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 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.

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

“…Notably, both the predicted number of genes and transcripts were about 50% higher in H. schachtii than in the two Globodera species (Table 1). These figures largely correspond to a H. schachtii genome assembly that was recently published from a German population referred to as “Bonn” with an assembly size of 179 Mb, and 26,700 predicted genes (Siddique et al, 2021).…”

“…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).…”

The Aphelenchoides genomes reveal substantial horizontal gene transfers in the last common ancestor of free‐living and major plant‐parasitic nematodes

“…In PPNs, the GH5 cellulase was found to be present in Tylenchida and only A. pseudobesseyi and A. bicaudatus within the Aphelenchoidea clade (Danchin et al, 2010; Wu et al, 2016), raising the possibility that many of the HGT genes were acquired in the last common ancestor of major PPNs but were differentially lost. To identify such events, a total of 27 proteomes from representative nematodes including the Aphelenchoides genomes were searched for evidence of HGT by calculating the AI score using alienness (Rancurel et al, 2017), which has been applied to infer HGT candidates in various nematode species (Grynberg et al, 2020; Schiffer et al, 2019; Siddique et al, 2022). We identified a total of 1675 HGT orthogroups in 22 nematodes.…”

An eggshell-localised annexin plays a key role in the coordination of the life cycle of a plant-parasitic nematode with its host

“…This expression profile was not seen for any other G. rostochiensis or G. pallida annexin sequences. This stage-specific expression pattern was shared by the orthologous protein in Heterodera schachtii which shares part of the Globodera spp.-specific annexin motif (Fig 3C and 3F) and may therefore have a similar functional role [22]. The three most similar sequences in the root knot nematode Meloidogyne incogntia…”