The C. elegans heterochronic gene lin-28 coordinates the timing of hypodermal and somatic gonadal programs for hermaphrodite reproductive system morphogenesis

Development. 2019 Mar 7;146(5):dev164293. doi: 10.1242/dev.164293.

Abstract

C. elegans heterochronic genes determine the timing of expression of specific cell fates in particular stages of developing larvae. However, their broader roles in coordinating developmental events across diverse tissues have been less well investigated. Here, we show that loss of lin-28, a central heterochronic regulator of hypodermal development, causes reduced fertility associated with abnormal somatic gonadal morphology. In particular, the abnormal spermatheca-uterine valve morphology of lin-28(lf) hermaphrodites traps embryos in the spermatheca, which disrupts ovulation and causes embryonic lethality. The same genes that act downstream of lin-28 in the regulation of hypodermal developmental timing also act downstream of lin-28 in somatic gonadal morphogenesis and fertility. Importantly, we find that hypodermal expression, but not somatic gonadal expression, of lin-28 is sufficient for restoring normal somatic gonadal morphology in lin-28(lf) mutants. We propose that the abnormal somatic gonadal morphogenesis of lin-28(lf) hermaphrodites results from temporal discoordination between the accelerated hypodermal development and normally timed somatic gonadal development. Thus, our findings exemplify how a cell-intrinsic developmental timing program can also control proper development of other interacting tissues, presumably by cell non-autonomous signal(s). This article has an associated 'The people behind the papers' interview.

Keywords: Heterochronic pathway; Lin-28; Morphogenesis; Reproductive system; Somatic gonad.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / physiology*
  • Cell Differentiation
  • Cell Movement
  • Female
  • Fertilization
  • Gene Expression Regulation, Developmental
  • Gonads / physiology*
  • Green Fluorescent Proteins / physiology
  • Male
  • Morphogenesis*
  • Mutation
  • Ovulation
  • Plasmids
  • RNA Interference
  • RNA-Binding Proteins / physiology
  • Repressor Proteins / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • LIN-28 protein, C elegans
  • RNA-Binding Proteins
  • Repressor Proteins
  • Green Fluorescent Proteins