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. 2025 Sep 16;16(9):1095.
doi: 10.3390/genes16091095.

Transcriptome of Sterile Testes in dnd-Depleted Atlantic Salmon (Salmo salar L.) Highlights Genes Involved in Gonadal and Brain Development

Aleksei Krasnov  1 , Sergey Afanasyev  2 , Jens-Erik Dessen  1 , Marianne H S Hansen  1 , Marianne Vaadal  1 , Helge Tveiten  3 , Øivind Andersen  1
Affiliations

Transcriptome of Sterile Testes in dnd-Depleted Atlantic Salmon (Salmo salar L.) Highlights Genes Involved in Gonadal and Brain Development

Aleksei Krasnov et al. Genes (Basel). .

Abstract

Background/objectives: Inactivation of the dnd gene involved in the development of primordial germ cells (PGCs) leads to the loss of gametes and halts reproductive development. Studies on sterile fish allow for the identification of genes and processes associated with GC differentiation.

Methods: Atlantic salmon with GC-ablated testes were produced by temporal silencing of dnd. Gene expression was analyzed in sterile and fertile testes using 44k microarray and qPCR.

Results: In sterile testes, transcripts of several GC markers were detected at low levels, suggesting the presence of cells with a GC-related expression profile that failed to initiate spermatogenesis. Expression of 260 genes was undetectable in the gonads of sterile males and females, and 61.5% of these were also inactivated during first maturation of fertile testes. This group was enriched with genes highly expressed in the brain, including those involved in endocrine and paracrine regulation, synaptic transmission, and numerous genes critical for brain development; among them, 45 genes encoding homeobox proteins. Another group of 229 genes showed increased expression in developing testes and included genes involved in neurosecretion and brain development regulation. GC-ablated testes showed increased expression of reproductive regulators such as amh and sdy and numerous immune genes, suggesting a reprogramming of GC-depleted testes. Temporal silencing of dnd indicated common developmental processes in the brains and gonads of Atlantic salmon testis that become inactive in testes at first maturation. These processes may play roles in PGC homing, the creation of a specific environment required for spermatogenesis, or facilitating communication between the gonads.

Keywords: Atlantic salmon; dead end; reprogramming; testes; transcriptome.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Gene markers of germ cells. (a) Microarray. Panel presents percentage of sterile testes in which expression was not detected; expression in relation to Atlantic salmon tissues (dSI, body map) and changes (log2-ER) during gonadal growth (w6/w0) and maturation of large fish (LM/LI). Differential expression is indicated with bold italics. (b) RT-qPCR of selected GC markers in sterile and fertile testes (centered ΔCt). Dnd was not detected in sterile testes.
Figure 2
Figure 2
Genes undetectable in at least ¾ of the sterile GC-depleted testes and ovaries and ½ of fertile maturing testes. The percentage of samples lacking transcripts is shown. dSI reflects the expression levels in normal testes and brain in relation to Atlantic salmon tissues (body map). Color highlights genes associated with developmental (light blue) and endocrine (green) processes, and genes involved in neural system function (light red).
Figure 3
Figure 3
Genes with increased expression during normal gonadal growth from w0 to w6 that were downregulated in sterile testes. The percentage of samples lacking detectable transcripts is shown. dSI reflects the expression levels in normal testes and brain in relation to Atlantic salmon tissues (body map). Color highlights genes associated with nervous system (yellow), development (gray), and reproduction (light blue).
Figure 4
Figure 4
Genes undetectable in not less than ½ of sterile testes that were upregulated during sexual maturation. Color highlights genes associated with cilia structure and activity (light blue), DNA recombination (yellow), and regulation of spermatogenesis (light green). dSI reflects expression levels in normal testes in relation to Atlantic salmon tissues (body map).
Figure 5
Figure 5
Genes upregulated in sterile testis. Differential expression (log2-ER) of sterile (S) to fertile (F) testes and mature (M) to immature testes (I) of large fish. dSI reflects expression in normal testes in relation to Atlantic salmon tissues (body map). Color highlights testis-specific genes. dSI > 4.3 (light blue) and genes with high expression in sterile testes (light red).
Figure 6
Figure 6
Genes upregulated in sterile testes. (a): Functional groups (STARS annotation) with similar expression changes. DEG numbers are indicated, data is mean log2-ER of sterile to fertile gonads (S/F) and maturing to immature testes of large fish (LM/LI). (b): Enrichment analysis, most highly ranked terms. (c): Expression of genes upregulated in sterile testes in Atlantic salmon tissues and cells (body map, dSI). TM—transcription modules, ECM—extracellular matrix, N—number of genes.
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