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

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 quies...

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Autores principales: Teramoto, Shota, Tsukiyama, Takuji, Okumoto, Yutaka, Tanisaka, Takatoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4055405/
https://www.ncbi.nlm.nih.gov/pubmed/24921928
http://dx.doi.org/10.1371/journal.pgen.1004396
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author Teramoto, Shota
Tsukiyama, Takuji
Okumoto, Yutaka
Tanisaka, Takatoshi
author_facet Teramoto, Shota
Tsukiyama, Takuji
Okumoto, Yutaka
Tanisaka, Takatoshi
author_sort Teramoto, Shota
collection PubMed
description 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.
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spelling pubmed-40554052014-06-18 Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing Teramoto, Shota Tsukiyama, Takuji Okumoto, Yutaka Tanisaka, Takatoshi PLoS Genet Research Article 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. Public Library of Science 2014-06-12 /pmc/articles/PMC4055405/ /pubmed/24921928 http://dx.doi.org/10.1371/journal.pgen.1004396 Text en © 2014 Teramoto et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Teramoto, Shota
Tsukiyama, Takuji
Okumoto, Yutaka
Tanisaka, Takatoshi
Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title_full Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title_fullStr Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title_full_unstemmed Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title_short Early Embryogenesis-Specific Expression of the Rice Transposon Ping Enhances Amplification of the MITE mPing
title_sort early embryogenesis-specific expression of the rice transposon ping enhances amplification of the mite mping
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4055405/
https://www.ncbi.nlm.nih.gov/pubmed/24921928
http://dx.doi.org/10.1371/journal.pgen.1004396
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