PMID- 35560992 OWN - NLM STAT- MEDLINE DCOM- 20230309 LR - 20240320 IS - 1365-294X (Electronic) IS - 0962-1083 (Print) IS - 0962-1083 (Linking) VI - 32 IP - 6 DP - 2023 Mar TI - Comparative genomics among cyst nematodes reveals distinct evolutionary histories among effector families and an irregular distribution of effector-associated promoter motifs. PG - 1515-1529 LID - 10.1111/mec.16505 [doi] AB - Potato cyst nematodes (PCNs), an umbrella term used for two species, Globodera pallida and G. rostochiensis, belong worldwide to the most harmful pathogens of potato. Pathotype-specific host plant resistances are essential for PCN control. However, the poor delineation of G. pallida pathotypes has hampered the efficient use of available host plant resistances. Long-read sequencing technology allowed us to generate a new reference genome of G. pallida population D383 and, as compared to the current reference, the new genome assembly is 42 times less fragmented. For comparison of diversification patterns of six effector families between G. pallida and G. rostochiensis, an additional reference genome was generated for an outgroup, the beet cyst nematode Heterodera schachtii (IRS population). Large evolutionary contrasts in effector family topologies were observed. While VAPs (venom allergen-like proteins) diversified before the split between the three cyst nematode species, the families GLAND5 and GLAND13 only expanded in PCNs after their separation from the genus Heterodera. Although DNA motifs in the promoter regions thought to be involved in the orchestration of effector expression ("DOG boxes") were present in all three cyst nematode species, their presence is not a necessity for dorsal gland-produced effectors. Notably, DOG box dosage was only loosely correlated with the expression level of individual effector variants. Comparison of the G. pallida genome with those of two other cyst nematodes underlined the fundamental differences in evolutionary history between effector families. Resequencing of PCN populations with different virulence characteristics will allow for the linking of these characteristics to the composition of the effector repertoire as well as for the mapping of PCN diversification patterns resulting from extreme anthropogenic range expansion. CI - (c) 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. FAU - van Steenbrugge, Joris J M AU - van Steenbrugge JJM AUID- ORCID: 0000-0002-9961-2538 AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - van den Elsen, Sven AU - van den Elsen S AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Holterman, Martijn AU - Holterman M AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. AD - Solynta, Wageningen, The Netherlands. FAU - Lozano-Torres, Jose L AU - Lozano-Torres JL AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Putker, Vera AU - Putker V AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Thorpe, Peter AU - Thorpe P AD - School of Medicine, Medical & Biological Sciences, University of St. Andrews, St Andrews, UK. FAU - Goverse, Aska AU - Goverse A AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Sterken, Mark G AU - Sterken MG AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Smant, Geert AU - Smant G AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. FAU - Helder, Johannes AU - Helder J AD - Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. LA - eng GR - WT_/Wellcome Trust/United Kingdom PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20220601 PL - England TA - Mol Ecol JT - Molecular ecology JID - 9214478 RN - 0 (Antioxidants) SB - IM MH - Animals MH - *Genomics MH - Sequence Analysis, DNA MH - Antioxidants MH - Promoter Regions, Genetic MH - *Nematoda PMC - PMC10946958 OTO - NOTNLM OT - Globodera OT - Heterodera OT - DOG box OT - cyst nematodes OT - nematode effectors COIS- All authors declare that they have no conflict of interest. EDAT- 2022/05/14 06:00 MHDA- 2023/03/10 06:00 PMCR- 2024/03/18 CRDT- 2022/05/13 19:31 PHST- 2022/04/26 00:00 [revised] PHST- 2021/11/02 00:00 [received] PHST- 2022/05/04 00:00 [accepted] PHST- 2022/05/14 06:00 [pubmed] PHST- 2023/03/10 06:00 [medline] PHST- 2022/05/13 19:31 [entrez] PHST- 2024/03/18 00:00 [pmc-release] AID - MEC16505 [pii] AID - 10.1111/mec.16505 [doi] PST - ppublish SO - Mol Ecol. 2023 Mar;32(6):1515-1529. doi: 10.1111/mec.16505. Epub 2022 Jun 1.