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. Kranse, Jose 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 () and Sebastian Eves- van den Akker ()
Additional contact information
Shahid Siddique: University of California Davis, One Shields Avenue
Zoran S. Radakovic: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Clarissa Hiltl: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Clement Pellegrin: University of Cambridge
Thomas J. Baum: Iowa State University
Helen Beasley: University of Cambridge
Andrew F. Bent: University of Wisconsin—Madison
Oliver Chitambo: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Divykriti Chopra: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Etienne G. J. Danchin: Université Côte d’Azur, INRAE, CNRS, Institut Sophia Agrobiotech
Eric Grenier: Université Rennes
Samer S. Habash: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
M. Shamim Hasan: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Johannes Helder: Wageningen University & Research, Droevendaalsesteeg 1
Tarek Hewezi: University of Tennessee
Julia Holbein: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Martijn Holterman: Wageningen University & Research, Droevendaalsesteeg 1
Sławomir Janakowski: Institute of Biology, Warsaw University of Life Sciences (SGGW)
Georgios D. Koutsovoulos: Université Côte d’Azur, INRAE, CNRS, Institut Sophia Agrobiotech
Olaf P. Kranse: University of Cambridge
Jose L. Lozano-Torres: Wageningen University & Research, Droevendaalsesteeg 1
Tom R. Maier: Iowa State University
Rick E. Masonbrink: Iowa State University
Badou Mendy: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Esther Riemer: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Mirosław Sobczak: Institute of Biology, Warsaw University of Life Sciences (SGGW)
Unnati Sonawala: University of Cambridge
Mark G. Sterken: Wageningen University & Research, Droevendaalsesteeg 1
Peter Thorpe: University of St Andrews, North Haugh
Joris J. M. van Steenbrugge: Wageningen University & Research, Droevendaalsesteeg 1
Nageena Zahid: Rheinische Friedrich-Wilhelms-University of Bonn
Florian Grundler: Rheinische Friedrich-Wilhelms-University of Bonn, INRES - Molecular Phytomedicine
Sebastian Eves- van den Akker: University of Cambridge

Nature Communications, 2022, vol. 13, issue 1, 1-19

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-33769-w

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