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

Shahid Siddique, Zoran S. Radakovic, Clarissa Hiltl, Clement Pellegrin, Thomas J. Baum, Helen Beasley, Andrew F. Bent, Oliver Chitambo, Divykriti Chopra, Etienne G. J. Danchin, Eric Grenier, Samer S. Habash, M. Shamim Hasan, Johannes Helder, Tarek Hewezi, Julia Holbein, Martijn Holterman, Sławomir Janakowski, Georgios D. Koutsovoulos, Olaf P. KranseJose L. Lozano-Torres, Tom R. Maier, Rick E. Masonbrink, Badou Mendy, Esther Riemer, Mirosław Sobczak, Unnati Sonawala, Mark G. Sterken, Peter Thorpe, Joris J. M. van Steenbrugge, Nageena Zahid, Florian Grundler*, Sebastian Eves-van den Akker*

*Corresponding author for this work

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Abstract

Plant-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.
Original languageEnglish
Article number6190
Number of pages19
JournalNature Communications
Volume13
DOIs
Publication statusPublished - 19 Oct 2022

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