Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing

Abstract

Miniature inverted-repeat transposable elements (MITEs) are numerically predominant transposable elements in the rice genome, and their activities have influenced the evolution of genes. Very little is known about how MITEs can rapidly amplify to thousands in the genome. The rice MITE mPing is quiescent in most cultivars under natural growth conditions, although it is activated by various stresses, such as tissue culture, gamma-ray irradiation, and high hydrostatic pressure. Exceptionally in the temperate japonica rice strain EG4 (cultivar Gimbozu), mPing has reached over 1000 copies in the genome, and is amplifying owing to its active transposition even under natural growth conditions. Being the only active MITE, mPing in EG4 is an appropriate material to study how MITEs amplify in the genome. Here, we provide important findings regarding the transposition and amplification of mPing in EG4. Transposon display of mPing using various tissues of a single EG4 plant revealed that most de novo mPing insertions arise in embryogenesis during the period from 3 to 5 days after pollination (DAP), and a large majority of these insertions are transmissible to the next generation. Locus-specific PCR showed that mPing excisions and insertions arose at the same time (3 to 5 DAP). Moreover, expression analysis and in situ hybridization analysis revealed that Ping, an autonomous partner for mPing, was markedly up-regulated in the 3 DAP embryo of EG4, whereas such up-regulation of Ping was not observed in the mPing-inactive cultivar Nipponbare. These results demonstrate that the early embryogenesis-specific expression of Ping is responsible for the successful amplification of mPing in EG4. This study helps not only to elucidate the whole mechanism of mPing amplification but also to further understand the contribution of MITEs to genome evolution.

Loss of function mutations in the rice chromomethylase OsCMT3a cause a burst of transposition

“…With regards to mPing , upregulation of Ping in the ‘3 days after pollination (DAP)’ embryo is proposed to be responsible for the transposition of mPing in EG4 (Teramoto et al ., ). Whether Ping in oscmt3a is also upregulated in the 3 DAP embryo and thus contributes to the mobilization of mPing in oscmt3a would be a future topic of investigation.…”

Mobilization of Diverse Transposable Elements in Rice Induced by Alien Pollination Without Entailing Genetic Introgression

“…We can confidently rule out (i) as a casual factor based on the following evidences: (a) in our previous efforts to induce TE activity by various means (e.g., Lin et al 2006;Yang et al 2012), we did not observe activity of any of the TEs studied here in the rice cultivar. In fact, as documented by other studies (Naito et al 2009;Teramoto et al 2014), rice cultivars with intrinsic TE mobility under normal growing conditions are extremely rare and so far only one (Gimbozu) was identified. (b) As detailed in the "Materials and Methods" section, Jijing88 was a pure-line rice cultivar and plants used for the pollination experiment had been purposely selfed for several additional generations.…”

Two key events associated with a transposable element burst occurred during rice domestication

“…However, the mechanism by which Ping16A_Stow may initiate the burst is unknown and warrants further investigation. Prior studies indicated that increased Ping transcripts were correlated with more mPing transpositions in strains undergoing mPing bursts 4,22 . Our unpublished data suggests that Ping16A_Stow does not produce more transcripts compared to other Ping elements, suggesting that mechanisms other than an increased transcript level from this locus may be responsible.…”

“…The vast majority of strains with Ping16A have only one Ping (105/154 strains) and a moderate number of mPing elements (mean = 28). One of these strains is the reference strain Nipponbare where the inability to detect transposition of Ping or mPing was initially attributed to Ping silencing 22 . In fact, Ping is not silenced in Nipponbare nor in any other strain analyzed to date 4 .…”