Early embryogenesis-specific expression of the rice transposon Ping enhances amplification of the MITE mPing

PLoS Genet. 2014 Jun 12;10(6):e1004396. doi: 10.1371/journal.pgen.1004396. eCollection 2014 Jun.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA Copy Number Variations
  • DNA Transposable Elements / genetics*
  • Gene Amplification / genetics*
  • Gene Dosage / genetics*
  • Inverted Repeat Sequences / genetics
  • Oryza / embryology*
  • Oryza / genetics*
  • Polymorphism, Single Nucleotide

Substances

  • DNA Transposable Elements

Grants and funding

This work was supported by grants from the Ministry of Education, Culture, Sports, Science, and Technology of Japan in the form of Grants-in-Aid for Scientific Research (21380004 and 25292006). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.