Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus

Eigo Fukai; Manabu Yoshikawa; Niraj Shah; Niels Sandal; Akio Miyao; Seijiro Ono; Hideki Hirakawa; Turgut Yigit Akyol; Yosuke Umehara; Ken-Ichi Nonomura; Jens Stougaard; Hirohiko Hirochika; Makoto Hayashi; Shusei Sato; Stig Uggerhøj Andersen; Keiichi Okazaki

doi:10.1111/tpj.15896

Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus

Eigo Fukai^*, Manabu Yoshikawa, Niraj Shah, Niels Sandal, Akio Miyao, Seijiro Ono, Hideki Hirakawa, Turgut Yigit Akyol, Yosuke Umehara, Ken-Ichi Nonomura, Jens Stougaard, Hirohiko Hirochika, Makoto Hayashi, Shusei Sato, Stig Uggerhøj Andersen, Keiichi Okazaki

^*Corresponding author for this work

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4 Citations (Scopus)

Abstract

Transposable elements (TEs) constitute a large proportion of genomes of multicellular eukaryotes including flowering plants. TEs are normally maintained in a silenced state and their transpositions rarely occur. Hybridization between distant species has been regarded as a "shock" that stimulates genome re-organization, including TE mobilization. However, whether crosses between genetically close parents that result in viable and fertile offspring can induce TE transpositions has remained obscure. Here, we investigated the activation of long terminal repeat (LTR) retrotransposons in three Lotus japonicus recombinant inbred line (RIL) populations. We found that at least six LTR retrotransposon families were activated and transposed in 78% of the investigated RILs. LORE1a, one of the transposed LTR retrotransposons, showed transgenerational epigenetic activation, indicating the long-term effects of epigenetic instability induced by hybridization. Our study highlights TE activation as unexpectedly common events in plant reproduction.

Original language	English
Journal	The Plant Journal
Volume	111
Issue	5
Pages (from-to)	1397-1410
Number of pages	14
ISSN	0960-7412
DOIs	https://doi.org/10.1111/tpj.15896
Publication status	Published - Sept 2022

Keywords

Lotus japonicus
epigenetics
hybridization
long terminal repeat (LTR) retrotransposons
pollen
recombinant inbred line (RIL) population
sexual reproduction
transposable elements (TEs)

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10.1111/tpj.15896

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Fukai, E., Yoshikawa, M., Shah, N., Sandal, N., Miyao, A., Ono, S., Hirakawa, H., Akyol, T. Y., Umehara, Y., Nonomura, K.-I., Stougaard, J., Hirochika, H., Hayashi, M., Sato, S., Andersen, S. U., & Okazaki, K. (2022). Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus. The Plant Journal, 111(5), 1397-1410. https://doi.org/10.1111/tpj.15896

@article{68627483556e4e9c8afa8e4a74ccaa62,

title = "Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus",

abstract = "Transposable elements (TEs) constitute a large proportion of genomes of multicellular eukaryotes including flowering plants. TEs are normally maintained in a silenced state and their transpositions rarely occur. Hybridization between distant species has been regarded as a {"}shock{"} that stimulates genome re-organization, including TE mobilization. However, whether crosses between genetically close parents that result in viable and fertile offspring can induce TE transpositions has remained obscure. Here, we investigated the activation of long terminal repeat (LTR) retrotransposons in three Lotus japonicus recombinant inbred line (RIL) populations. We found that at least six LTR retrotransposon families were activated and transposed in 78% of the investigated RILs. LORE1a, one of the transposed LTR retrotransposons, showed transgenerational epigenetic activation, indicating the long-term effects of epigenetic instability induced by hybridization. Our study highlights TE activation as unexpectedly common events in plant reproduction.",

keywords = "Lotus japonicus, epigenetics, hybridization, long terminal repeat (LTR) retrotransposons, pollen, recombinant inbred line (RIL) population, sexual reproduction, transposable elements (TEs)",

author = "Eigo Fukai and Manabu Yoshikawa and Niraj Shah and Niels Sandal and Akio Miyao and Seijiro Ono and Hideki Hirakawa and Akyol, {Turgut Yigit} and Yosuke Umehara and Ken-Ichi Nonomura and Jens Stougaard and Hirohiko Hirochika and Makoto Hayashi and Shusei Sato and Andersen, {Stig Uggerh{\o}j} and Keiichi Okazaki",

year = "2022",

month = sep,

doi = "10.1111/tpj.15896",

language = "English",

volume = "111",

pages = "1397--1410",

journal = "The Plant Journal",

issn = "0960-7412",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "5",

}

Fukai, E, Yoshikawa, M, Shah, N, Sandal, N, Miyao, A, Ono, S, Hirakawa, H, Akyol, TY, Umehara, Y, Nonomura, K-I, Stougaard, J, Hirochika, H, Hayashi, M, Sato, S, Andersen, SU & Okazaki, K 2022, 'Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus', The Plant Journal, vol. 111, no. 5, pp. 1397-1410. https://doi.org/10.1111/tpj.15896

Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus. / Fukai, Eigo; Yoshikawa, Manabu; Shah, Niraj et al.
In: The Plant Journal, Vol. 111, No. 5, 09.2022, p. 1397-1410.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus

AU - Fukai, Eigo

AU - Yoshikawa, Manabu

AU - Shah, Niraj

AU - Sandal, Niels

AU - Miyao, Akio

AU - Ono, Seijiro

AU - Hirakawa, Hideki

AU - Akyol, Turgut Yigit

AU - Umehara, Yosuke

AU - Nonomura, Ken-Ichi

AU - Stougaard, Jens

AU - Hirochika, Hirohiko

AU - Hayashi, Makoto

AU - Sato, Shusei

AU - Andersen, Stig Uggerhøj

AU - Okazaki, Keiichi

PY - 2022/9

Y1 - 2022/9

N2 - Transposable elements (TEs) constitute a large proportion of genomes of multicellular eukaryotes including flowering plants. TEs are normally maintained in a silenced state and their transpositions rarely occur. Hybridization between distant species has been regarded as a "shock" that stimulates genome re-organization, including TE mobilization. However, whether crosses between genetically close parents that result in viable and fertile offspring can induce TE transpositions has remained obscure. Here, we investigated the activation of long terminal repeat (LTR) retrotransposons in three Lotus japonicus recombinant inbred line (RIL) populations. We found that at least six LTR retrotransposon families were activated and transposed in 78% of the investigated RILs. LORE1a, one of the transposed LTR retrotransposons, showed transgenerational epigenetic activation, indicating the long-term effects of epigenetic instability induced by hybridization. Our study highlights TE activation as unexpectedly common events in plant reproduction.

AB - Transposable elements (TEs) constitute a large proportion of genomes of multicellular eukaryotes including flowering plants. TEs are normally maintained in a silenced state and their transpositions rarely occur. Hybridization between distant species has been regarded as a "shock" that stimulates genome re-organization, including TE mobilization. However, whether crosses between genetically close parents that result in viable and fertile offspring can induce TE transpositions has remained obscure. Here, we investigated the activation of long terminal repeat (LTR) retrotransposons in three Lotus japonicus recombinant inbred line (RIL) populations. We found that at least six LTR retrotransposon families were activated and transposed in 78% of the investigated RILs. LORE1a, one of the transposed LTR retrotransposons, showed transgenerational epigenetic activation, indicating the long-term effects of epigenetic instability induced by hybridization. Our study highlights TE activation as unexpectedly common events in plant reproduction.

KW - Lotus japonicus

KW - epigenetics

KW - hybridization

KW - long terminal repeat (LTR) retrotransposons

KW - pollen

KW - recombinant inbred line (RIL) population

KW - sexual reproduction

KW - transposable elements (TEs)

UR - http://www.scopus.com/inward/record.url?scp=85135101396&partnerID=8YFLogxK

U2 - 10.1111/tpj.15896

DO - 10.1111/tpj.15896

M3 - Journal article

C2 - 35792830

SN - 0960-7412

VL - 111

SP - 1397

EP - 1410

JO - The Plant Journal

JF - The Plant Journal

IS - 5

ER -

Widespread and transgenerational retrotransposon activation in inter- and intra-species recombinant inbred populations of Lotus japonicus

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