Abstract
Previous studies have shown that telomeric P elements inserted at the left end of the X chromosome are anchors of the P cytotype, the maternally inherited state that regulates P-element activity in the germ line of Drosophila melanogaster. This regulation is mediated by small RNAs that associate with the Piwi family of proteins (piRNAs). We extend the analysis of cytotype regulation by studying new combinations of telomeric and nontelomeric P elements (TPs and non-TPs). TPs interact with each other to enhance cytotype regulation. This synergism involves a strictly maternal effect, called presetting, which is apparently mediated by piRNAs transmitted through the egg. Presetting by a maternal TP can elicit regulation by an inactive paternally inherited TP, possibly by stimulating its production of primary piRNAs. When one TP has come from a stock heterozygous for a mutation in the aubergine, piwi, or Suppressor of variegation 205 genes, the synergism between two TPs is impaired. TPs also interact with non-TPs to enhance cytotype regulation, even though the non-TPs lack regulatory ability on their own. Non-TPs are not susceptible to presetting by a TP, nor is a TP susceptible to presetting by a non-TP. The synergism between TPs and non-TPs is stronger when the TP was inherited maternally. This synergism may be due to the accumulation of secondary piRNAs created by ping-pong cycling between primary piRNAs from the TPs and mRNAs from the non-TPs. Maternal transmission of P-element piRNAs plays an important role in the maintenance of strong cytotype regulation over generations.
Highlights
Previous studies have shown that telomeric P elements inserted at the left end of the X chromosome are anchors of the P cytotype, the maternally inherited state that regulates P-element activity in the germ line of Drosophila melanogaster
In crosses that segregated different genotypes, the daughters with the TP and those without it were scored separately, but because there were no differences between them, the results have been pooled. a In cross A, TP/TP females were mated to wild-type males from the M strain Samarkand (Sam), which is devoid of P elements, to produce TP/+ heterozygotes. b In cross B, TP males were mated to wild-type females from the M strain Samarkand to produce +/TP heterozygotes. c Unweighted average percentage gonadal dysgenesis (GD) 6 SE. d TP5 and TP6 are tightly linked to a null allele of the w locus. e NA is tightly linked to the wsp allele of the w locus
Do two TPs interact synergistically to bring about strong cytotype regulation? Can a TP interact with or preset a TP that has a different DNA sequence? Is synergism between two TPs sensitive to mutational depletion of the proteins heterochromatin protein 1 (HP1), Piwi, or Aub [a cytoplasmic member of the Piwi family encoded by the aubergine gene]? How does synergism between TPs and non-TPs compare to synergism between TPs? Can a TP preset a non-TP, and can a non-TP preset a TP? To answer these questions, we focus on one aspect of dysgenesis, the temperature-sensitive sterility seen in the offspring of crosses between M females and P males
Summary
Previous studies have shown that telomeric P elements inserted at the left end of the X chromosome are anchors of the P cytotype, the maternally inherited state that regulates P-element activity in the germ line of Drosophila melanogaster This regulation is mediated by small RNAs that associate with the Piwi family of proteins (piRNAs). P elements are mobilized by a transposase encoded by structurally complete members of the P family (Karess and Rubin 1984) Their activity is normally restricted to the germ line, where it causes hybrid dysgenesis, a syndrome of abnormalities that includes temperature-sensitive sterility and high frequencies of mutation and chromosome breakage (Kidwell et al 1977). In crosses that segregated different genotypes, the daughters with the TP and those without it were scored separately, but because there were no differences between them, the results have been pooled. a In cross A, TP/TP females were mated to wild-type males from the M strain Samarkand (Sam), which is devoid of P elements, to produce TP/+ heterozygotes. b In cross B, TP males were mated to wild-type females from the M strain Samarkand to produce +/TP heterozygotes. c Unweighted average percentage GD 6 SE. d TP5 and TP6 are tightly linked to a null allele of the w locus. e NA is tightly linked to the wsp allele of the w locus
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