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A Critical Appraisal of DNA Transfer from Plants to Parasitic Cyst Nematodes.

Published version
Peer-reviewed

Repository DOI


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Authors

Ko, Itsuhiro 
Kranse, Olaf Prosper 
Senatori, Beatrice 
Eves-van den Akker, Sebastian  ORCID logo  https://orcid.org/0000-0002-8833-9679

Abstract

Plant-parasitic nematodes are one of the most economically important pests of crops. It is widely accepted that horizontal gene transfer-the natural acquisition of foreign genes in parasitic nematodes-contributes to parasitism. However, an apparent paradox has emerged from horizontal gene transfer analyses: On the one hand, distantly related organisms with very dissimilar genetic structures (i.e. bacteria), and only transient interactions with nematodes as far as we know, dominate the list of putative donors, while on the other hand, considerably more closely related organisms (i.e. the host plant), with similar genetic structure (i.e. introns) and documented long-term associations with nematodes, are rare among the list of putative donors. Given that these nematodes ingest cytoplasm from a living plant cell for several weeks, there seems to be a conspicuous absence of plant-derived cases. Here, we used comparative genomic approaches to evaluate possible plant-derived horizontal gene transfer events in plant parasitic nematodes. Our evidence supports a cautionary message for plant-derived horizontal gene transfer cases in the sugar beet cyst nematode, Heterodera schachtii. We propose a 4-step model for horizontal gene transfer from plant to parasite in order to evaluate why the absence of plant-derived horizontal gene transfer cases is observed. We find that the plant genome is mobilized by the nematode during infection, but that uptake of the said "mobilome" is the first major barrier to horizontal gene transfer from host to nematode. These results provide new insight into our understanding of the prevalence/role of nucleic acid exchange in the arms race between plants and plant parasites.

Description

Acknowledgements: This manuscript is based on I.K.'s MPhil degree thesis at the University of Cambridge, United Kingdom. Thanks to Dr. Clement Pellegrin, Dr. Unnati Sonawala, and Helen Beasley for their support during the study. Thanks to Jean-Francisco Popoff for the media preparation service. Thanks to Dr. Marie Mirouze from IRD for providing hypomethylated A. thaliana seeds. Thanks to Dr. Etienne G.J. Danchin from INRAE for advising HGT screening. Thanks to Dr. Rick E. Masonbrink and Mr. Thomas R. Maier from the Iowa State University for sharing the advice and data for HGT research in PPNs. Special thanks to Dr. Claude W. dePamphilis from the Pennsylvania State University and Dr. Huiting Zhang from Washington State University for suggesting writing and phylogenetic analysis of HGT screening.


Funder: British Society for Plant Pathology; DOI: https://doi.org/10.13039/501100000567

Keywords

cyst nematodes, horizontal gene transfer, plant-parasitic nematodes, Animals, Plants, DNA, Genomics, Tylenchoidea, Plant Diseases

Journal Title

Mol Biol Evol

Conference Name

Journal ISSN

0737-4038
1537-1719

Volume Title

41

Publisher

Oxford University Press (OUP)
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/R011311/1)
Biotechnology and Biological Sciences Research Council (BB/S006397/1)