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

Abstract

Plant-parasitic nematodes are a major, and in some cases a dominant, threat to crop production in all agricultural systems. The relative scarcity of classical resistance genes highlights a pressing need to identify new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality 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 stages of the interaction. This novel approach enabled the analysis of the hologenome of the infection site, to identify 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 the highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is critically important for parasitism. Knockout of either the plant-encoded or the now nematode-encoded steps in the pathway blocks parasitism. Our experiments establish a reference for cyst nematodes, use this platform to further our fundamental understanding of the evolution of plant-parasitism by nematodes, and show that understanding congruent differential expression of metabolic pathways represents a new way to find nematode susceptibility genes, and thereby, targets for future genome editing-mediated generation of nematode-resistant crops.

Glutathione contributes to plant defence against parasitic cyst nematodes

“…To investigate the roles of glutathione biosynthetic genes during different phases of Arabidopsis parasitism by CN, we examined the expression patterns of GSH1 and GSH2 in publicly available transcriptomic data (Mendy et al, 2017 ; Siddique et al, 2021 ; Szakasits et al, 2009 ). These surveys revealed a significant increase in GSH1 expression during the migratory (10 h postinoculation, hpi) and sedentary (5 and 15 days postinfection, dpi) stages of cyst nematode infection (Table S1 and Figure S1 ).…”

Mode of action of fluopyram in plant-parasitic nematodes

“…These protein sequences were used as queries to search for similar sequences in different nematode species as well as Homo sapiens , Mus musculus and Rattus norvegicus utilizing the basic local alignment search tool (BLAST) provided by the National Center for Biotechnology Information (NCBI; blast.ncbi.nlm.nih.gov) 24 and WormBase (wormbase.org) 25 . The respective sequences of H. schachtii were extracted from in house genomic data 26 .…”

Comparative genomics among cyst nematodes reveals distinct evolutionary histories among effector families and an irregular distribution of effector‐associated promoter motifs

“…This allowed us to compare effector family diversification among the two PCN species, G. pallida and G. rostochiensis, and establish the polarity of these contrasts by using H. schachtii as an outgroup (both Globodera and Heterodera belong to the family Heteroderidae). The current genome size, 190 Mb, is slightly above the genome size estimated by flow cytometry, 160-170 Mb (Siddique et al, 2021). Notably, both the predicted number of genes and transcripts were about 50% higher in H. schachtii than in the two Globodera species (Table 1).…”