Delegating Sex: Differential Gene Expression in Stolonizing Syllids Uncovers the Hormonal Control of Reproduction

Abstract

Stolonization in syllid annelids is a unique mode of reproduction among animals. During the breeding season, a structure resembling the adult but containing only gametes, called stolon, is formed generally at the posterior end of the animal. When stolons mature, they detach from the adult and gametes are released into the water column. The process is synchronized within each species, and it has been reported to be under environmental and endogenous control, probably via endocrine regulation. To further understand reproduction in syllids and to elucidate the molecular toolkit underlying stolonization, we generated Illumina RNA-seq data from different tissues of reproductive and nonreproductive individuals of Syllis magdalena and characterized gene expression during the stolonization process. Several genes involved in gametogenesis (ovochymase, vitellogenin, testis-specific serine/threonine-kinase), immune response (complement receptor 2), neuronal development (tyrosine-protein kinase Src42A), cell proliferation (alpha-1D adrenergic receptor), and steroid metabolism (hydroxysteroid dehydrogenase 2) were found differentially expressed in the different tissues and conditions analyzed. In addition, our findings suggest that several neurohormones, such as methyl farnesoate, dopamine, and serotonin, might trigger stolon formation, the correct maturation of gametes and the detachment of stolons when gametogenesis ends. The process seems to be under circadian control, as indicated by the expression patterns of r-opsins. Overall, our results shed light into the genes that orchestrate the onset of gamete formation and improve our understanding of how some hormones, previously reported to be involved in reproduction and metamorphosis processes in other invertebrates, seem to also regulate reproduction via stolonization.

Comparative Aspects of Annelid Regeneration: Towards Understanding the Mechanisms of Regeneration

“…However, this effect may be manifested in opposite ways during different ontogenetic stages and in different taxa [65]. Recent advances in the studies of the molecular nature of such humoral factors in nereids and syllids [125][126][127] open fascinating possibilities for a fundamentally new understanding of the NS systemic action on specific targets in the context of environmental conditions.…”

Rethinking Sesquiterpenoids: A Widespread Hormone in Animals

“…MF application suppressed the expression of the yolk protein gene Vitellogenin (Vg) and arrested reproductive maturation [ 49 ]. Later, in another polychaete Syllis magdolena , MF, along with dopamine and serotonin, was found to trigger the formation of a posterior gamete containing a structure known as a stolon, which upon maturation releases gametes [ 50 ]. Recent genome analyses have also revealed the presence of biosynthetic pathway genes in gastropods and bivalves, and in vivo MF treatment could alter the gene expression of sesquiterpenoid pathway genes in the snail Biomphalaria straminea [ 51 ].…”

Differential Gene Expression Between Polymorphic Zooids of the Marine BryozoanBugulina stolonifera

“…Transcriptome annotations: The relatively high percentage of unannotated sequences in our transcriptome is likely due to the low representation of bryozoan sequences in publicly available databases and percent annotation in this study is similar to those in studies of other underrepresented metazoans (Wong et al 2014;Kitchen et al 2015;Álvarez-Campos et al 2019).…”

“…Additionally, a reference transcriptome from all six sample types together was constructed, for a downstream comparison by genetic individual. Lastly, four additional zooid-specific assemblies were constructed to more clearly isolate a signal of tissue-specific expression in downstream differential gene expression analyses, focusing on four biologically relevant pairwise contrasts ( Álvarez-Campos et al 2019 ). The first contrast of focus is between autozooids and their derived homologs, and the remaining three contrasts between two developmental stages of our three zooids of interest, the avicularia (autozooid buds, mature autozooids, avicularium buds, and mature avicularia), autozooids (autozooids buds and mature autozooids), avicularia (avicularium buds and mature avicularia), and rhizoids (rhizoid stolons and rhizoid autozooids).…”