Soma-germ line interactions and a role for muscle in the regulation of C. elegans sperm motility

Abstract

The development of highly differentiated sperm cells that are specialized for navigating to and fusing with an oocyte is essential for sexual reproduction. As a major part of differentiation, sperm undergo extensive post-meiotic maturation en route to the oocyte. This is regulated largely by soma-derived cues. In Caenorhabditis elegans, this process is called sperm activation, and it transforms immotile spermatids into migratory fertilization-competent cells. Here, we show that the negative regulator of sperm activation, SWM-1, is produced in an unexpected cell type: body wall muscle. SWM-1 is secreted into the body cavity and enters the gonad; there, it is present with its likely target, TRY-5, a spermiogenesis activator. We show that, in addition to SWM-1, the somatic gonad and body fluid can exchange other factors, suggesting that soma-germ line transfer could affect other reproductive processes. In addition, we show that SWM-1 may have a separate role in the sperm migratory environment, to which it is contributed by both males and hermaphrodites. These findings reveal that late stages in gamete differentiation can be regulated at the wholeorganism level by broadly secreted factors. This article has an associated 'The people behind the papers' interview.

Loss of flavin adenine dinucleotide (FAD) impairs sperm function and male reproductive advantage inC. elegans

“…Our data support a cell autonomous role for proline catabolism in sperm. However, although whole animal RNAi of alh-6 closely phenocopies the alh-6 mutant including reduced spermatid size, germline specific RNAi of alh-6 did not significantly reduce the size of spermatids; perhaps suggesting a partial role for ALH-6 in somatic tissues for spermatid development, which is in line with recent studies in C. elegans describing soma to germline signaling in sperm activation (Chavez, Snow, Smith, & Stanfield). Intriguingly, the impact of loss of alh-6 is mostly independent of diet source, unlike the somatic phenotypes which are diet-dependent (Pang & Curran).…”

Reproduction disrupts stem cell homeostasis in testes of aged male Drosophila via an induced microenvironment

“…Many studies have revealed cross talk between germ cells and somatic cells in the modulation of reproduction and aging, such as the regulation of germ cell division and differentiation by somatic cells, and modulation of organismal longevity, stress resistance, and trans-generational inheritance of survival advantages through germ cells [6, 38, 85–88]. We found that reproduction blocks future gamete production by signals from smooth muscles, revealing a somatic cell-mediated mechanism in negative feedback control of reproduction.…”

Two isoforms of the essentialC. elegansArgonaute CSR-1 differentially regulate sperm and oocyte fertility

“…This suggests that the sperm genes could also be expressed and targeted by sRNAs in somatic tissues. The link between these tissues and its role in spermatogenesis (Chavez et al, 2018) will be intriguing to explore in the future.…”