A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera)

Snell, Terry W.; Kubanek, Julia; Carter, William; Payne, Audra B.; Kim, Jerry; Hicks, Melissa; Stelzer, Claus‐Peter

doi:10.1007/s00227-006-0251-2

Cited by 150 publications

(113 citation statements)

References 49 publications

Supporting

Mentioning

107

Contrasting

Unclassified

Order By: Relevance

“…N-terminal sequencing of 17 amino acids from the mixis-inducing protein established that this fragment was identical to a putative steroidogenesis-inducing protein reported from humans (11). This observation led to the hypothesis that steroid hormones may be involved in regulating sexual reproduction in B. manjavacas.…”

supporting

confidence: 51%

See 1 more Smart Citation

Conservation of progesterone hormone function in invertebrate reproduction

Stout¹,

Clair

Snell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

Steroids play fundamental roles regulating mammalian reproduction and development. Although sex steroids and their receptors are well characterized in vertebrates and several arthropod invertebrates, little is known about the hormones and receptors regulating reproduction in other invertebrate species. Evolutionary insights into ancient endocrine pathways can be gained by elucidating the hormones and receptors functioning in invertebrate reproduction. Using a combination of genomic analyses, receptor imaging, ligand identification, target elucidation, and exploration of function through receptor knockdown, we now show that comparable progesterone chemoreception exists in the invertebrate monogonont rotifer Brachionus manjavacas, suggesting an ancient origin of the signal transduction systems commonly associated with the development and integration of sexual behavior in mammals.receptor | imaging steroids S ex steroids and their receptors have been well studied in vertebrate animals, but much less is known about the mechanisms by which they regulate physiology and behavior in invertebrates (1). Recent gene sequencing, bioinformatics, and protein synthesis approaches suggested that modern nuclear steroid receptors evolved from an ancient receptor that arose 0.6-1.2 billion y ago, before a common bilateral ancestor diverged into the deuterostomes and protostomes (2). This ancient receptor is postulated to have been activated by estrogen, the terminal product in steroid biosynthesis, with intermediates progesterone and testosterone acquiring uses as hormones later in evolutionary history (3). The discovery of estrogen receptor homologs in mollusks (4) and annelids (5) indicated that Lophotrochozoan lineages have not lost this type of hormone chemoreception, despite the use of nonandrogen steroid hormones in Ecdysozoans (e.g., ecdysteroids in insects; dafachronic acids in Caenorhabditis elegans). Recently, an estrogen-like receptor was identified in C. elegans (6), supporting the hypothesis that steroid receptors are ancient and widespread. In addition, progesterone activates nonnuclear, membrane-associated receptors in vertebrates and invertebrates with impacts on behavior and reproduction (7). However, substantial gaps still remain in the phylogenetic distribution of sex steroid receptors in many invertebrates and their functions in sexual differentiation, development, reproduction, and behavior are unclear.The invertebrate monogonont rotifer Brachionus manjavacas belongs to the Lophotrochozoa, one of the three major animal clades whose origin predates the Cambrian period 543 million years ago (8). An essential attribute of monogonont rotifers is their ability to reproduce both asexually and sexually. Although this flexible reproductive strategy is central to their evolutionary success, little is known about how reproduction is regulated in rotifers or the molecules involved in reproductive signaling in most nonarthropod invertebrates (9).The switch from asexual to sexual reproduction in B. manjavacas is triggered ...

show abstract

supporting

confidence: 51%

“…We used Brachionus manjavacas (24) as test animals, a species originally collected from the Azov Sea (25), and formerly known as B. plicatilis Russian (11). This species has been cultured continuously in the laboratory since 1983, with periodic collection and storage of resting eggs.…”

Section: Methodsmentioning

confidence: 99%

Conservation of progesterone hormone function in invertebrate reproduction

Stout¹,

Clair

Snell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

show abstract

“…The hatched eggs usually develop into asexually reproducing amictic females (FA), until they encounter a mixis signal directing them to embark on sexual reproduction. The factors inducing the mixis signal in the Brachionus species complex are largely unknown, although population density, salinity, temperature, presence of pheromones and food availability were found to play a role (Lubzens et al, 1985;Lubzens & Zmora, 2003;Serra & King, 1999;Gilbert, 2004aGilbert, , 2007Hagiwara et al, 2005;Snell et al, 2006;Denekamp et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

The expression pattern of dormancy-associated genes in multiple life-history stages in the rotifer Brachionus plicatilis

et al. 2010

View full text Add to dashboard Cite

Rotifer resting eggs retain their viability for several decades in a non-desiccated form and are of interest in discerning the processes associated with dormancy, since in most organisms this phenomenon is linked with desiccation. The expression pattern of candidate genes with biological functions associated with dormancy in several other organisms was examined in rotifers. High-throughput transcriptome profiling revealed three patterns of gene expression in resting eggs: (1) relatively highly expressed genes coding for LEA proteins and putative paralogs of the small heat shock protein family (shsp); (2) genes coding for ferritin (ferr), glutathione-6-transferase (gts) and HSP70, where some of the putative gene paralogs of these families show relatively high expression levels and other putative paralogs show relatively low expression levels in resting eggs; and (3) genes with relatively low expression levels in resting eggs, for trehalose-6-phosphate synthase (tps), fatty-acid binding proteins (fab) and of lipoprotein lipase (lpl) and the aquaporins gene family (aqp). Changes in the expression pattern of some members of putative gene families occurred during the obligatory dormant period of resting eggs. A transition was observed from an expression pattern of diapausing embryos to an expression pattern of amictic females, during hatching. Differences were also found in the expression pattern in the different types of females, especially in those carrying resting eggs, and in males compared with females. These results suggest putative functional significance to genes associated with dormancy in non-desiccated resting eggs. It could also be proposed that their occurrence in resting eggs is developmentally programmed to facilitate survival in case of desiccation.

show abstract

“…For example, the body size increased with exposure to human chorionic gonadotropin, suggesting that rotifers may have receptors for this or a similar hormone. A 39 kD mixis-inducing protein (MIP) pheromone has been isolated from rotifer-conditioned medium which appeared to trigger sexual reproduction in B. plicatilis (Snell et al 2006) The first 17 amino acids of its N-terminus are identical to a steroidogenesis-inducing protein isolated from human ovarian follicular fluid. Rotifer MIP may play a similar role in steroidogenesis (Snell and DesRosiers 2008).…”

Section: Discussionmentioning

confidence: 99%