Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

Abstract

Lateral gene transfer from prokaryotes to animals is poorly understood, and the scarce documented examples generally concern genes of uncharacterized role in the receiver organism. In contrast, in plant-parasitic nematodes, several genes, usually not found in animals and similar to bacterial homologs, play essential roles for successful parasitism. Many of these encode plant cell wall-degrading enzymes that constitute an unprecedented arsenal in animals in terms of both abundance and diversity. Here we report that independent lateral gene transfers from different bacteria, followed by gene duplications and early gain of introns, have shaped this repertoire. We also show protein immunolocalization data that suggest additional roles for some of these cell wall-degrading enzymes in the late stages of these parasites' life cycle. Multiple functional acquisitions of exogenous genes that provide selective advantage were probably crucial for the emergence and proficiency of plant parasitism in nematodes.

Fig. 1.

Phylogenetic trees of pectin-modifying proteins. (A) GH28 polygalacturonases. (B) PL3 pectate lyases. (C) GH43 candidate arabinanases. Phylogenetic groups are color-coded according to their taxonomy. Posterior probability (PP) support values are indicated at corresponding nodes, and those supported by bootsrap values higher than 75 in maximum likelihood trees are underlined and in boldface type. RKN, root-knot nematode; CN, cyst nematode. Dashed lines delineate phylogenetic groupings of bacterial and plant-parasitic nematode genes; the corresponding PP value is circled.

Fig. 2.

Phylogenetic trees of cellulose/hemicellulose-modifying proteins and expansin-like proteins. (A) GH5 cellulases. Radop. stands for Radopholinae, Pratyl. for Pratylenchidae. (B) GH5 xylanases. (C) Expansin-like proteins. Phylogenetic groups are color-coded according to their taxonomy. Posterior probability (PP) support values are indicated at corresponding nodes, and those supported by bootstrap values higher than 75 in maximum likelihood trees are underlined and in boldface type. Groups supported by PP values higher than 0.8 were collapsed. RKN, root-knot nematode; CN for cyst nematode.

Fig. 3.

Immunodetection of CBM2-bearing proteins within adult sedentary females of M. incognita during parasitism of tomato roots. (A and B) Gall containing an adult female, displaying CBM2-bearing proteins accumulated in the eggs (green and indicated by orange arrows) within the ovary. (C and D) Localization of CBM2-bearing proteins accumulated in the vagina of adult females (green and indicated by orange arrow in C). (A and C) Overlay images of CBM2-bearing proteins (green) and DAPI-stained nuclei (blue); (B and D) Overlay images of CBM2-bearing proteins (green), DAPI-stained nuclei (blue), and differential interference contrast (gray). N, nematode; e, egg; G, gall; gm, gelatinous matrix; v, vagina; rg, rectal gland. Scale bar: 10 μm. Control images are available in the SI Appendix, Fig. S10.