TY - JOUR
T1 - A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans
AU - Seidel, Hannah S.
AU - Ailion, Michael
AU - Li, Jialing
AU - van Oudenaarden, Alexander
AU - Rockman, Matthew V.
AU - Kruglyak, Leonid
N1 - Funding Information:
Foremost, we are very grateful to Michel Labouesse for his generous advice regarding the analysis of peel-1-affected embryos. We also thank Michael Brauchle for help with microscopy; Arjun Raj for providing the nuclei counting code; Joshua Bloom for help with phylogenetic analysis; Andy Singson, Steve L'Hernault, Christian Frøkjœr-Jensen, and Indrani Chatterjee for reagents and protocols; three anonymous reviewers for comments on the manuscript; and Marie-Anne Félix, Antoine Barrière, Elie Dolgin, Erik Andersen, the National Bioresource Project of Japan, and the Caenorhabditis Genetics Center, funded by the NIH National Center for Research Resources, for strains. MA thanks Erik Jorgensen for allowing him to work on this project in his laboratory.
PY - 2011/7
Y1 - 2011/7
N2 - 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.
AB - 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.
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U2 - 10.1371/journal.pbio.1001115
DO - 10.1371/journal.pbio.1001115
M3 - Article
C2 - 21814493
AN - SCOPUS:79960915775
SN - 1544-9173
VL - 9
JO - PLoS Biology
JF - PLoS Biology
IS - 7
M1 - e1001115
ER -