ROSINA (RSI) is part of a CACTA transposable element, TamRSI, and links flower development to transposon activity

Abstract

ROSINA (RSI) was isolated as a DNA binding factor able to bind to the CArG-box present in the promoter of the MADS-box gene DEFICIENS of Antirrhinum majus. The mosaic nature of RSI and its multi-copy presence in the A. majus genome indicated that RSI could be a part of a mobile genetic element. Here we show that RSI is a part of a CACTA transposable element system of A. majus, named TamRSI, which has evolved and is still evolving within the terminal inverted repeats (TIRs) of this CACTA transposon. Interestingly, RSI is always found in opposite orientation with respect to the transcription of a second gene present within the CACTA transposon, which encodes a putative TRANSPOSASE (TNP). This structural conWguration has not yet been described for any member of the CACTA transposons superfamily. Internal deletion derivatives of the TamRSI produce aberrant RSI transcripts (RSIATs) that carry parts of the RSI RNA fused to parts of the TNP RNA. In addition, an intriguing seed phenotype shown by RNAi transgenic lines generated to silence RSI, relate TamRSI to epigenetic mechanisms and associate the control of Xower development to transposon activity.

A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus

“…Furthermore, in Antirrhinum, Roccaro et al (2005) reported that the binding factor ROSINA (RSI) can bind the promoter of the MADSbox DEFICIENS gene involved in petal and stamen identity. The genomic organization of several RSI copies proved that this DNA binding factor is a part of a CACTA TE (Roccaro et al 2007). …”

Transposons and Gene Creation

“…Both DNA and RNA elements possess the ability to acquire host genomic sequences and move them to new locations, although they do it by altogether different mechanisms. The DNA elements include MULEs (Mutator-like elements) from maize (Talbert and Chandler, 1988), rice (Jiang et al, 2004), Lotus (Jiang et al, 2004), and melon (van Leeuwen et al, 2007), CACTA elements from Sorghum (Paterson et al, 2009;Wicker et al, 2011), Japanese morning glory (Kawasaki and Nitasaka, 2004), Antirrhinum (Roccaro et al, 2007), and soybean (Zabala and Vodkin, 2007) and Helitron elements from maize (Lal et al, 2003;Lai et al, 2005;Morgante et al, 2005) and Sorghum (Paterson et al, 2009). Peculiarly, and for an as yet unknown reason, some elements in some species, such as the rice MULEs-referred to as PackMULEs (Jiang et al, 2004) or Anacondas (Ohtsu et al, 2005)-the maize Helitrons (Du et al, 2009;Yang and Bennetzen, 2009), and the Sorghum CACTA elements (Paterson et al, 2009) have been highly successful at capturing sequences from multiple genes.…”

“…In Antirrhinum majus (snapdragon), the product of the ROSINA (RSI) gene binds upstream of MADS box genes essential for proper development of flower petals and stamens, as well as proper seed morphology and dispersal (Roccaro et al, 2005). The RSI gene is multicopy, and sequence analysis revealed it to be part of a CACTA family transposon, dubbed TamRSI, that also encodes a TPase (Figure 8.2A) (Roccaro et al, 2007). RSI is the product of a second gene that is transcribed inward from the transposon end, in opposite direction to the TPase gene.…”

“…Of particular interest is that the spontaneous internal deletions that this element goes through have a special effect on its convergently transcribed genes. For TamRSI, such deletions can create novel genes that result in part of the TPase gene, now fused to the 3 end of the RSI gene, being transcribed as antisense RNA; these RNAs are involved in epigenetically silencing TamRSI activity (Roccaro et al, 2007). Likewise, antisense transcripts of RSI that come from the TPase promoter may play a role in the down-regulation of RSI expression in carpels.…”

Stable Transcription Activities Dependent on an Orientation of Tam3 Transposon Insertions intoAntirrhinumand Yeast Promoters Occur Only within Chromatin

“…If TEs have contributed to adaptive evolution with their host plant genomes, the elements should be advantageous to the host irrespective of the induction of mutations (Dooner and Weil, 2007). In fact, substantial evidence has demonstrated that plant TPase genes have turned into new genes for essential functions in their host plants (Bundock and Hooykaas, 2005;Lin et al, 2007;Roccaro et al, 2007). In another aspect, TEs have been occasionally found in the regions proximal to genes, and Jordan et al (2003) provided substantial evidence that 25% of the promoter regions analyzed in the human genome contain TE-derived sequences.…”