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

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.