Comprehensive transposon insertion profiling unravels the asexual breeding history of sweet orange cultivars

Authors: WU, BO - Clemson University; CUI, YIPING - Clemson University; Duan, Yong Ping; GMITTER, FRED - University Of Florida; LUO, FENG - Clemson University

Submitted to: Plant Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/3/2025
Publication Date: 6/6/2025
Citation: Wu, B., Cui, Y., Duan, Y., Gmitter, F., Luo, F. Comprehensive transposon insertion profiling unravels the asexual breeding history of sweet orange cultivars. Plant Communications. 2025. https://doi.org/10.1016/j.xplc.2025.101409.
DOI: https://doi.org/10.1016/j.xplc.2025.101409

Interpretive Summary: Inter-specific hybridizations between pummelo (Citrus maxima) and mandarin (Citrus reticulata) created the original sweet orange (Citrus × sinensis , SWO), but when and where have yet to be discovered. SWO has been propagated asexually through apomixis and grafting, and somatic mutations from the original plant gave rise to its diversified cultivars, and has yielded the largest number of bud sport selections in Citrus with diverse horticultural traits. In this study, we completely survey the Transposable element (TE) activities and identify six highly active TE families in SWO. We further examine the contribution of active TE families to the SWO bud sport diversity and evaluation, as well as the relationship between artificial selections and TE activities in SWO. Our research reveals that TE insertions are present as tag mutations for all SWO cultivar groups and are significantly enriched in affecting horticultural traits. Our results show that the high bud sport selection frequency of SWO could be explained by the activation of boosted TE families in SWO. On the other hand, TEs are much more controllable in promoting mutation rates and less harmful in the long term since many organisms, such as SWO have developed epigenetic mechanisms to silence the transposons.

Technical Abstract: Sweet orange (SWO) has multiple asexually propagated lineages that have been under artificial selections for centuries and the most bud sports selected in Citrus. The impact of artificial selections on SWO’s mutation rates and the reason for its high bud sport frequency are unknown. Here, we find six transposon families with up to 12,706.2-fold higher transposition activity in SWO compared to its two parental species (pumelo and mandarin). These six boosted families have contributed to 98.0% SWO-specific transposon insertions and produced tag insertions (with universal and exclusive presence) for all analyzed cultivar groups and almost all cultivars. Based on the insertion phylogenetic tree, we have recovered three major spread events in SWO cultivation history and dated modern SWOs back to a common ancestor around 500 years ago. The formation of all analyzed SWO cultivar groups involves activating at least one boosted transposon family. During the repeated selection of SWO lineages, transpositions have been accelerated. Noticeably, the transposition of active DNA TE families increased several fold within decades in a few SWO lineages. Transposons function as accelerators in the asexual breeding of SWO. Meanwhile, we have also observed the silencing of transpositions of three TE families after cultivar group formation. The controllable activity of transposons suggests they may play an important role in adjusting mutation rates in evolution.