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

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Abstract

Transposable elements (TEs) are major components of eukaryotic genomes and have played important roles in genome evolution. Plant introgressive hybridization is widespread in nature and may induce a wide range of genetic and epigenetic variations including reactivation of dormant TEs. Newly elicited TE transpositions may lead to heritable expression alteration in genes adjacent to excision and insertion sites and consequently to phenotypic novelty. Prior studies showed that distant hybridization between sexually incompatible plant species might cause reactivation of TEs. However, these studies used plants with confirmed alien genetic introgression, so it remains unclear whether the cause of TE activation is introgression or the alien pollination process itself. We pollinated rice stigma (Oryza sativa L., cv. Jijing88) with Zizania latifolia pollen. Immediate offspring and subsequent generations were self-fertilized. We conducted whole-genome resequencing on a derivative line that showed heritable phenotypic variations in plant height and grain characteristics. No genetic introgression from the pollen donor was observed, but transpositional reactivation of otherwise quiescent rice endogenous TEs was detected. In total, 33 de novo mobilization events occurred involving 13 TEs, namely a MITE mPing, Pong (the transposase-donor of mPing), and 11 LTR retrotransposons. Transpositions were verified by locus-specific polymerase chain reaction amplification and Southern analysis. Gene expression analysis suggested that at least some of the mobilized TEs caused heritable expression changes in neighboring genes, including genes that mapped to quantitative trait loci (QTLs) associated with grain weight and size. Thus, pollination by Zizania without entailing introgression can induce mobilization of endogenous TEs and cause heritable gene expression alterations. Our results suggest that pollination by related but sexually incompatible species may generate genetic and phenotypic novelty via modifications induced by enhanced mobility of TEs.

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Acknowledgments

This work was supported by the State Key Basic Research and Development Plan of China (2011CB100205, 2013CBA01404), National Natural Science Foundation of China (No. 30970232 & 31170208), Morden Seed Industry Development Special Fund and the Programme for Introducing Talents to Universities (B07017), and Graduate Student Innovation Fund (12SSXT130).

Author Contributions

XYL and YZD conceived and designed the experiments. WY, JTT, SS, WJ, WZH, ZD, LN, XCM, and LXY performed the experiments. BL contributed reagents/materials/analysis tools. WY, SY, and YZD wrote the paper.

Conflict of Interests

The authors have declared that no competing interests exist.

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Authors and Affiliations

  1. Jilin Academy of Agricultural Sciences, Changchun, 130032, China

    Ying Wu, Guizhen Guo, Jinming Wang & Xiuyun Lin

  2. Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE), Northeast Normal University, Changchun, 130024, China

    Ying Wu, Tingting Jiang, Yue Sun, Zeyang Wang, Shuai Sun, Jie Wang, Ning Li, Zhenhui Wang, Di Zhang, Yan Bai, Yang Gao, Bao Liu & Yuzhu Dong

  3. Faculty of Agronomy, Jilin Agricultural University, Changchun, 130118, China

    Zhenhui Wang

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  1. Ying Wu
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Correspondence to Xiuyun Lin or Yuzhu Dong.

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Ying Wu, Tingting Jiang, and Yue Sun contributed equally to this work.

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Table S1

Primers used for locus-specific PCR amplification. (DOC 38 kb)

Table S2

Primers used to generate probes for Southern analysis. (DOC 32 kb)

Table S3

Primers used for qRT-PCR analysis. (DOC 35 kb)

Table S4

Positioning of TE insertion and excision. (DOC 72 kb)

Table S5

Primers used to amplify fragments of SSR and the chromosomal information. (DOC 162 kb)

Table S6

AFLP adapters/primers list. (DOC 45 kb)

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Wu, Y., Jiang, T., Sun, Y. et al. Mobilization of Diverse Transposable Elements in Rice Induced by Alien Pollination Without Entailing Genetic Introgression. Plant Mol Biol Rep 33, 1181–1191 (2015). https://doi.org/10.1007/s11105-014-0819-9

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