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

Nature Plants volume 5, pages 991–1001 (2019)Cite this article

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Abstract

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.

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Fig. 1: Identification and characterization of HGT genes and donors.
Fig. 2: Convergent evolution of expressed HGTs in two independent parasitic lineages.
Fig. 3: C. campestris HGT events are a frequent source of small RNAs.
Fig. 4: HGT is both ancestral and an ongoing process in Cuscuta.
Fig. 5: HGT pathways in light of interaction with mobile mRNAs and mobile small RNAs.

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Data availability

Publicly available data sources are as given in the Methods section of the manuscript. Web links for publicly available datasets are indicated in Supplementary Table 22. C. campestris genome assembly and annotations are available from http://ppgp.huck.psu.edu/cuscuta.html. The raw sequence reads for the eight Cuscuta taxa sampled in this study (Cuscuta species RNA sequencing datasets), C. campestris HGT sequences, all multiple sequence alignments and HGT tree files, as well as the supporting trees and alignments for selective constraint analyses (C. campestris HGT gene sequences, alignments and phylogenies), are given as supporting data at http://ppgp.huck.psu.edu/data/Cuscuta_HGT_Manuscript_Data/. All HGT sequences extracted from these assemblies are included as supporting data in the posted multiple sequence alignments and as described below. The raw data for Fig. 1a are in Supplementary Table 2 (column C); Fig. 1b in Supplementary Table 3; Fig. 1d in Supplementary Figs. 11 and 12; Fig. 2a,c,d in Supplementary Table 11; Fig. 2b on http://ppgp.huck.psu.edu/data/Cuscuta_HGT_Manuscript_Data/; Fig. 3a,b in Supplementary Tables 13 and 14; Fig. 3c in Supplementary Table 2; Fig. 3g on http://ppgp.huck.psu.edu/data/Cuscuta_HGT_Manuscript_Data/; Fig. 4 in Supplementary Table 15; and Fig. 5 in Supplementary Tables 2, 13 and 14.

Code availability

The customized code and pipeline associated with data analysis are available from https://github.com/dePamphilis/Cuscuta_HGT_ms_code.

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Acknowledgements

Sequence data are archived at National Center for Biotechnology Information BioProject ID SRP001053, and at http://ppgp.huck.psu.edu. This research was supported by award No. IOS-1238057 to J.H.W. and C.W.deP. from the NSF Plant Genome Research Program; No. 2018-05102 to M.J.A., J.H.W. and C.W.deP. from the United States Department of Agriculture, with additional support to Z.Y. from the Plant Biology and Biology Department graduate programmes at Penn State; and by the National Institute of Food and Agriculture Project (No. 131997) to J.H.W. The authors thank I. Ko for help with PCR experiments and E. Bellis, Y. Zheng and three anonymous reviewers for helpful comments and suggestions.

Author information

Author notes

  1. Zhenzhen Yang

    Present address: Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, China

  2. Gunjune Kim

    Present address: Future Technology Corporate R&D, Seoul, Republic of Korea

  3. Saima Shahid

    Present address: Donald Danforth Plant Science Center, St. Louis, MO, USA

  4. Wen-bin Yu

    Present address: Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China

  5. James H. Westwood

    Present address: School of Plant and Environmental Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

Authors and Affiliations

  1. Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Zhenzhen Yang, Saima Shahid, Elizabeth A. Kelly, Huiting Zhang, Michael J. Axtell & Claude W. dePamphilis

  2. Department of Biology, The Pennsylvania State University, University Park, PA, USA

    Zhenzhen Yang, Eric K. Wafula, Saima Shahid, Paula E. Ralph, Prakash R. Timilsena, Wen-bin Yu, Elizabeth A. Kelly, Huiting Zhang, Michael J. Axtell & Claude W. dePamphilis

  3. Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

    Gunjune Kim & James H. Westwood

  4. Department of Ecology, Evolution, and Organismal Biology, Kennesaw State University, Kennesaw, GA, USA

    Joel R. McNeal

  5. Intercollege Graduate Program in Bioinformatics and Genomics, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Thomas Nate Person & Claude W. dePamphilis

  6. Department of Statistics and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Naomi S. Altman

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  1. Zhenzhen Yang
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Contributions

C.W.deP., J.H.W. and Z.Y. conceived this project. Z.Y. performed major analyses, with additional analyses by E.K.W., S.S., G.K., J.R.M., P.R.T, W.-b.Y. and T.N.P. G.K. and P.E.R. performed experiments. E.A.K. and H.Z. performed RT–PCR. J.R.M. generated transcriptome samples for ancestral inference. M.J.A. and S.S. contributed small RNA analyses. N.S.A. supervised the statistical analyses and conception of HGTpropor. Z.Y. and C.W.deP. wrote the manuscript with contributions from E.K.W., J.H.W., P.E.R., S.S. and M.J.A. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to James H. Westwood or Claude W. dePamphilis.

Additional information

Peer review information: Nature Plants thanks David Hannapel, Fay-Wei Li, Jianqiang Wu and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Yang, Z., Wafula, E.K., Kim, G. et al. Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants. Nat. Plants 5, 991–1001 (2019). https://doi.org/10.1038/s41477-019-0458-0

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