where there is a lack of sequence similarity between eIF4E1-PB in D. melanogaster and eIF4E1-PB in D. ananassae .

Description

This article reports a predicted gene model generated by undergraduate work using a structured gene model annotation protocol defined by the Genomics Education Partnership (GEP; thegep.org) for Course-based Undergraduate Research Experience (CURE). The following information may be repeated in other articles submitted by participants using the same GEP CURE protocol for annotating Drosophila species orthologs of Drosophila melanogaster genes in the insulin signaling pathway.

"In this GEP CURE protocol students use web-based tools to manually annotate genes in non-model Drosophila species based on orthology to genes in the well-annotated model organism fruitfly Drosophila melanogaster . The GEP uses web-based tools to allow undergraduates to participate in course-based research by generating manual annotations of genes in non-model species (Rele et al., 2023) . Computational-based gene predictions in any organism are often improved by careful manual annotation and curation, allowing for more accurate analyses of gene and genome evolution (Mudge and Harrow 2016; Tello-Ruiz et al., 2019) . These models of orthologous genes across species, such as the one presented here, then provide a reliable basis for further evolutionary genomic analyses when made available to the scientific community.” (Myers et al., 2024) .

“The particular gene ortholog described here was characterized as part of a developing dataset to study the evolution of the Insulin/insulin-like growth factor signaling pathway (IIS) across the genus Drosophila . The Insulin/insulin-like growth factor signaling pathway (IIS) is a highly conserved signaling pathway in animals and is central to mediating organismal responses to nutrients (Hietakangas and Cohen 2009; Grewal 2009) .” (Myers et al., 2024) .

“ eukaryotic translation initiation factor 4E1 ( eIF4E1 ) encodes eIF4F cap-binding complex essential cap-dependent translation of mRNA, and binds the 7-methyl-guanosine cap structure of mRNA in Drosophila (Lachance et al., 2002; Lavoie et al., 1996) . The protein product of eIF4E-3 , a paralog of eIF4E1 , is specifically required during spermatogenesis in Drosophila (Hernendez et al., 2012).” (Lose et al., 2025) .

“ D . ananassae (NCBI:txid7217) is part of the melanogaster species group within the subgenus Sophophora of the genus Drosophila (Sturtevant 1939; Bock and Wheeler 1972) . It was first described by Doleschall (1858). D. ananassae is circumtropical (Markow and O'Grady 2005; https://www.taxodros.uzh.ch, accessed 1 Feb 2023), and often associated with human settlement (Singh 2010) . It has been extensively studied as a model for its cytogenetic and genetic characteristics, and in experimental evolution (Kikkawa 1938; Singh and Yadav 2015) .” (Lawson et al., 2024) .

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We propose a gene model for the D. ananassae ortholog of the D. melanogaster eukaryotic translation initiation factor 4E1 ( eIF4E1 ) gene. The genomic region of the ortholog corresponds to the uncharacterized protein LOC6506375 (RefSeq accession LOC6506375 ) in the Dana_CAF1 Genome Assembly of D. ananassae (GenBank Accession: GCA_000005115.1 ; Drosophila 12 Genomes Consortium et al., 2007). This model is based on RNA-Seq data from D. ananassae ( SRP006203 ; SRP007906 - Graveley et al., 2010) and eIF4E1 in D. melanogaster using FlyBase release FB2022_04 ( GCA_000001215.4 ; Larkin et al., 2021; Gramates et al., 2022; Jenkins et al., 2022).

Synteny

The reference gene, eIF4E1 , occurs on chromosome 3L in D. melanogaster and is flanked upstream by CG4022 and Cuticular protein 67B ( Cpr67B ) and downstream by CG4080 and Heat shock protein 23 ( Hsp23 ). The tblastn search of D. melanogaster eIF4E1-PB (query) against the D. ananassae (GenBank Accession: GCA_000005115.1 ) Genome Assembly (database) placed the putative ortholog of eIF4E1 within scaffold scaffold_13337 ( CH902618.1 ) at locus LOC6506375 ( XP_014764725.1 ) — with an E-value of 8e-131 and a percent identity of 80.80%. Furthermore, the putative ortholog is flanked upstream by LOC6506374 ( XP_001958001.1 ) and LOC6493561 ( XP_001958000.1 ), which correspond to CG4022 and Cpr67B in D. melanogaster (E-value: 6e-118 and 1e-168; identity: 88.17% and 97.31%, respectively, as determined by blastp ) ( Figure 1A, A ltschul et al., 1990). The putative ortholog of eIF4E1 is flanked downstream by LOC6506376 ( XP_001957998.1 ) and LOC6493560 ( XP_001957997.1 ), which correspond to CG4080 and Hsp23 in D. melanogaster (E-value: 0.0 and 2e-103; identity: 87.56% and 83.08%, respectively, as determined by blastp ). The putative ortholog assignment for eIF4E1 in D. ananassae is supported by the following evidence: The genes surrounding the eIF4E1 ortholog are orthologous to the genes at the same locus in D. melanogaster and synteny is completely conserved, supported by results generated from blastp , so we conclude that LOC6506375 is the correct ortholog of eIF4E1 in D. ananassae ( Figure 1A ).

Protein Model

eIF4E1 in D. ananassae contains two unique protein-coding isoforms: eIF4E1-PB (identical to eIF4E1-PA, eIF4E1-PD, eIF4E1-PE, eIF4E1-PF, eIF4E1-PG, eIF4E1-PH, eIF4E1-PI) and eIF4E1-PC ( Figure 1B ). mRNA isoforms ( eIF4E1-RB , eIF4E1-RA , eIF4E1-RD , eIF4E1-RE , eIF4E1-RF , eIF4E1-RG , eIF4E1-RH , eIF4E1-RI ) contain five CDSs but differ in their UTRs. eIF4E1-RC differs from the other isoforms only in the first CDS. The remaining protein-coding isoforms are identical. Relative to the ortholog in D. melanogaster , the RNA CDS number and the protein isoform count are conserved. The sequence of eIF4E1-PB in D. ananassae has 80.80% identity (E-value: 8e-131) with the protein-coding isoform eIF4E1-PB in D. melanogaster , as determined by blastp ( Figure 1C ). Three indels were found within the second CDS of D. ananassae , outlined in boxes purple labeled I, II, and III ( Figure 1C, 1D ). Two regions containing a lack of sequence similarity were found between eIF4E1-PB in D. ananassae and D. melanogaster , outlined in green boxes labeled IV and V ( Figure 1C, 1D ). Coordinates of this curated gene model (eIF4E1-PE, eIF4E1-PF, eIF4E1-PH, eIF4E1-PA, eIF4E1-PG, eIF4E1-PI, eIF4E1-PD, eIF4E1-PB, eIF4E1-PC) are stored by NCBI at GenBank/BankIt (accessions BK064567 , BK064568 , BK064569 , BK064570 , BK064571 , BK064572 , BK064573 , BK064574 , and BK064575 , respectively). These data are also archived in the CaltechDATA repository (see “Extended Data” section below).

Special characteristics of the protein model

Three indels within CDS two, found in isoform eIF4E1-RB , are shown in the dot plot and protein alignment outlined by the purple boxes labeled I, II, and III ( Figure 1C and 1D). The first indel (I) consists of seven amino acids and is an insertion in D. ananassae and relative to D. melanogaster . The second (II) consists of four amino acids while the third (III) consists of two amino acids. Both (II and III) show deletions in D. ananassae relative to D. melanogaster .

Methods

Detailed methods including algorithms, database versions, and citations for the complete annotation process can be found in Rele et al. (2023). Briefly, students use the GEP instance of the UCSC Genome Browser v.435 ( https://gander.wustl.edu ; Kent WJ et al., 2002; Navarro Gonzalez et al., 2021) to examine the genomic neighborhood of their reference IIS gene in the D. melanogaster genome assembly (Aug. 2014; BDGP Release 6 + ISO1 MT/dm6). Students then retrieve the protein sequence for the D. melanogaster reference gene for a given isoform and run it using tblastn against their target Drosophila species genome assembly on the NCBI BLAST server ( https://blast.ncbi.nlm.nih.gov/Blast.cgi ; Altschul et al., 1990) to identify potential orthologs. To validate the potential ortholog, students compare the local genomic neighborhood of their potential ortholog with the genomic neighborhood of their reference gene in D. melanogaster . This local synteny analysis includes at minimum the two upstream and downstream genes relative to their putative ortholog. They also explore other sets of genomic evidence using multiple alignment tracks in the Genome Browser, including BLAT alignments of RefSeq Genes, Spaln alignment of D. melanogaster proteins, multiple gene prediction tracks (e.g., GeMoMa, Geneid, Augustus), and modENCODE RNA-Seq from the target species. Detailed explanation of how these lines of genomic evidenced are leveraged by students in gene model development are described in Rele et al. (2023). Genomic structure information (e.g., CDSs, intron-exon number and boundaries, number of isoforms) for the D. melanogaster reference gene is retrieved through the Gene Record Finder ( https://gander.wustl.edu/~wilson/dmelgenerecord/index.html ; Rele et al ., 2023). Approximate splice sites within the target gene are determined using tblastn using the CDSs from the D. melanogaste r reference gene. Coordinates of CDSs are then refined by examining aligned modENCODE RNA-Seq data, and by applying paradigms of molecular biology such as identifying canonical splice site sequences and ensuring the maintenance of an open reading frame across hypothesized splice sites. Students then confirm the biological validity of their target gene model using the Gene Model Checker ( https://gander.wustl.edu/~wilson/dmelgenerecord/index.html ; Rele et al., 2023), which compares the structure and translated sequence from their hypothesized target gene model against the D. melanogaster reference gene model. At least two independent models for a gene are generated by students under mentorship of their faculty course instructors. Those models are then reconciled by a third independent researcher mentored by the project leaders to produce the final model. Note: comparison of 5' and 3' UTR sequence information is not included in this GEP CURE protocol.

Acknowledgments

Acknowledgments

This publication is dedicated to the memory of Dr. James J. Youngblom. We would like to thank Wilson Leung for developing and maintaining the technological infrastructure that was used to create this gene model and Bethany C. Lieser for retrofitting this model. Thank you to FlyBase for providing the definitive database for Drosophila melanogaster gene models. FlyBase is supported by grants: NHGRI U41HG000739 and U24HG010859, UK Medical Research Council MR/W024233/1, NSF 2035515 and 2039324, BBSRC BB/T014008/1, and Wellcome Trust PLM13398.

Funding Statement

This material is based upon work supported by the National Science Foundation (1915544) and the National Institute of General Medical Sciences of the National Institutes of Health (R25GM130517) to the Genomics Education Partnership (GEP; https://thegep.org/; PI-LKR). Any opinions, findings, and conclusions or recommendations expressed in this material are solely those of the author(s) and do not necessarily reflect the official views of the National Science Foundation nor the National Institutes of Health.

Extended Data

Description: A GFF, FASTA, and PEP of the model. Resource Type: Dataset. DOI: https://doi.org/10.22002/r7f2j-ads26

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Description: A GFF, FASTA, and PEP of the model. Resource Type: Dataset. DOI: https://doi.org/10.22002/r7f2j-ads26

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