Population biology of accessory gland-expressed <i>de novo</i> genes in <i>Drosophila melanogaster</i>

Cridland, Julie M.; Majane, Alex C; Zhao, Li; Begun, David J.

doi:10.1093/genetics/iyab207

Cited by 16 publications

(33 citation statements)

References 65 publications

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“…As an example, whether evolutionarily young genes function as RNAs or as proteins is often an area of debate. One of the earliest recognized young genes is an RNA ( Wang et al, 2002 ); other studies also had similar conclusions ( Cridland et al, 2022 ; Ruiz-Orera et al, 2015 ). In contrast, in several cases, even de novo genes have been empirically shown to yield protein products ( Bungard et al, 2017 ; Cai et al, 2008 ; Knowles and McLysaght, 2009 ; Li et al, 2010 ; Zhang et al, 2019 ).…”

Section: Introductionmentioning

confidence: 65%

Protein evidence of unannotated ORFs in Drosophila reveals diversity in the evolution and properties of young proteins

Zheng

Zhao

2022

eLife

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De novo gene origination, where a previously non-genic genomic sequence becomes genic through evolution, has been increasingly recognized as an important source of evolutionary novelty across diverse taxa. Many de novo genes have been proposed to be protein-coding, and in several cases have been experimentally shown to yield protein products. However, the systematic study of de novo proteins has been hampered by doubts regarding the translation of their transcripts without the experimental observation of protein products. Using a systematic, ORF-focused mass-spectrometry-first computational approach, we identify almost 1000 unannotated open reading frames with evidence of translation (utORFs) in the model organism Drosophila melanogaster, 371 of which have canonical start codons. To quantify the comparative genomic similarity of these utORFs across Drosophila and to infer phylostratigraphic age, we further develop a synteny-based protein similarity approach. Combining these results with reference datasets on tissue- and life-stage-specific transcription and conservation, we identify different properties amongst these utORFs. Contrary to expectations, the fastest-evolving utORFs are not the youngest evolutionarily. We observed more utORFs in the brain than in the testis. Most of the identified utORFs may be of de novo origin, even accounting for the possibility of false-negative similarity detection. Finally, sequence divergence after an inferred de novo origin event remains substantial, raising the possibility that de novo proteins turn over frequently. Our results suggest that there is substantial unappreciated diversity in de novo protein evolution: many more may exist than have been previously appreciated; there may be divergent evolutionary trajectories; and de novo proteins may be gained and lost frequently. All in all, there may not exist a single characteristic model of de novo protein evolution, but instead, there may be diverse evolutionary trajectories for de novo proteins.

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Section: Introductionmentioning

confidence: 65%

Protein evidence of unannotated ORFs in Drosophila reveals diversity in the evolution and properties of young proteins

Zheng

Zhao

2022

eLife

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“…Alignment, barcode removal, and UMI counting were done in CellRanger (6.1.2) with the “count” command. Reads were aligned to version 6.41 of the D. melanogaster genome (FlyBase, downloaded August 9, 2021), with an index built using CellRanger “mkref.” To the FlyBase D. melanogaster 6.41 GTF file, we added de novo gene annotations from (Cridland et al 2022) and de novo and newly assembled gene annotation models from (Lombardo et al 2023). Because the cellranger pipeline does not accept annotations with unknown strandedness, we edited the annotations for all single exon de novo genes to be on the ‘+’ strand.…”

Section: Methodsmentioning

confidence: 99%

Regional specialization, polyploidy, and seminal fluid transcripts in the Drosophila female reproductive tract

Thayer,

Polston,

et al. 2023

Preprint

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Internal fertilization requires the choreographed interaction of female cells and molecules with seminal fluid and sperm. In many animals, including insects, the female reproductive tract is physically subdivided into sections that carry out specialized functions. For example, females of many species have specialized organs for sperm storage.Drosophila melanogasteris a premier model system for investigating many aspects of animal reproduction. Nevertheless, in contrast to males, much of the basic biology of theD. melanogasterfemale reproductive tract remains poorly understood or completely unknown. Here we use single-cell RNA-seq data and in situ hybridization to reveal a rich and previously unknown female reproductive tract cell diversity, including widespread variation in ploidy levels. We find that many so-called seminal fluid protein genes appear to be transcribed in specialized cells of the female reproductive tract, motivating a re-evaluation of the functional and evolutionary biology of this major class of proteins.

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“…Previous allelic imbalance experiments found the expression of de novo genes to be partially explained, in most cases, by cis-regulatory variation, suggesting a local genetic basis for their expression (5,18). However, genetic variation can affect expression variance among genetically identical cells ("expression noise") as well as mean expression level (39)(40)(41).…”

Section: Sampling and Estimating The Age Of De Novo Genesmentioning

confidence: 99%

“…We selected D. melanogaster annotated genes (v6.41 D. melanogaster release) that demonstrated strong AG bias. This procedure was similar to Cridland et al (18). We used the FlyAtlas2 data (57) to identify genes that showed the highest expression in the D. melanogaster AG and showed tissue specificity index (58) τ > 0.9.…”

Section: Selection Of Ag-biased Annotated Genesmentioning

confidence: 99%

New insights into the dynamics ofde novogene origin

Blair,

Cridland,

Luo

et al. 2023

Preprint

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The evolution of genesde novofrom ancestrally nongenic sequences is a significant mechanism of gene origin. Many studies have focused on distant evolutionary comparisons, which bias the sample ofde novogenes towards older genes that have acquired important functions and have been refined by selection. In this report, we focus on the earliest steps inde novogene origin by identifying young, polymorphic transcripts that may be missed by other study designs. To accomplish this, we sequenced tissue-specific transcriptomes from a much larger sample of genotypes than have been used in previous analyses ofde novogenes inDrosophila melanogaster. We identified 90 potential species-specificde novogenes expressed in the male accessory glands of 29D melanogasterlines derived from the same natural population. We find that most young, unannotated transcripts are both rare in the population and transcribed at low abundance. Improved sampling of both ingroup and outgroup genotypes reveals that many young genes are polymorphic in more than one species, resulting in substantial uncertainty about the age and phylogenetic distribution ofde novogenes. Among the genes expressed in the same tissue, gene age correlates with proximity to other tissue-specific genes, with the youngest genes being least likely to occur near established tissue-specific genes. This and other lines of evidence suggest thatde novogenes do not commonly evolve by simply reutilizing pre-existing regulatory elements. Together, these results provide new insights into the origin and early evolution ofde novogenes.Author SummaryGenes may be born and lost without any lasting evidence of their existence. The typical longevity may be especially limited forde novogenes – that is, genes that originate from ancestrally non-genic, untranscribed sequences, since most genomic regions are not expected to be beneficial when transcribed. To better capture the population biology of nascentde novogenes at points close to their origin, we sequenced tissue-specific transcriptomes from a large number ofDrosophila melanogastergenotypes. Mostde novogenes were expressed in very few genotypes, consistent with the expectation of transience and rapid turnover. However, many young genes showed polymorphic transcription in multiple species, suggesting that the combination of low frequency with limited sampling can lead us to underestimate how longde novogenes persist in populations. We identified several features thatde novogenes come to share with established tissue-specific genes the longer they persist. This study highlights important challenges in reconstructingde novogene origin and helps elucidate why some transcripts may survive long enough to acquire selectable functions.

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Population biology of accessory gland-expressed de novo genes in Drosophila melanogaster

Cited by 16 publications

References 65 publications

Protein evidence of unannotated ORFs in Drosophila reveals diversity in the evolution and properties of young proteins

Protein evidence of unannotated ORFs in Drosophila reveals diversity in the evolution and properties of young proteins

Regional specialization, polyploidy, and seminal fluid transcripts in the Drosophila female reproductive tract

New insights into the dynamics ofde novogene origin

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