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Extensive changes in gene expression and alternative splicing due to homoeologous exchange in rice segmental allopolyploids

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Abstract

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We report rampant homoeologous exchanges in progenies of a newly synthesized rice segmental allotetraploid and demonstrate their consequences to changes of gene expression and alternative splicing.

Abstract

Allopolyploidization is recurrent across the tree of angiosperms and known as a driving evolutionary force in both plants and animals. A salient feature of allopolyploidization is the induction of homoeologous exchange (HE) events between the constituent subgenomes, which may in turn cause changes in gene expression, transcript alternative splicing, and phenotypic novelty. However, this issue has been poorly studied, largely because lack of a system in which the exact parentage donating the subgenomes is known and the HE events are occurring in real time. Here, we employed whole-genome re-sequencing and RNA-seq-based transcriptome profiling in four randomly chosen progeny individuals (at the 10th-selfed generation) of segmental allotetraploids that were constructed by colchicine-mediated whole-genome doubling of F1 hybrids between the two subspecies (japonica and indica) of Asian cultivated Oryza sativa. We show that rampant HE events occurred in these tetraploid individuals, which converted most of the otherwise heterozygous genomic regions into a homogenized state of one parental subgenome. We demonstrate that genes within these homogenized genomic regions in the tetraploids showed high frequencies of altered expression and enhanced alternative splicing relative to their counterparts in the corresponding diploid parents in the embryo tissue. Intriguingly, limited overlaps between the differentially expressed genes and the differential alternative spliced genes were identified, which were partitioned to distinctly enriched gene ontology terms. Together, our results indicate that HE is a major mechanism to rapidly generate novelty in gene expression and transcriptome diversity, which may facilitate phenotypic innovation in nascent allopolyploids and relevant to allopolyploid crop breeding.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31500176), the National Key Research and Development Program of China (2016YFD0101004), the Recruitment Program of Global Youth Experts, the Program of Changbai Mountain Scholar and the Program for Introducing Talents to Universities (B07017).

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  1. Zhibin Zhang and Tiansi Fu authors contributed equally to this work.

Authors and Affiliations

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

    Zhibin Zhang, Tiansi Fu, Zhijian Liu, Hongwei Xun, Guo Li, Baoxu Ding, Yuzhu Dong, Bao Liu, Ying Wu & Lei Gong

  2. Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA

    Xutong Wang

  3. Jilin Academy of Agricultural Sciences (JAAS), Changchun, 136100, China

    Xiuyun Lin

  4. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164, USA

    Karen A. Sanguinet

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  1. Zhibin Zhang
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Zhang, Z., Fu, T., Liu, Z. et al. Extensive changes in gene expression and alternative splicing due to homoeologous exchange in rice segmental allopolyploids. Theor Appl Genet 132, 2295–2308 (2019). https://doi.org/10.1007/s00122-019-03355-8

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