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

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 wholegenome 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.

The Role of Transposable Elements in Speciation

“…Horizontal gene transfer regularly acts as a genetic bridge between vastly diverged species [ 257 , 258 ]. Horizontal transfers of TEs between angiosperm genomes have been documented in nature [ 263 , 264 , 265 ] and experimentally [ 266 ]. In Drosophila , HGT seems to have occurred from the willistoni species group to D. melanogaster .…”

Significance of introgression hybridization for extension of genetic variability in recipient genome

“…However, in a later work performed with the same material [32] it is stated with absolute certainty that the introgression lines originated from the incongruent crossing of two types of rice arose exclusively under the influence of pollen that did not incorporate DNA into the genome of the lines. In this study, the activation of transposons was confirmed.…”

“…Numerous studies on the expression of alien genes against the background of the resident genome have shown that a change in the expression of such a gene is quite common and is a consequence of the interaction between the alien gene and the genetic environment of the host genome [32,[37][38][39][40]. For wheat, the attenuation of resistance was repeatedly shown when a resistance gene was transferred from an alien species to the background of the wheat genome [9,[40][41][42][43]45].…”

In silico analysis of disease resistance and defence-related genes for a major sheath blight qShb 9-2 QTL in rice

“…For example, TE excision or insertion resulted in heritable altered expression of eight neighbouring genes in X9 rice line with four being significantly induced and four suppressed. Particularly, three of the induced genes were found within QTLs related to 1000 seed weight and grain length (Wu et al, 2015).…”