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. 2024 Nov 30;2024:10.17912/micropub.biology.000856. doi: 10.17912/micropub.biology.000856

Gene model for the ortholog Myc in Drosophila ananassae

Abigail Myers 1, Alexa Hoffman 2, Mindy Natysin 3, Andrew M Arsham 3, Joyce Stamm 2, Jeffrey S Thompson 4, Chinmay P Rele 5, Laura K Reed 6,§
Reviewed by: GEP Review Panel 2, David Molik, Sebastian Sorge
PMCID: PMC11645546  PMID: 39677519

Abstract

Gene model for the ortholog of Myc ( Myc ) 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 Myc in Drosophila ananassae .

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

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(A) Synteny comparison of the genomic neighborhoods for Myc in Drosophila melanogaster and D. ananassae . Thin underlying arrows indicate the DNA strand within which the target gene– Myc –is located in D. melanogaster (top) and D. ananassae (bottom). Thin arrow(s) pointing to the right indicate(s) that Myc is on the positive (+) strand in D. ananassae and D.melanogaster . The wide gene arrows pointing in the same direction as Myc are on the same strand relative to the thin underlying arrows, while wide gene arrows pointing in the opposite direction of Myc 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 Myc in D. ananassae are displayed in the User Supplied Track (black); 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 Wolbachia -cured Embryos (red, light blue, and pink respectively; alignment of Illumina RNA-Seq reads from D. ananassae ), and Splice Junctions Predicted by regtools using D. ananassae RNA-Seq (Graveley et al. , 2011; SRP006203 , SRP007906 ; PRJNA257286 , PRJNA388952 ). Splice junctions shown have a read-depth of >1000 supporting reads in red. (C) Dot Plot of Myc-PB in D. melanogaster ( x -axis) vs. the orthologous peptide in D. ananassae ( y -axis). Amino acid number is indicated along the left and bottom; CDS number is indicated along the top and right, and CDSs are also highlighted with alternating colors. Tandem repeats of serine are present in both sequences of the second CDS represented by the red box, Box W. (D) The Conservation Track of 28 Drosophila Species compared to CDSs one and two of D. melanogaster Myc-RA and Myc-RB contains many regions having lack of sequence similarity (vertical red boxes, Box X and Y; D. ananassae is highlighted in the horizontal red box, Box Z).

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 D. melanogaster genes in the insulin signaling pathway (ISP).

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 (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.

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) .

" 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 2006; 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, submitted).

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We propose a gene model for the D. ananassae ortholog of the D. melanogaster Myc ( Myc ) gene. The genomic region of the ortholog corresponds to the uncharacterized protein LOC6502359 (RefSeq accession XP_044573530.1 ) in the dana_caf1 Genome Assembly of D. ananassae (GenBank Accession: GCA_000005115.1 ; Drosophila 12 Genomes Consortium 2007). This model is based on RNA-Seq data from D. ananassae ( SRP006203 , SRP007906 ; PRJNA257286 , PRJNA388952 - Graveley et al., 2011 ) and Myc in D. melanogaster using FlyBase release FB2022_04 ( GCA_000001215.4 ; Larkin et al., 2021; Gramates et al., 2022; Jenkins et al., 2022).

Myc acts downstream of the insulin signaling pathway, with Myc protein accumulating in response to insulin through transcriptional and post-transcriptional mechanisms (Parisi et al., 2011) , resulting in the activation of genes involved in anabolic processes that promote cell growth (Terakawa et al., 2022) . Myc encodes a basic helix-loop-helix transcription factor in Drosophila melanogaster that is homologous to vertebrate Myc proto-oncogenes (Gallant et al., 1996) . In Drosophila melanogaster , Myc transcriptionally regulates a wide range of genes, including those that influence cell growth and metabolism (Teleman et al., 2008; Gallant 2013) .

Synteny

The reference gene, Myc, occurs on chromosome X in D. melanogaster and is flanked upstream by new glue 4 ( ng4 ), and dunce ( dnc ), which nests Pre-intermoult gene 1 ( Pig1 ), salivary gland secretion 4 ( Sgs4 ) and CG10793 . Myc is flanked downstream by CG12535 and CG14269 . The tblastn search of D. melanogaster Myc-PB (query) against the D. ananassae (GenBank Accession: GCA_000005115.1 ) Genome Assembly (database) placed the putative ortholog of Myc within scaffold_12613 ( CH902663.1 ) at locus LOC6502359 (XP_ 044573530.1 )— with an E-value of 1e-42 and a percent identity of 36.30%. Furthermore, the putative ortholog is flanked upstream by LOC116655047 ( XP_032307915.1 ) and LOC6502358 ( XP_032307954.2 ) which nests LOC6502594 ( XP_032307960.1 ) and correspond to ng4 , dnc, and CG10793 in D. melanogaster (E-value: 4e-16, 0.0, and 0.0; identity:71.43%, 84.49% and 80.13%, respectively, as determined by blastp ; Figure 1A, A ltschul et al., 1990). The putative ortholog of Myc is flanked downstream by LOC6502362 ( XP_001967532.1 ) and LOC6502361 ( XP_001967530.1 ), which correspond to CG12535 and CG14269 in D. melanogaster (E-value: 7e-45 and 1e-104; identity: 47.80% and 83.16%, respectively, as determined by blastp ). The putative ortholog assignment for Myc in D. ananassae is supported by the following evidence: The genes surrounding the Myc ortholog are orthologous to the genes at the same locus in D. melanogaster and local synteny is nearly completely conserved, so we conclude that LOC6502359 is the correct ortholog of Myc in D. ananassae ( Figure 1A ).

Protein Model

Myc in D. ananassae has one unique protein-coding isoforms ( Figure 1B ), encoded by mRNA isoforms Myc-RB and Myc-RA that differ in their UTRs, and contain two CDSs. Relative to the ortholog in D. melanogaster , the RNA CDS number and protein isoform count is conserved. The sequence of Myc-PB in D. ananassae has 44.38% identity (E-value: 9e-77) with the protein-coding isoform Myc-PB in D. melanogaster , as determined by blastp ( Figure 1C ). Box W in red highlights tandem repeats of serine in CDS two, shown in Figure 1C . Coordinates of this curated gene model are stored by NCBI at GenBank/BankIt ( BK064666 and BK064667 ). These data are also archived in the CaltechDATA repository (see “Extended Data” section below).

Special characteristics of the protein model

Regions of low conservation: Lack of sequence similarity in CDSs one and two of Myc-RA and Myc-RB is displayed in the 28 Drosophila Species Conservation track ( Figure 1D ) within the vertical red boxes (X and Y). The most obvious lack of sequence similarity primarily exists at the start of the first CDS and in the middle of CDS two in many Drosophila species including D. ananassae which is indicated by the horizontal red box ( Figure 1D ). This lack of sequence similarity is likely due to the divergence of the species D. ananassae from 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 target gene for a given isoform and run it using tblastn against their target Drosophila species genome assembly ( D. ananassae (GenBank Accession: GCA_000005115.1 ) 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. Genomic structure information (e.g., CDSs, CDS 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 each gene are generated by students under mentorship of their faculty course instructors. These models are then reconciled by a third independent researcher mentored by the project leaders to produce a final model like the one presented here. Note: comparison of 5' and 3' UTR sequence information is not included in this GEP CURE protocol.

Extended Data

Description: GFF, FASTA, and PEP sequences for Myc in D ananassae. Resource Type: Dataset. DOI: 10.22002/0c391-eeh07

Acknowledgments

Acknowledgments

We would like to thank Wilson Leung for developing and maintaining the technological infrastructure that was used to create this gene model and Laura K. Reed for overseeing the project. Also, thank you to Madeline Gruys and Logan Cohen for assistance in updating the manuscript to the current template. 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. This article was prepared while Joyce Stamm was employed at the University of Evansville. The opinions expressed in this article are the author's own and do not reflect the view of the National Institutes of Health, the Department of Health and Human Services, or the United States government.

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.

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