Signatures of adaptation to plant parasitism in nematode genomes

Abstract

Plant-parasitic nematodes cause considerable damage to global agriculture. The ability to parasitize plants is a derived character that appears to have independently emerged several times in the phylum Nematoda. Morphological convergence to feeding style has been observed, but whether this is emergent from molecular convergence is less obvious. To address this, we assess whether genomic signatures can be associated with plant parasitism by nematodes. In this review, we report genomic features and characteristics that appear to be common in plant-parasitic nematodes while absent or rare in animal parasites, predators or free-living species. Candidate horizontal acquisitions of parasitism genes have systematically been found in all plant-parasitic species investigated at the sequence level. Presence of peptides that mimic plant hormones also appears to be a trait of plant-parasitic species. Annotations of the few genomes of plant-parasitic nematodes available to date have revealed a set of apparently species-specific genes on every occasion. Effector genes, important for parasitism are frequently found among those species-specific genes, indicating poor overlap. Overall, nematodes appear to have developed convergent genomic solutions to adapt to plant parasitism.

Keywords: convergence.

Fig. 1.

Schematic phylogeny of Nematoda. Simplified tree topology modified from van Megen et al. (2009), based on SSU rDNA. Clades 1–12 are according to the classification proposed by van Megen et al. (2009). Roman numbers I – V correspond to clades that had been defined in Blaxter et al. (1998). The three major Nematode lineages Enoplia, Dorylaimia and Chromadoria as described in De Ley (2006) are represented by coloured rectangles. The Chromadoria lineage is further subdivided in Spirurina, Rhabditina and Tylenchina. Taxonomic groups in which plant-parasitic species are found are coloured in green and highlighted by a leaf symbol. Underlined species names indicate availability of a genome assembly. Nematomorpha, a group mainly constituted of parasites of arthropods is the closest outgroup to nematodes.

Fig. 2.

Phylogenetic relations of nematode GH5 cellulases. This simplified phylogenetic tree is adapted from Danchin et al. (2010) and represents the evolutionary relations between nematode GH5 cellulases and their closest homologues in other species. RKN stands for ‘root-knot nematodes’, CYST for ‘cyst nematodes’, Lesion for lesion nematodes (Radopholus similis), B for bacteria. The phytophagous insects represented in this phylogeny are Apriona germari and Psacothea hilaris.

Fig. 3.

Nematode CLE motifs. LogoPlots of the 27 unique CLE domains in Arabidopsis (top) and the nine unique candidate CLE domains from M. hapla (bottom). Each M. hapla domain was included four times to balance the amplitude.

Fig. 4.

Meloidogyne hapla CEP domains. LogoPlots of the 12 CEP domains from M. hapla (top) aligned with the 11 unique CEP from Medicago truncatula (bottom).

Fig. 5.

Comparison of surface characteristics of nematode and plant CEP domains. Surface characteristics of CEP11 from Meloidogyne hapla (MhCEP11) and Medicago truncatula CEP1 (MtCEP1), shown through a 90° rotation series. Residues are colour-coded by physico-chemical property: Orange  =  hydrophobic; Blue  =  positive residues; Cyan  =  Asp; Green  =  Pro; Red = Hydroxyl group on Pro.