Genomic reconstruction of the introduction and diversification of golden potato cyst nematode populations in Indonesia.

Potato cyst nematodes (PCN), the umbrella term for Globodera rostochiensis and G. pallida, co-evolved with their Solanaceous hosts in the Andeans. From there, PCN proliferated worldwide to virtually all potato production areas. PCN is a major factor limiting the potato production in Indonesia. In our survey, only G. rostochiensis was found. Fourteen field populations were collected on Java and Sumatra, and unique variants were called by mapping re-sequencing data on a G. rostochiensis reference genome. A phylogenetic tree based on 1.4 million unique variants showed a genotypic separation between the outgroup, a Scottish Ro1 population, and all Indonesian populations. This separation was comparable in size to the genotypic distinction between the Javanese and the Sumatran PCN populations. Next, variants within PCN effector gene families SPRYSEC, 1106, 4D06, and venom allergen-like protein (VAL) that all interfere with the host innate immune system were compared. Distinct selective pressures acted on these effector families; while SPRYSECs (4,341 SNPs/indels) behaved like neutral genes, the phylogenetic trees of 1106, 4D06 and VAL proteins (respectively 235, 790 and 150 SNPs/indels) showed deviating topologies. Our data suggest that PCN was introduced on Java not too long after the introduction of potato in the middle of the 18th century. Soon thereafter, the pathogen established on Sumatra, and started to diversify independently. This scenario was corroborated by diversification patterns of the effector families 1106, 4D06 and VAL. Our data demonstrate how genome re-sequencing data from a non-indigenous pathogen can be used to reconstruct the introduction and diversification process.