Academic journal article Genetics

The Activator/Dissociation Transposable Elements Comprise a Two-Component Gene Regulatory Switch That Controls Endogenous Gene Expression in Maize

Academic journal article Genetics

The Activator/Dissociation Transposable Elements Comprise a Two-Component Gene Regulatory Switch That Controls Endogenous Gene Expression in Maize

Article excerpt

ABSTRACT

The maize Activator/Dissociation (Ac/Ds) elements are able to replicate and transpose throughout the maize genome. Both elements preferentially insert into gene-rich regions altering the maize genome by creating unstable insertion alleles, stable derivative or excision alleles, or by altering the spatial or temporal regulation of gene expression. Here, we characterize an Ac insertion in the 5'-UTR of the Pink Scutellum1 (Ps1) gene and five Ds derivatives generated through abortive transposition events. Characterization of Ps1 transcription initiation sites in this allelic series revealed several that began within the terminus of the Ac and Ds elements. Transcripts originating within Ds or Ac accumulated to lower levels than the wild-type Ps1 allele, but were often sufficient to rescue the seedling lethal phenotype associated with severe loss-of-function alleles. Transcription initiation sites were similar in Ac and Ds derivatives, suggesting that Ac transposase does not influence transcript initiation site selection. However, we show that Ac transposase can negatively regulate Ps1 transcript accumulation in a subset of Ds-insertion alleles resulting in a severe mutant phenotype. The role of maize transposons in gene evolution is discussed.

THE maize hAT family members Activator/Dissociation (Ac/Ds) are composed of the autonomous Ac and nonautonomous Ds transposable elements (Kunze and Weil 2002). Ac is 4565 bp and encodes a 3.5-kb open reading frame (ORFa) that directs the synthesis of an 807-amino-acid-transposase (TPase) protein (Fedoroff et al. 1983; Kunze et al. 1987). The TPase transcript initiates at several sites within a 100-bp interval at the 5' end of the element and spans most of Ac (Kunze et al. 1987). The lack of canonical CAAT and TATA boxes in the promoter region may account for the multiple transcriptional initiation sites within Ac and the low levels of Ac transcript (Dynan 1986; Fusswinkel et al. 1991; Fridlender et al. 1998). Ac contains ~240 bp subterminal repeats and 11 bp terminal inverted repeats at each end. The subterminal repeat regions at both Ac ends contain TPase binding sites that are essential for TPase recognition and subsequent transposition of both Ac and Ds (Muller-Neumann et al. 1984; Pohlman et al. 1984a,b; Coupland et al. 1989; Kunze and Starlinger 1989).

Ds elements are structurally diverse but share the feature that they are capable of nonautonomous transposition (reviewed in Doring and Starlinger 1986; Kunze 1996). Most Ds elements arise from Ac internal deletions that ablate TPase activity. Some Ds elements, such as Ds9, are derived from simple internal deletions of Ac sequence (Pohlman et al. 1984b). More complex structures can also be generated when one Ds element inserts into or near another Ds element (Courage- Tebbe et al. 1983; Klein et al. 1988; Doring et al. 1989; Ralston et al. 1989; Dooner and Belachew 1991). These complex elements are capable of inducing chromosome breakage (English et al. 1995), a phenomenon first discovered by McClintock in 1946 (McClintock 1946; Doring et al. 1989). Ac and Ds are also capable of inducing large-scale structural rearrangements of the genome such as chromosome translocations, inversions, and deletions (Dooner and Belachew 1991; Zhang et al. 2009).

Ac and Ds element insertions can regulate andmodify flanking gene expression in a variety of ways (reviewed in Wessler 1988; Feschotte et al. 2002). Ac/Ds elements can alter the RNA splicing patterns (Simon and Starlinger 1987; Wessler et al. 1987; Grotewold et al. 1991) or affect the timing and tissue-specific accumulation of adjacent gene transcripts (Klein et al. 1988; Schiefelbein et al. 1988a; Sullivan et al. 1989; Dowe et al. 1990;Moreno et al. 1992). Vollbrecht et al. (2000) have also described a Ds-insertion allele of knotted1 that shows altered expressivity in the presence of Ac. The mutant phenotype is most enhanced (i.e., more knots on leaves) in the presence of Ac-st1, whereas in the absence of Ac, the mutant phenotype is relatively weak. …

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