Any movement of genetic information, other than by vertical transmission from parents to their offspring via conventional reproduction, is defined as horizontal or lateral gene transfer (HGT or LGT). Although LGT occurs frequently among members of the Archaea and Bacteria, there are only a few probable cases of LGT between prokaryotes and multicellular eukaryotes that have resulted in new functional genes for the recipient. Likely cases of LGT in which the eukaryote is acting as a donor have been described for two mosquito species, Aedes aegypti
and Anopheles gambiae
]. The transfer of a gene related to malaria sporozoite invasion from mosquito to its endosymbiotic bacterium Wolbachia pipientis
was demonstrated by Woolfit et al. (2008,
]). This gene showed substantial divergence, and the level of expression suggested it to be functional in the new prokaryote host. Inter-domain gene transfers can also happen in the reverse way. The pea aphid Acyrthisiphon pisum
probably acquired two genes from bacteria by LGT
]. These laterally transferred genes are expressed in the bacteriocytes, and they contribute to the maintenance of Buchnera aphidicola,
the aphid’s primary symbiont. Donors from multiple domains (bacteria, fungi and plants) are thought to be implicated in the acquisition of at least ten protein-coding sequences by the bdelloid rotifer Adineta vaga
]. A subset of these genes were transcribed and correctly spliced. Interestingly, the authors hypothesized that LGT could be facilitated by mechanisms underlying the desiccation tolerance of this rotifer.
The lateral gene transfer of prokaryotic genes has presumably also played a key role in the evolution of plant parasitism in nematodes. Plant cells are protected by a cell wall, and penetration of this wall is a prerequisite to reach the cytosol. Potato and a soybean cyst nematode (Globodera rostochiensis
and Heterodera glycines
) were the first animals shown to harbor symbiont-independent cellulases
]. These cellulases are classified as members of the glycoside hydrolase family 5 (GHF5). The nematode cellulases appeared to be most similar to bacterial cellulases. In an editorial comment Keen and Roberts
] suggested that lateral gene transfer may drive the mobility of “pathogenicity islands” (including cellulases) from one organism to the other. Over the last decade, plant parasitic nematodes were shown to harbor a wide spectrum of cell wall-degrading proteins such as pectate lyases
] and expansins
]. These genes are expressed during infective life stages, and contribute to nematode’s ability to exploit plants as a food source.
Bacterivory is generally accepted as the ancestral feeding type of nematodes. A longstanding hypthesis suggests that bacterivores gave rise to fungivorous nematodes, and facultative and obligatory plant parasites arose from fungal feeding ancestors
]. It is conceivable that the evolution of plant parasitism in nematodes was driven by the lateral transfer of genes via ingestion of the donor (soil bacteria) by the recipient (bacterivorous nematodes)
]. Mechanisms underlying desiccation tolerance could have facilitated the uptake of prokaryotic DNA
]. A number of nematode species including Aphelenchus avenae
], Ditylenchus dipsaci
], and Panagrolaimus superbus
] can develop into highly drought resistant Dauer larva.
Among nematode genes that could have been acquired via one or multiple HGT events, GHF5 cellulases are best characterized. Recent genome sequencing projects resulted in the identification of large cellulase families in the root-knot nematodes Meloidogyne incognita
] and Meloidogyne hapla
]. These are highly derived (distal) species within the family Meloidogynidae, and to identify possible origin(s) of these genes, cellulase sequence information is required from less derived representatives of this family. Recent morphological and molecular studies based on female gonoduct architecture
] and small subunit ribosomal DNA sequences
] suggest that root-knot nematodes originate from - and constitute a subclade within - the genus Pratylenchus
. By sequencing cellulase genes from Pratylenchus spp.
(lesion nematodes) and basal root-knot nematode species - the ones that do not belong to one of the subclades I, II and III as defined in 2002 by Tandingan De Ley et al.
] -, we intended to generate clues to establish the evolutionary relationship between members of the Pratylenchidae genera Pratylenchus
and basal root-knot nematode species such as Meloidogyne ichinohei, M. mali
and M ulmi
Several models have been proposed about HGT event(s) underlying the acquisition of cellulases by plant parasitic and fungivorous nematodes. So far it is unclear whether the distribution of cellulase-encoding genes among Tylenchida is the result of a single HGT event, followed by early single duplication event as suggested by Kyndt et al.
], or the outcome of multiple HGT events. Comparison of the topologies of phylogenetic trees based on SSU rDNA data (e.g.
GHF5 cellulase-based tree might tell us whether the evolution within the Pratylenchidae/Meloidogynidae branch includes one or multiple distinct cellulase lineages. Analysis of 103 paralogs and orthologs of cellulase-encoding gene(s) (fragments) from plant parasitic Tylenchida revealed a major clade with a topology similar to the one revealed by SSU rDNA, a neutral gene. Moreover, a relatively small, divergent subset of cellulases was found that is probably the result of early substrate specificity-driven diversification. Within the catalytic domain types A and B (too few type C sequences are available to make a statement), the overall topology resembles the topologies revealed by neutral ribosomal DNA sequences, and it is hypothesized that root-knot, cyst and lesion nematodes received their cellulases from more ancient Pratylenchidae or even more basal members of Clade 12
], rather than by direct lateral gene transfer.