Jönsson M et al. (2022), Sex-specific expression of pheromones and other...

ECB-ART-51109

BMC Biol 2022 Dec 17;201:288. doi: 10.1186/s12915-022-01491-0.

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Sex-specific expression of pheromones and other signals in gravid starfish.

Jönsson M , Morin M , Wang CK , Craik DJ , Degnan SM , Degnan BM .

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BACKGROUND: Many echinoderms form seasonal aggregations prior to spawning. In some fecund species, a spawning event can lead to population outbreaks with detrimental ecosystem impacts. For instance, outbreaks of crown-of-thorns starfish (COTS), a corallivore, can destroy coral reefs. Here, we examine the gene expression in gravid male and female COTS prior to spawning in the wild, to identify genome-encoded factors that may regulate aggregation and spawning. This study is informed by a previously identified exoproteome that attracts conspecifics. To capture the natural gene expression profiles, we isolated RNAs from gravid female and male COTS immediately after they were removed from the Great Barrier Reef. RESULTS: Sexually dimorphic gene expression is present in all seven somatic tissues and organs that we surveyed and in the gonads. Approximately 40% of the exoproteome transcripts are differentially expressed between sexes. Males uniquely upregulate an additional 68 secreted factors in their testes. A suite of neuropeptides in sensory organs, coelomocytes and gonads is differentially expressed between sexes, including the relaxin-like gonad-stimulating peptide and gonadotropin-releasing hormones. Female sensory tentacles-chemosensory organs at the distal tips of the starfish arms-uniquely upregulate diverse receptors and signalling molecules, including chemosensory G-protein-coupled receptors and several neuropeptides, including kisspeptin, SALMFamide and orexin. CONCLUSIONS: Analysis of 103 tissue/organ transcriptomes from 13 wild COTS has revealed genes that are consistently differentially expressed between gravid females and males and that all tissues surveyed are sexually dimorphic at the molecular level. This finding is consistent with female and male COTS using sex-specific pheromones to regulate reproductive aggregations and synchronised spawning events. These pheromones appear to be received primarily by the sensory tentacles, which express a range of receptors and signalling molecules in a sex-specific manner. Furthermore, coelomocytes and gonads differentially express signalling and regulatory factors that control gametogenesis and spawning in other echinoderms.

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	Fig. 1. Differential expression of CDS in male and female COTS tissues/organs. A PCA of global gene expression profiles for the eight different COTS tissues/organs. B PCAs for only aboral (top) and oral (bottom) tissues/organs. C Pairwise correlation of eight tissue/organ transcriptomes; female and male gonads and coelomocyte transcriptomes are distinct from all other tissues. Pink, tube feet; purple, sensory tentacles; green, radial nerve; turquoise, skin; brown, papulae; blue, spines; red, coelomocytes; yellow, gonads; circles, females; triangles, males. Depicted values illustrate the scaled (z-score) expression levels based on collapsed VST-normalised read counts
	Fig. 2. Expression of potential attractants and spawning factors in COTS tissues/organs. A Expression of 84 putative attractant CDS [28]. Male and female expression profiles are grouped by tissues/organs. Heatmap of expression levels in eight tissues/organs combine all analysed CEL-Seq2 data. Depicted values illustrate scaled (z-score) expression levels based on TPM normalised reads from seven females and six males (except radial nerve, which is from five males). Pie charts depict the proportion of highly expressed genes, per tissue, that fall into broad secreted protein classes (blue, hydrolytic enzymes; light green, other enzymes; orange, enzyme inhibitors; green, structural/signalling proteins; red, conserved uncharacterized proteins; yellow, uncharacterised proteins). B Individual COTS expression profiles of the 37 putative attractants that are significantly differentially expressed between the testes and the ovaries. CDS names are listed to the right. Left heatmap, quartile analysis of the mean transcript abundance; Q4, most highly expressed CDS; Q1, lowest expressed CDS; and 0, expression was not detected. Right heatmap, TPM normalised expression. Star (*) indicates the COTS-specific ependymin-related proteins. C Heatmap of 194 putative secreted proteins upregulated in male tissues/organs, 68 of which are highly expressed in the testes. Highlighted are conserved CDS of interest (Additional file 2: Table S2.3)
	Fig. 3. Neuropeptidome expression in the sensory tentacles and other tissues and organs. A Expression of 39 neuropeptides [122]. Male and female expression profiles are grouped by tissues/organs. Left heatmap, quartile analysis of the mean transcript abundance; Q4, most highly expressed CDS; Q1, lowest expressed CDS; and 0, no expression was detected. The right heatmap illustrates the scaled (z-score) expression levels based on TPM normalised read counts. Star (*) indicates the significant differential expression between male and female sensory tentacles. B Expression level of RGP across the different tissues/organs. Males and females are grouped by tissue/organ. Values depict square root-transformed TPM read counts of RGP. The expression of RGP is significantly higher in the coelomocytes of both sexes compared to all other tissues (p-adj < 0.001). C Volcanoplot of 15,777 expressed CDS in male and female sensory tentacles. Grey dots depict non-significantly differentially expressed CDS, and black dots depict significantly differentially expressed CDS (146) (p-adj < 0.05). Highlighted CDS names: green, neuropeptides; red, transcription factors; purple, GPCRs. CDS with negative and positive Log2fold change are upregulated in female and male sensory tentacles, respectively
	Fig. 4. GPCR expression. A The number and subfamily type of GPCRs expressed in each tissue/organ (blue, olfactory receptors; orange, other class A rhodopsin-like; grey, class B secretin-like; yellow, class C glutamate-like; light blue, class F frizzled; green, others). B Upset plot of expressed GPCRs. The 276 GPCRs expressed commonly by all tissues are not shown. The interaction size is the number of GPCRs expressed uniquely or in tissue combinations shown at the bottom of the graph. C Expression heatmap of kisspeptin, CRZ, GnRH, orexin and RGP and their putative receptors. The expression of the neuropeptide is shown above their putative receptors. Male and female expression profiles are grouped by tissue/organ. Depicted values illustrate scaled (z-score) of TPM normalised read counts. D Maximum likelihood tree showing the phylogenetic relationship of four COTS relaxin receptor-likes to other metazoans. The outgroup is tachykinin-like receptors (grey). gbr.100.30.t1 is more closely related to GRL101 receptors (green), whereas gbr.180.30.t1, gbr.57.58.t1 and gbr.152.19.t1 cluster with other relaxin receptor-likes (red) and fall within echinoderm-specific clades. Model of substitution: LG + F + R8, with 1000 bootstrap replications visualised on the tree’s main branches (Fasta file and full tree with all bootstrap values are available in Additional files 9 and 10)
	Fig. 5. Proposed regulation of COTS spawning based on the gene expression profiles. (1) Physical seasonal environmental cues such as temperature and photoperiod trigger the commencement of gonad growth and gametogenesis and potentially sexually dimorphic gene expression. (2) Maturing individuals migrate towards shallow waters for spawning, with chemotaxis occurring along conspecific pheromone gradients. (3) Once aggregated, males initiate spawning based on abiotic and biotic (pheromones) cues. Spawning males release attractants and factors that trigger final oocyte maturation and spawning in females. (4) Females are competent to receive and transduce signals associated with the male spawn via receptors, hormones and neuropeptides in their sensory tentacles. (5) For both sexes, internal signalling cascades may include the secretion of neuropeptides, such as kisspeptin and SALMFamide, or a GnRH-like factor from sensory tentacles and radial nerves. (6) These may bind to cell-surface receptors on the coelomocytes, which may induce the secretion of RGP into the coelomic fluid. (7) RGP binds to cell-surface receptors on the gonads, (8) triggering the release of 1-methyladenine, which leads to oocyte maturation, the contraction of the gonad walls and the spawning of mature eggs

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