scholarly journals Horizontal Gene Transfer in Nematodes: A Catalyst for Plant Parasitism?

2011 ◽  
Vol 24 (8) ◽  
pp. 879-887 ◽  
Author(s):  
Annelies Haegeman ◽  
John T. Jones ◽  
Etienne G. J. Danchin

The origin of plant parasitism within the phylum Nematoda is intriguing. The ability to parasitize plants has originated independently at least three times during nematode evolution and, as more molecular data has emerged, it has become clear that multiple instances of horizontal gene transfer (HGT) from bacteria and fungi have played a crucial role in the nematode's adaptation to this new lifestyle. The first reported HGT cases in plant-parasitic nematodes were genes encoding plant cell wall–degrading enzymes. Other putative examples of HGT were subsequently described, including genes that may be involved in the modulation of the plant's defense system, the establishment of a nematode feeding site, and the synthesis or processing of nutrients. Although, in many cases, it is difficult to pinpoint the donor organism, candidate donors are usually soil dwelling and are either plant-pathogenic or plant-associated microorganisms, hence occupying the same ecological niche as the nematodes. The exact mechanisms of transfer are unknown, although close contacts with donor microorganisms, such as symbiotic or trophic interactions, are a possibility. The widespread occurrence of horizontally transferred genes in evolutionarily independent plant-parasitic nematode lineages suggests that HGT may be a prerequisite for successful plant parasitism in nematodes.

2013 ◽  
Vol 280 (1763) ◽  
pp. 20131021 ◽  
Author(s):  
Yannick Pauchet ◽  
David G. Heckel

The primary plant cell wall comprises the most abundant polysaccharides on the Earth and represents a rich source of energy for organisms which have evolved the ability to digest them. Enzymes able to degrade plant cell wall polysaccharides are widely distributed in micro-organisms but are generally absent in animals, although their presence in insects, especially phytophagous beetles from the superfamilies Chrysomeloidea and Curculionoidea, has recently begun to be appreciated. The observed patchy distribution of endogenous genes encoding these enzymes in animals has raised questions about their evolutionary origins. Recent evidence suggests that endogenous plant cell wall degrading enzymes-encoding genes have been acquired by animals through a mechanism known as horizontal gene transfer (HGT). HGT describes how genetic material is moved by means other than vertical inheritance from a parent to an offspring. Here, we provide evidence that the mustard leaf beetle, Phaedon cochleariae , possesses in its genome genes encoding active xylanases from the glycoside hydrolase family 11 (GH11). We also provide evidence that these genes were originally acquired by P. cochleariae from a species of gammaproteobacteria through HGT. This represents the first example of the presence of genes from the GH11 family in animals.


Nematology ◽  
2005 ◽  
Vol 7 (5) ◽  
pp. 641-646 ◽  
Author(s):  
Taisei Kikuchi ◽  
Cleber Furlanetto ◽  
John Jones

AbstractPhylogenetic studies have shown that parasitism of plants by nematodes has arisen independently on at least three separate occasions. We argue that horizontal gene transfer has played a critical role in the evolution of plant parasitism on each occasion. In addition, we discuss evidence that suggests this process has driven the evolution of other life strategies within the Nematoda and that it may be considerably more common within the Phylum than commonly thought. We review recent literature that shows horizontal gene transfer to nematodes has occurred from both bacteria and fungi.


2008 ◽  
Vol 148 (1) ◽  
pp. 358-368 ◽  
Author(s):  
Wim Grunewald ◽  
Mansour Karimi ◽  
Krzysztof Wieczorek ◽  
Elke Van de Cappelle ◽  
Elisabeth Wischnitzki ◽  
...  

2016 ◽  
Vol 33 (6) ◽  
pp. 1571-1579 ◽  
Author(s):  
Etienne G.J. Danchin ◽  
Elena A. Guzeeva ◽  
Sophie Mantelin ◽  
Adokiye Berepiki ◽  
John T. Jones

BMC Genomics ◽  
2019 ◽  
Vol 20 (1) ◽  
Author(s):  
Matan Shelomi ◽  
Shih-Shun Lin ◽  
Li-Yu Liu

Abstract Background The coconut rhinoceros beetle, Oryctes rhinoceros, is a major pest of palm crops in tropical Asia and the Pacific Islands. Little molecular data exists for this pest, impeding our ability to develop effective countermeasures and deal with the species’ growing resistance to viral biocontrols. We present the first molecular biology analyses of this species, including a metagenomic assay to understand the microbiome of different sections of its digestive tract, and a transcriptomics assay to complement the microbiome data and to shed light on genes of interest like plant cell wall degrading enzymes and immunity and xenobiotic resistance genes. Results The gut microbiota of Oryctes rhinoceros larvae is quite similar to that of the termite gut, as both species feed on decaying wood. We found the first evidence for endogenous beta-1,4-endoglucanase in the beetle, plus evidence for microbial cellobiase, suggesting the beetle can degrade cellulose together with its gut microfauna. A number of antimicrobial peptides are expressed, particularly by the fat body but also by the midgut and hindgut. Conclusions This transcriptome provides a wealth of data about the species’ defense against chemical and biological threats, has uncovered several potentially new species of microbial symbionts, and significantly expands our knowledge about this pest.


Parasitology ◽  
2014 ◽  
Vol 142 (S1) ◽  
pp. S71-S84 ◽  
Author(s):  
DAVID McK. BIRD ◽  
JOHN T. JONES ◽  
CHARLES H. OPPERMAN ◽  
TAISEI KIKUCHI ◽  
ETIENNE G. J. DANCHIN

SUMMARYPlant-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.


Nematology ◽  
2015 ◽  
Vol 17 (1) ◽  
pp. 1-9 ◽  
Author(s):  
Sebastian Eves-van den Akker ◽  
Catherine J. Lilley ◽  
John T. Jones ◽  
Peter E. Urwin

Several structures associated with feeding by plant-parasitic nematodes have been described using two terms, feeding tubes and feeding plugs. However, both of these terms encompass multiple structures of independent evolution, some of which are functionally distinct. We have reviewed the literature on both structures and provide a new perspective on the function of intracellular feeding tubes to maintain the integrity and efficacy of the feeding site. We propose that they provide sufficient hydraulic resistance against the feeding site pressure to prevent it from collapsing during feeding. In addition, we propose that extracellular feeding tubes of migratory ectoparasites should be considered as the functional analogue of the stylet of all other plant-parasitic nematodes for withdrawal of host cell cytoplasm and, therefore, provide an example of convergent evolution. We also suggest that the main role of the feeding plug, irrespective of origin or composition, may be in adhesion.


Parasitology ◽  
1996 ◽  
Vol 113 (6) ◽  
pp. 589-597 ◽  
Author(s):  
R. H. C. Curtis

SUMMARYSecretions of plant-parasitic nematodes which are released into plant tissue may play critical roles in plant-nematode interactions. The identification and characterization of these molecules are of fundamental importance and may help to facilitate the development of novel strategies to interfere with nematode infection of plants and thereby decrease nematode-induced damage to crops. An antibody-based approach was used to isolate molecules present on the nematode surface and in nematode secretions. Monoclonal antibodies (MAbs) were produced to secretions and to whole Heterodera avenue 2nd-stage juveniles; several of these MAbs recognized molecules present in nematode secretions produced in vitro. Three of these molecules have been partly characterized in H. avenae, Globodera rostochiensis, G. pallida and Meloidogyne incognita. A MAb reacting with the surfaces of these nematodes recognized antigens of different molecular weight in each of the species tested. This difference in antigenicity might be related to specific functions in these nematodes. Preliminary results show that this antibody also localized the antigen in root cells surrounding the feeding site induced by M. incognita in Arabidopsis thaliana.


2010 ◽  
Vol 37 (10) ◽  
pp. 933 ◽  
Author(s):  
Samira Hassan ◽  
Carolyn A. Behm ◽  
Ulrike Mathesius

Plant parasitic nematodes infect the roots of a wide range of host plants. Migratory endo- or ectoparasites feed off the roots temporarily, but sedentary endoparasites are biotrophic parasites that invade roots and establish a permanent feeding site by re-directing root cell development. Feeding sites develop after injection of nematode effectors into plant cells through a stylet. In this review, we concentrate on several recently-identified effectors and discuss their possible functions in re-directing root cell development. We give examples of effectors that regulate host gene expression, interact with specific host proteins or mimic plant signalling molecules.


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