Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants

First author: Zhenzhen Yang; Affiliations: The Pennsylvania State University (宾夕法尼亚州立大学): University Park, USA

Corresponding author: Claude W. dePamphilis

Horizontal gene transfer (HGT), the movement and genomic integration of DNA across species boundaries, is commonly associated with bacteria and other microorganisms, but functional HGT (fHGT) is increasingly being recognized in heterotrophic parasitic plants that obtain their nutrients and water from their host plants through direct haustorial feeding. Here, in the holoparasitic stem parasite Cuscuta, we identify 108  transcribed and probably functional HGT events in Cuscuta campestris and related species, plus 42  additional regions with host-derived transposon, pseudogene and non-coding sequences. Surprisingly, 18  Cuscuta fHGTs were acquired from the same gene families by independent HGT events in Orobanchaceae parasites, and the majority are highly expressed in the haustorial feeding structures in both lineages. Convergent retention and expression of HGT sequences suggests an adaptive role for specific additional genes in parasite biology. Between 16 and 20 of the transcribed HGT events are inferred as ancestral in Cuscuta based on transcriptome sequences from species across the phylogenetic range of the genus, implicating fHGT in the successful radiation of Cuscuta parasites. Genome sequencing of C. campestris supports transfer of genomic DNA—rather than retroprocessed RNA—as the mechanism of fHGT. Many of the C. campestris genes horizontally acquired are also frequent sources of 24-nucleotide small RNAs that are typically associated with RNA-directed DNA methylation. One HGT encoding a leucine-rich repeat protein kinase overlaps with a microRNA that has been shown to regulate host gene expression, suggesting that HGT-derived parasite small RNAs may function in the parasite–host interaction. This study enriches our understanding of HGT by describing a parasite–host system with unprecedented gene exchange that points to convergent evolution of HGT events and the functional importance of horizontally transferred coding and non-coding sequences.

水平基因转移是DNA跨越物种界限，在不同物种之间移动、整合的过程，通常与细菌及其它微生物关联在一起，但在异养寄生植物中人们逐渐了解了功能性水平基因转移，这些异养寄生植物通过吸器直接从寄主植物中吸收营养和水分。本文中，作者在全寄生生物菟丝子属植物平原菟丝子及其近缘种中鉴定到了108个转录的、可能属于功能性水平基因转移事件，另外还有42个区域是来自于寄主植物的转座子、假基因和非编码序列。有趣的是，其中18个水平转移基因来自于列当科寄主植物的同一个基因家族，且均为独立性水平基因转移事件，并且在两个不同的菟丝子支系中，这18个水平转移基因大多在吸器组织中高表达。趋同的保留和表达模式说明这些基因对于菟丝子的寄生生活具有重要的作用。作者通过对菟丝子属所有植物的转录组序列分析发现其中大概有16到20个水平转移基因比较古老，表明这些基因作用于菟丝子寄生植物的成功辐射。对于平原菟丝子的基因组测序发现相比于逆转录的RNA，基因组DNA更有可能是功能性基因水平转移的基础。许多平原菟丝子通过水平转移获取的基因属于24个核苷酸的小RNA，这些基因通常与RNA指导的DNA甲基化相关。其中一个水平转移基因编码一个亮氨酸富含重复蛋白激酶，与一个已知能够调控寄主基因表达的microRNA存在重叠，说明来自于寄主植物水平转移的小RNA可能会作用于寄生植物与寄主植物之间互作。本文的研究丰富了我们对于寄生植物与寄主植物之间基因水平转移的理解，发现了前所未见的水平基因转移事件趋同演化，突出了水平转移编码基因和非编码序列的功能重要性。

通讯：Claude W. dePamphilis (http://amborella.huck.psu.edu)

个人简介：佐治亚大学，博士。

研究方向：植物花的演化；寄生植物相关研究；叶绿体基因组及系统基因组演化。

doi: https://doi.org/10.1038/s41477-019-0458-0

Journal: Nature Plants

Published date: July 22, 2019