A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans

Hannah S. Seidel, Michael Ailion, Jialing Li, Alexander van Oudenaarden, Matthew V. Rockman, Leonid Kruglyak

Research output: Contribution to journalArticle

Abstract

The evolutionary fate of an allele ordinarily depends on its contribution to host fitness. Occasionally, however, genetic elements arise that are able to gain a transmission advantage while simultaneously imposing a fitness cost on their hosts. We previously discovered one such element in C. elegans that gains a transmission advantage through a combination of paternal-effect killing and zygotic self-rescue. Here we demonstrate that this element is composed of a sperm-delivered toxin, peel-1, and an embryo-expressed antidote, zeel-1. peel-1 and zeel-1 are located adjacent to one another in the genome and co-occur in an insertion/deletion polymorphism. peel-1 encodes a novel four-pass transmembrane protein that is expressed in sperm and delivered to the embryo via specialized, sperm-specific vesicles. In the absence of zeel-1, sperm-delivered PEEL-1 causes lethal defects in muscle and epidermal tissue at the 2-fold stage of embryogenesis. zeel-1 is expressed transiently in the embryo and encodes a novel six-pass transmembrane domain fused to a domain with sequence similarity to zyg-11, a substrate-recognition subunit of an E3 ubiquitin ligase. zeel-1 appears to have arisen recently, during an expansion of the zyg-11 family, and the transmembrane domain of zeel-1 is required and partially sufficient for antidote activity. Although PEEL-1 and ZEEL-1 normally function in embryos, these proteins can act at other stages as well. When expressed ectopically in adults, PEEL-1 kills a variety of cell types, and ectopic expression of ZEEL-1 rescues these effects. Our results demonstrate that the tight physical linkage between two novel transmembrane proteins has facilitated their co-evolution into an element capable of promoting its own transmission to the detriment of organisms carrying it.

Original languageEnglish (US)
Article numbere1001115
JournalPLoS Biology
Volume9
Issue number7
DOIs
StatePublished - Jul 2011

Fingerprint

Spermatozoa
Antidotes
embryo (animal)
toxins
Embryonic Structures
spermatozoa
antidotes
transmembrane proteins
Proteins
Ubiquitin-Protein Ligases
paternal effect
Polymorphism
ubiquitin-protein ligase
Muscle
coevolution
Genes
lethal genes
Tissue
Embryonic Development
linkage (genetics)

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans. / Seidel, Hannah S.; Ailion, Michael; Li, Jialing; van Oudenaarden, Alexander; Rockman, Matthew V.; Kruglyak, Leonid.

In: PLoS Biology, Vol. 9, No. 7, e1001115, 07.2011.

Research output: Contribution to journalArticle

Seidel, Hannah S. ; Ailion, Michael ; Li, Jialing ; van Oudenaarden, Alexander ; Rockman, Matthew V. ; Kruglyak, Leonid. / A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans. In: PLoS Biology. 2011 ; Vol. 9, No. 7.
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