Europe as a secondary distribution hub in the worldwide invasion of the potato cyst nematode Globodera rostochiensis

Authors: ESQUIBET, MAGALI - University Of Rennes, France; MWANGI, JAMES - Julius Kuhn Institute; KIEWNICK, SEBASTIAN - Julius Kuhn Institute; Wang, Xiaohong; MIMEE, BENJAMIN - Agriculture And Agri-Food Canada; HANDAYANI, NURAL DWI - Ghent University; BERT, WIM - Ghent University; HELDER, JOHANNES - Wageningen University; WAINER, JOHN - Agriculture Victoria; SAKATA, ITARU - National Agriculture And Food Research Organization (NARO), Agricultrual Research Center; GARCA, NATHAN - University Of Rennes, France; GRENIER, ERIC - University Of Rennes, France; MONTARRY, JOSSELIN - University Of Rennes, France

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/11/2024
Publication Date: 6/17/2024
Citation: Esquibet, M., Mwangi, J.M., Kiewnick, S., Wang, X., Mimee, B., Handayani, N., Bert, W., Helder, J., Wainer, J., Sakata, I., Garca, N., Grenier, E., Montarry, J. 2024. Europe as a secondary distribution hub in the worldwide invasion of the potato cyst nematode Globodera rostochiensis. Scientific Reports. 14, Article number: 13915 (2024). https://doi.org/10.1038/s41598-024-64617-0.
DOI: https://doi.org/10.1038/s41598-024-64617-0

Interpretive Summary: The potato cyst nematode (Globodera rostochiensis; a.k.a. golden nematode) originates from the Andean Mountains in South America, and it has unintentionally spread to every continent. Previous studies have looked at the genetic relationship of different nematode populations in various countries using specific DNA markers. But combining data from different labs is tough and can introduce difficulty in interpreting the results. To tackle this issue and investigate how this pest has been spread, we studied 22 golden nematode populations from every continent. We observed the highest genetic diversity among the South American populations. European populations had a moderate level of diversity, while the other populations had lower genetic diversity. Our study confirmed the previous knowledge that the pest was initially introduced to Europe from South America. Further analyses support the hypothesis that populations from North America, Africa, Asia, and Oceania most likely originated from Europe, highlighting Europe as a bridgehead in the worldwide invasion history of the golden nematode. As international trade of seed tubers is expected to increase, our study emphasizes the importance of importing seed tubers from approved supplies to reduce the risk of new introductions of the golden nematode.

Technical Abstract: The potato cyst nematode Globodera rostochiensis originates from the Andean Mountain region in South America and has unintentionally been introduced to all inhabited continents. Several studies have examined the population genetic structure of this pest in various countries by using microsatellite markers. However, merging microsatellite data produced from different laboratories is challenging and can introduce uncertainty when interpreting the results. To overcome this challenge and to explore invasion routes of this pest, we have genotyped 22 G. rostochiensis populations from all continents. Within populations, the highest genetic diversity was observed in the South American populations, the European populations showed an intermediate level of genetic diversity and the remaining populations were the less diverse. This confirmed pre-existing knowledge such as a first introduction event from South America to Europe, but the less diverse populations could originate either from South America or from Europe. At the continental scale, STRUCTURE genetic clustering output indicated that North America and Asia have experienced at least two introduction events. Comparing different evolutionary scenarios, the Approximate Bayesian Computation analysis showed that Europe served as a secondary distribution centre for the invasion of G. rostochiensis into all other continents (North America, Africa, Asia and Oceania).