The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

• DOI: 10.1038/s41467-022-33769-w
• Publication Date: 2022-10-19T14:04:20Z
• Authors: Shahid Siddique; Zoran S. Radakovic; Clarissa Hiltl; Clement Pellegrin; Thomas J. Baum; Helen Beasley; Andrew F. Bent; Oliver Chitambo; Divykriti Chopra; Etienne G. J. Dan...; Eric Grenier; Samer S. Habash; M. Shamim Hasan; Johannes Helder; Tarek Hewezi; Julia Holbein; Martijn Holterman; Sławomir Janakowski; Georgios D. Kouts...; Olaf P. Kranse; Jose L. Lozano-To...; Tom R. Maier; Rick E. Masonbrink; Badou Mendy; Esther Riemer; Mirosław Sobczak; Unnati Sonawala; Mark G. Sterken; Peter Thorpe; Joris J. M. van S...; Nageena Zahid; Florian Grundler; Sebastian Eves-va...
• Keywords: 0301 basic medicine; [SDV]Life Sciences [q-bio]; 02 engineering and technology; 630; Pantothenic Acid; 2.2 Factors relating to the physical environment; QR180 Immunology; Aetiology; 2. Zero hunger; Cysts; Q; article; Biological Sciences; /96/63; Infectious Diseases; QR180; /631/208/212; Infection; Tylenchida; Science; 0206 medical engineering; Veterinary and Food Sciences; /631/337/2019; /45/23; QH426 Genetics; QK Botany; Article; /38/91; 03 medical and health sciences; /38/89; Genetics; Life Science; Animals; Parasites; /631/449/2676/2677; Veterinary Sciences; QH426; Nutrition; MCC; Agricultural; Prevention; QK; Human Genome; DAS; /631/158/2456; Transcriptome

AbstractPlant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops.