Peng Z et al. (2024), Genome-Wide Comparative Analysis of SRCR Gene S...

ECB-ART-52880

Int J Mol Sci 2024 Jan 26;253:. doi: 10.3390/ijms25031515.

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Genome-Wide Comparative Analysis of SRCR Gene Superfamily in Invertebrates Reveals Massive and Independent Gene Expansions in the Sponge and Sea Urchin.

Peng Z , Zhang W , Fu H , Li Y , Zhang C , Li J , Chan J , Zhang L .

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Without general adaptative immunity, invertebrates evolved a vast number of heterogeneous non-self recognition strategies. One of those well-known adaptations is the expansion of the immune receptor gene superfamily coding for scavenger receptor cysteine-rich domain containing proteins (SRCR) in a few invertebrates. Here, we investigated the evolutionary history of the SRCR gene superfamily (SRCR-SF) across 29 metazoan species with an emphasis on invertebrates. We analyzed their domain architectures, genome locations and phylogenetic distribution. Our analysis shows extensive genome-wide duplications of the SRCR-SFs in Amphimedon queenslandica and Strongylocentrotus purpuratus. Further molecular evolution study reveals various patterns of conserved cysteines in the sponge and sea urchin SRCR-SFs, indicating independent and convergent evolution of SRCR-SF expansion during invertebrate evolution. In the case of the sponge SRCR-SFs, a novel motif with seven conserved cysteines was identified. Exon-intron structure analysis suggests the rapid evolution of SRCR-SFs during gene duplications in both the sponge and the sea urchin. Our findings across nine representative metazoans also underscore a heightened expression of SRCR-SFs in immune-related tissues, notably the digestive glands. This observation indicates the potential role of SRCR-SFs in reinforcing distinct immune functions in these invertebrates. Collectively, our results reveal that gene duplication, motif structure variation, and exon-intron divergence might lead to the convergent evolution of SRCR-SF expansions in the genomes of the sponge and sea urchin. Our study also suggests that the utilization of SRCR-SF receptor duplication may be a general and basal strategy to increase immune diversity and tissue specificity for the invertebrates.

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	Figure 1. The distribution of members of the SRCR-SFs in 29 representative animal species across metazoans. The colors of species represent different phyla. The red cladogram on the left illustrates the phylogenetic relationships between species, with dashed lines indicating the disputed phylogenetic positions of ctenophores and sponges. The blue histogram on the right chart tallies the total number of identified SRCR-SFs for each species.
	Figure 2. Transcriptome expression heatmaps of SRCRs of different tissues in nine representative metazoan species. Amphimedon queenslandica: archeocyte (Ac), choanocyte (Cc), pinacocyte (Pc; Nematostella vectensis: mesenterial filament 1 (Mf1), mesenterial filament 2 (Mf2), muscle 1 (M1), muscle 2 (M2), gonad 1 (G1), gonad 2 (G2); Phoronis australis: trunk with lophophore (TL), trunk (TK), lophophore (LP), ampulla (AM), actinotroch larva (AL), whole animal (W); Notospermus geniculatus: posterior end (PE), proboscis (PB), midbody with gut (MB), anterior part1 (AP1), anterior part2, posterior half without head (AP2), female midbody with gut (MB(F)), anterior end (AE); Lingula anatina: lophophore (LP), whole gut tissue (GT), digestive cecum (DC), dorsal mantle (DM), ventral mantle (VM), pedicle (PD), regenerated pedicle (RP); Octopus bimaculoides: sucker rims dissociated cells (SD), brain tissue from optic lobe (BO), eye (E), olfactory organ (OO), skin from mantle (SM), statocyst tissue (ST); Crassostrea gigas: digestive gland (DG), gill (G), male gonad (MG), female gonad (FG), muscle (MU); Acanthaster planci: stomach (SO), tube fee (TF), sensory tentacle (ST), eyes (E), radial nerve (RN), testes (T); Strongylocentrotus purpuratus: adult lantern (Al), adult guts (Ag), adult epidermis (Ae), adult radial nerve (Ar). Heatmap displays the expression level of SRCR genes.
	Figure 3. Genomic distribution analysis of sponge SRCR-SFs. (A) Proportions of clustered and individual members of sponge SRCR-SFs. Blue represents the 138 members of sponge SRCR-SFs scattered on the scaffolds; orange represents the 158 members of sponge SRCR-SFs linked in tandem array. (B) The histogram shows the tandem clusters containing 2, 3, 4, 5, 6, and 7 SRCR-SFs. (C) Gene distribution of the scaffold (NW_003546273.1) with the most SRCR-SFs in the sponge is shown. Pink represents SRCR-SFs, blue represents non-SRCR-SF genes. Numbers represent the quantity of SRCR domains encoded by a certain gene.
	Figure 4. Gene structure analysis of sponge SRCR-SFs. (A) Gene structure of the tandem gene cluster with the largest number of sponge SRCR-SFs. Blue represents exon, green represents UTR, orange represents SRCR domains, black horizontal lines represent intron, light orange represents SignalP (signal peptide), light green represents TM, and numbers represent sequence lengths. (B) Sequence similarity of sponge SRCR-SFs. Blue represents exon, black horizontal lines represent intron.
	Figure 5. The replication units of SRCR-SFs. The predicted essential units include a single or two SRCR domains. Type 1 signifies that the SRCR gene is replicated from a single SRCR domain, while Type 2 signifies that the SRCR gene is replicated from two SRCR domains as a group. Type 3 and Type 4 signifies duplication with both Type 1 and Type 2 units.
	Figure 6. Gene distribution analysis of sea urchin SRCR-SFs. (A) The proportion of scattered and tandem linked SRCR-SFs in the sea urchin genome. Blue indicates that 104 SRCR-SFs are scattered on the scaffolds, while orange indicates that 253 SRCR-SFs are linked in tandem array. (B) A histogram showing the number of clusters containing 2, 3, 4, 5, 6, 7, 9, 10, 13 and 16 SRCR genes. (C) The gene distribution of SRCR-SFs on the scaffold (NW_022145609.1). Pink represents SRCR-SFs, blue represents non-SRCR-SF genes. Numbers represent the quantity of SRCR domains encoded by a certain gene.
	Figure 7. Gene structure analysis of sea urchin SRCR-SFs. (A) The gene structure of the SRCR-SFs in sea urchins is shown (gene cluster in Figure 6C). Blue represents exon, orange represents SRCR domain, black horizontal lines represent intron, and white numbers represent sequence length. (B) Analysis of special exon sequence alignment. Sequence alignment analysis was performed on the exons marked by the same color dashed box in (A). Red arrows mark the mutations.
	Figure 8. Analysis of different types of SRCR domain motifs and three-dimensional structure analysis. (A) Comparative analysis of motifs of Group A, Group B, and Group C SRCR domains. (B) Comparative analysis of the three-dimensional structures of Group A, Group B, and Group C SRCR domains. The numbers represent conserved cysteine sites.

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