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.LGT) is the transmission of genes between organisms by mechanisms other than vertical inheritance from an ancestor to an offspring. Although largely documented as an important evolutionary mechanism in prokaryotes (1), LGT in animals that have a separate germline and whose genome is segregated in a nucleus is poorly explored. Although some examples have been described (2-4), most concern transfers from endosymbiotic bacteria, and none provide a clear link between the activity of the transferred gene products and the biology of the host species. Thus, arguments are lacking to support a selective advantage that would have driven fixation of transferred genes at the level of a population or species. By contrast, in plant-parasitic nematodes, a series of genes encoding plant cell wall-degrading or -modifying enzymes, which are usually absent from animals, exhibit similarity to bacteria and may thus originate from LGT. These genes are transcriptionally active, their products have been biochemically characterized, they are secreted in plant tissues, and their inactivation impairs parasitism efficiency (5). The most damaging nematodes to agriculture worldwide belong to the suborder Tylenchina in clade IV that comprises root-knot nematodes and cyst nematodes, the two most-studied lineages (SI Appendix, Fig. S1). These nematodes are able to penetrate and migrate into plant tissue and establish sophisticated parasitic interactions with their hosts. Invasion of the root tissues by nematodes requires degradation of the plant cell wall protective barrier, constituted mainly of cellulose and hemicelluloses as well as pectin and its branched decorations. The first plant cell wall-degrading enzymes from an animal were characterized in cyst nematodes in 1998 (6). Ten years later, analysis of the genome of Meloidogyne incognita, the first genome analysis for a plant-parasitic nematode, revealed that the repertoire of cell wall-degrading enzymes in a single species is diverse and abundant with more than 60 genes covering six different pro...

TheDitylenchus destructorgenome provides new insights into the evolution of plant parasitic nematodes

“…Other cell wall-modifying genes identified in other plant nematodes were also present in D. destructor, including xylanases (GH30), arabinases (GH43) and pectate lyase (PL3). However, no genes homologous to polygalacturonase (GH28) or expansin were found in D. destructor, despite their frequent presence in other plant nematodes [39].…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…A number of cellulase genes probably acquired from different sources have been found in genomes of plantparasitic nematodes [35][36][37]. Interestingly, these cellulase genes have experienced multiple post-transfer duplication events [37] and are different from those present in necromenic nematodes (see above), thereby suggesting that they might be involved in degradation of the plant cell wall.…”

“…Other plant cell wall-degrading enzymes presumptively acquired by horizontal gene transfer, such as xylanases, pectate lyases and polygalacturonases have been found in these nematodes [37]. A number of experimental data (reviewed in Danchin & Rosso [25] have shown that these genes are transcribed, their products are functional and excreted to plant tissues and the gene inactivation by knock-down leads to a reduction in the success of infection.…”

“…Interestingly, these cellulase genes have experienced multiple post-transfer duplication events [37] and are different from those present in necromenic nematodes (see above), thereby suggesting that they might be involved in degradation of the plant cell wall.…”

Nematode-derived drosomycin-type antifungal peptides provide evidence for plant-to-ecdysozoan horizontal transfer of a disease resistance gene

“…Extensive gene duplication to assemble a multigene family is a typical feature observed in many genes transferred to the nematode genomes 43 . In plants and the ecdysozoans with this gene, most of DTAFPs also exist as multigene families and some have evolved novel biological functions.…”