Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach

Scholl, Elizabeth H.; Thorne, Jeffrey L.; McCarter, James P.; Bird, David

doi:10.1186/gb-2003-4-6-r39

Cited by 136 publications

(35 citation statements)

References 55 publications

(62 reference statements)

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“…We concur with this notion and propose that the evolution of parasitism in RKN was accompanied by conscription of the older symbiotic pathways for RKN pathogenesis. The previous findings that RKN appear to have acquired rhizobial genes via horizontal gene transfer (18,19), including those associated with NF biosynthesis, suggest a mechanism for such evolutionary adaptation. We have shown that legume root-hair cells respond in a defined, rapid, and stereotypical manner to RKN perfusates before direct contact is made between nematode and plant; models of GC induction should allow for a similar possibility.…”

Section: Discussionmentioning

confidence: 99%

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Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus

Weerasinghe

Bird

Allen

2005

Proc. Natl. Acad. Sci. U.S.A.

135

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The symbiosis responsible for nitrogen fixation in legume root nodules is initiated by rhizobial signaling molecules [Nod factors (NF)]. Using transgenically tagged microtubules and actin, we dynamically profiled the spatiotemporal changes in the cytoskeleton of living Lotus japonicus root hairs, which precede root-hair deformation and reflect one of the earliest host responses to NF. Remarkably, plant-parasitic root-knot nematodes (RKN) invoke a cytoskeletal response identical to that seen in response to NF and induce root-hair waviness and branching in legume root hairs via a signal able to function at a distance. Azide-killed nematodes do not produce this signal. A similar response to RKN was seen in tomato. Aspects of the host responses to RKN were altered or abolished by mutations in the NF receptor genes nfr1, nfr5, and symRK, suggesting that RKN produce a molecule with functional equivalence to NF, which we name NemF. Because the ability of RKN to establish feeding sites and reproduce was markedly reduced in the mutant lines, we propose that RKN have adapted at least part of the symbiont-response pathway to enhance their parasitic ability.cytoskeleton ͉ NemF ͉ rhizobia ͉ actin ͉ microtubule P lants engage other organisms in diverse symbioses ranging from mutualistic associations with rhizobia and mycorrhizae (supplying the plant with fixed nitrogen and phosphorous, respectively) to hosting harmful parasites such as root-knot nematodes (RKN, Meloidogyne spp.). Unlike rhizobia, which interact with strictly defined legume species, the RKN host range encompasses essentially all vascular plants, leading to extensive crop loss worldwide (1). The specificity of particular rhizobial-legume associations is largely mediated at the root surface via specific lipochitooligosaccharide signaling molecules (2) synthesized by the bacterium and collectively termed Nod factors (NF). Invasion of the host by rhizobia is a highly orchestrated process, beginning with ion movements (3-5) and changes in cytoskeletal organization (6 -8). The resultant signals lead to the first morphologically visible step, which is the disruption of the normal tip-growing pattern and curling of epidermal root hair cells 2-4 h after initial exposure and before bacterial entry (9). NF alone is sufficient to elicit cytoskeletal and ion responses, gene expression changes (10, 11), root-hair deformation, and the formation of pseudonodules, but not infection threads. NF production and host sensitivity both are essential for nodulation (12,13).In contrast, RKN apparently enter the host simply by mechanical penetration. Migration into the vascular cylinder is intercellular and nondestructive and, once in the stele, RKN induce characteristic giant cells (GC), from which the developing larvae feed. GC formation invokes host pathways in common with those necessary for nitrogen-nodule formation, including induction of specific transcription regulators (14), early nodulation genes (15, 16), and cytokinin-response pathways (17), suggesting that at the cellular ...

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Section: Discussionmentioning

confidence: 99%

“…Consistent with this, a beet cyst nematodeinducible resistance gene is induced during rhizobial invasion (11). EST sequencing revealed RKN homologues of rhizobial sequences, including genes required for NF synthesis (18,19).…”

mentioning

confidence: 99%

Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus

Weerasinghe

Bird

Allen

2005

Proc. Natl. Acad. Sci. U.S.A.

135

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“…Horizontal transfer of GHF5 cellulases from bacteria to other plant parasitic nematodes has been proposed and it has been suggested that this transfer occurred from a bacterium closely associated with an ancestor of these nematodes [27,28]. The ancestor of B. xylophilus was probably a fungal feeder [29] and more closely associated with fungi than with bacteria.…”

Section: Discussionmentioning

confidence: 99%

A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus

Jones²,

et al. 2004

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We have characterized a family of GHF45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. The absence of such genes from other nematodes and their similarity to fungal genes suggests that they may have been acquired by horizontal gene transfer (HGT) from fungi. The cell wall degrading enzymes of other plant parasitic nematodes may have been acquired by HGT from bacteria. B. xylophilus is not directly related to other plant parasites and our data therefore suggest that horizontal transfer of cell wall degrading enzymes has played a key role in evolution of plant parasitism by nematodes on more than one occasion.

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“…However, relatively few cases have been documented in multicellular organisms [3-7]. Reports of HGT in animals are usually limited to the description of the transfer of only one or a few genes, making the extent of horizontal gene transfer in animals unclear.…”

Section: Introductionmentioning

confidence: 99%

Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes

et al. 2015

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BackgroundA fundamental concept in biology is that heritable material, DNA, is passed from parent to offspring, a process called vertical gene transfer. An alternative mechanism of gene acquisition is through horizontal gene transfer (HGT), which involves movement of genetic material between different species. HGT is well-known in single-celled organisms such as bacteria, but its existence in higher organisms, including animals, is less well established, and is controversial in humans.ResultsWe have taken advantage of the recent availability of a sufficient number of high-quality genomes and associated transcriptomes to carry out a detailed examination of HGT in 26 animal species (10 primates, 12 flies and four nematodes) and a simplified analysis in a further 14 vertebrates. Genome-wide comparative and phylogenetic analyses show that HGT in animals typically gives rise to tens or hundreds of active ‘foreign’ genes, largely concerned with metabolism. Our analyses suggest that while fruit flies and nematodes have continued to acquire foreign genes throughout their evolution, humans and other primates have gained relatively few since their common ancestor. We also resolve the controversy surrounding previous evidence of HGT in humans and provide at least 33 new examples of horizontally acquired genes.ConclusionsWe argue that HGT has occurred, and continues to occur, on a previously unsuspected scale in metazoans and is likely to have contributed to biochemical diversification during animal evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0607-3) contains supplementary material, which is available to authorized users.

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Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach

Cited by 136 publications

References 55 publications

Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus

Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus

A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus

Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes

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