scholarly journals Root-Knot Nematode Parasitism Suppresses Host RNA Silencing

2017 ◽  
Vol 30 (4) ◽  
pp. 295-300 ◽  
Author(s):  
E. Walsh ◽  
J. M. Elmore ◽  
C. G. Taylor

Root-knot nematodes damage crops around the world by developing complex feeding sites from normal root cells of their hosts. The ability to initiate and maintain this feeding site (composed of individual “giant cells”) is essential to their parasitism process. RNA silencing pathways in plants serve a diverse set of functions, from directing growth and development to defending against invading pathogens. Influencing a host’s RNA silencing pathways as a pathogenicity strategy has been well-documented for viral plant pathogens, but recently, it has become clear that silencing pathways also play an important role in other plant pathosystems. To determine if RNA silencing pathways play a role in nematode parasitism, we tested the susceptibility of plants that express a viral suppressor of RNA silencing. We observed an increase in susceptibility to nematode parasitism in plants expressing viral suppressors of RNA silencing. Results from studies utilizing a silenced reporter gene suggest that active suppression of RNA silencing pathways may be occurring during nematode parasitism. With these studies, we provide further evidence to the growing body of plant-biotic interaction research that suppression of RNA silencing is important in the successful interaction between a plant-parasitic animal and its host.

2013 ◽  
Vol 26 (1) ◽  
pp. 44-54 ◽  
Author(s):  
Heather H. Marella ◽  
Erik Nielsen ◽  
Daniel P. Schachtman ◽  
Christopher G. Taylor

The root-knot nematode, Meloidogyne incognita, is an obligate parasite which depends entirely on the host plant for its nutrition. Root-knot nematodes induce the formation of a highly specialized feeding site consisting of several giant cells surrounded by a network of vascular tissues. Nutrients, including amino acids and sugars, are transferred apoplastically from the vascular tissues to the feeding site. Using Arabidopsis thaliana lacking the vascular-expressed amino acid permeases (AAP) AAP3 or AAP6, we demonstrate that disruption of amino acid transport can affect nematode parasitism. Nematode infestation levels are significantly reduced on the aap3 and aap6 mutants. AAP3 and AAP6 act distinctly in the transport of amino acids to the feeding site, as demonstrated by differences in their carrying capacity profiles. Furthermore, analyses of promoter: β-glucuronidase lines show different expression patterns for AAP3 and AAP6 in infected roots. In the aap3-3 mutant, part of the decrease in infestation is connected to a defect in early infection, where juveniles enter but then leave the root. Both aap3-3 and aap6-1 produce fewer females and produce more adult male nematodes. Additionally, detrimental effects are observed in the nematodes harvested from aap3-3 and aap6-1 mutants, including decreased egg hatching and infectivity and lower levels of lipid reserves. The transport of amino acids by AAP3 and AAP6 is important for nematode infection and success of the progeny.


2006 ◽  
Vol 19 (5) ◽  
pp. 463-470 ◽  
Author(s):  
Guozhong Huang ◽  
Ruihua Dong ◽  
Rex Allen ◽  
Eric L. Davis ◽  
Thomas J. Baum ◽  
...  

Parasitism genes expressed in the esophageal gland cells of root-knot nematodes encode proteins that are secreted into host root cells to transform the recipient cells into enlarged multinucleate feeding cells called giant-cells. Expression of a root-knot nematode parasitism gene which encodes a novel 13-amino-acid secretory peptide in plant tissues stimulated root growth. Two SCARECROW-like transcription factors of the GRAS protein family were identified as the putative targets for this bioactive nematode peptide in yeast two-hybrid analyses and confirmed by in vitro and in vivo coimmunoprecipitations. This discovery is the first demonstration of a direct interaction of a nematode-secreted parasitism peptide with a plant-regulatory protein, which may represent an early signaling event in the root-knot nematode-host interaction.


2020 ◽  
Vol 33 (3) ◽  
pp. 412-422
Author(s):  
Chao Zhang ◽  
Dong Chen ◽  
Guoyi Yang ◽  
Xiyuan Yu ◽  
Jianguo Wu

Viral suppressors of RNA silencing (VSRs) are a cluster of viral proteins that have evolved to counteract eukaryotic antiviral RNA silencing pathways, thereby contributing to viral pathogenicity. In this study, we revealed that the matrix protein P4 encoded by rice stripe mosaic virus (RSMV), which is an emerging cytoplasmic rhabdovirus, is a weak RNA silencing suppressor. By conducting yeast two-hybrid, bimolecular fluorescence complementation, and subcellular colocalization assays, we proved that P4 interacts with the rice endogenous suppressor of gene silencing 3 (OsSGS3). We also determined that P4 overexpression has no effect on OsSGS3 transcription. However, P4 can promote the degradation of OsSGS3 via ubiquitination and autophagy. Additionally, a potato virus X–based expression system was used to confirm that P4 enhances the development of mosaic symptoms on Nicotiana benthamiana leaves by promoting hydrogen peroxide accumulation but not cell death. To verify whether P4 is a pathogenicity factor in host plants, we generated transgenic P4-overexpressing rice plants that exhibited disease-related developmental defects including decreased plant height and excessive tillering. Our data suggest that RSMV-encoded P4 serves as a weak VSR that inhibits antiviral RNA silencing by targeting OsSGS3.


1999 ◽  
Vol 89 (12) ◽  
pp. 1138-1143 ◽  
Author(s):  
Yuji Oka ◽  
Yigal Cohen ◽  
Yitzhak Spiegel

Chemical inducers of pathogenesis-related proteins and plant resistance were applied to tomato plants, with the aim of inducing resistance to the root-knot nematode Meloidogyne javanica. Relative to control plants, foliar spray and soil-drenching with dl-β-amino-n-butyric acid (BABA) reduced root-galling 7 days after inoculation, as well as the number of eggs 30 days after inoculation. Other chemicals (α- and γ-amino-n-butyric acid, jasmonic acid, methyl jasmonate, and salicylic acid) were either phytotoxic to tomato plants or did not improve control of root-knot nematodes. Fewer second-stage juveniles invaded BABA-treated tomato roots, and root-galling indices were lower than in control tomato plants. Resistance phenomena in seedlings lasted at least 5 days after spraying with BABA. Nematodes invading the roots of BABA-treated seedlings induced small, vacuolate giant cells. Postinfection treatment of tomato plants with BABA inhibited nematode development. It is speculated that after BABA application tomato roots become less attractive to root-knot nematodes, physically harder to invade, or some substance(s) inhibiting nematode or nematode feeding-site development is produced in roots.


2005 ◽  
Vol 18 (12) ◽  
pp. 1277-1284 ◽  
Author(s):  
Stéphanie Jaubert ◽  
Adina L. Milac ◽  
Andrei J. Petrescu ◽  
Janice de Almeida-Engler ◽  
Pierre Abad ◽  
...  

Esophageal secretions from endoparasitic sedentary nematodes are thought to play key roles throughout plant parasitism, in particular during the invasion of the root tissue and the initiation and maintenance of the nematode feeding site (NFS) essential for nematode development. The secretion in planta of esophageal cell-wall-degrading enzymes by migratory juveniles has been shown, suggesting a role for these enzymes in the invasion phase. Nevertheless, the secretion of an esophageal gland protein into the NFS by nematode sedentary stages has never been demonstrated. The calreticulin Mi-CRT is a protein synthesized in the esophageal glands of the root-knot nematode Meloidogyne incognita. After three-dimensional modeling of the Mi-CRT protein, a surface peptide was selected to raise specific antibodies. In planta immunolocalization showed that Mi-CRT is secreted by migratory and sedentary stage nematodes, suggesting a role for Mi-CRT throughout parasitism. During the maintenance of the NFS, the secreted Mi-CRT was localized outside the nematode at the tip of the stylet. In addition, Mi-CRT accumulation was observed along the cell wall of the giant cells that compose the feeding site, providing evidence for a nematode esophageal protein secretion into the NFS.


2017 ◽  
Author(s):  
◽  
Carola M. De La Torre Cuba

Cyst and root-knot nematodes are obligate plant parasites of global economic importance with a remarkable ability to reprogram root cells into unique feeding sites. Previous studies have suggested a role for cytokinin in feeding site formation induced by these two types of nematodes, but the mechanistic details have not yet been described. Using Arabidopsis as a host plant species, this study shows a comparative analysis of cytokinin genes in response to the beet cyst nematode (BCN), Heterodera schachtii, and the root-knot nematode (RKN), Meloidogyne incognita. Distinct differences in the regulation of cytokinin biosynthesis, catabolism and signaling genes in response to BCN and RKN infection were found, suggesting differential manipulation of the cytokinin pathway by these two nematode species. Furthermore, key cytokinin genes contributing to BCN and RKN disease susceptibility were identified. This study also evaluated ARABIDOPSIS HISTIDINE KINASE (AHK), ahk2/3, ahk2/4 and ahk3/4 receptor mutant lines in response to BCN and RKN infection and found a decrease in susceptibility compared to the wild type control, Col-0. An analysis of ahk double mutants using CYCB1:GUS/ahk introgressed lines revealed contrasting differences in the cytokinin receptors controlling cell cycle activation in feeding sites caused by RKN and BCN. Results from these studies could be used in the future to engineer novel forms of nematode resistance in crops of economic importance.


2019 ◽  
Vol 20 (21) ◽  
pp. 5465 ◽  
Author(s):  
Christianna Meidani ◽  
Nikoletta G. Ntalli ◽  
Eleni Giannoutsou ◽  
Ioannis-Dimosthenis S. Adamakis

Meloidogyne incognita is a root knot nematode (RKN) species which is among the most notoriously unmanageable crop pests with a wide host range. It inhabits plants and induces unique feeding site structures within host roots, known as giant cells (GCs). The cell walls of the GCs undergo the process of both thickening and loosening to allow expansion and finally support nutrient uptake by the nematode. In this study, a comparative in situ analysis of cell wall polysaccharides in the GCs of wild-type Col-0 and the microtubule-defective fra2 katanin mutant, both infected with M. incognita has been carried out. The fra2 mutant had an increased infection rate. Moreover, fra2 roots exhibited a differential pectin and hemicellulose distribution when compared to Col-0 probably mirroring the fra2 root developmental defects. Features of fra2 GC walls include the presence of high-esterified pectic homogalacturonan and pectic arabinan, possibly to compensate for the reduced levels of callose, which was omnipresent in GCs of Col-0. Katanin severing of microtubules seems important in plant defense against M. incognita, with the nematode, however, to be nonchalant about this “katanin deficiency” and eventually induce the necessary GC cell wall modifications to establish a feeding site.


2013 ◽  
Vol 26 (1) ◽  
pp. 36-43 ◽  
Author(s):  
Rosane H. C. Curtis ◽  
Pankaj ◽  
Stephen J. Powers ◽  
Johnathan Napier ◽  
Michaela C. Matthes

We report that the F-box/Kelch-repeat protein At2g44130 is specifically induced by the root-knot nematode Meloidogyne incognita during the initial stages of the initiation and maintenance of the feeding site. In addition, we show that the expression of this gene promotes susceptibility of infection because knocking down the F-box gene (At2g44130) drastically reduces nematode attraction to and infection of roots. In contrast, F-box overexpressing (OE) lines had a hypersusceptible phenotype, with an increase of 34% in nematode attraction and 67% in nematode infection when grown in soil. This hypersusceptibility might be the result of an increased attraction of the second-stage juveniles toward root exudates of the F-box OE, which would suggest that the blend of compounds in the root exudates of the OE line was somewhat different from the ones present in the root exudates of the wild type and the F-box knockout and tilling lines. Although the function of the F-box/Kelch-repeat protein (At2g44130) is not known, we postulate that its activation by nematode effectors released during the infection process leads to the formation of SCF(At2g44130) (Skp1-Cullin1-F-box protein) complexes, which are involved in facilitating successful infection by the nematode through targeting specific proteins for degradation.


2021 ◽  
Vol 12 ◽  
Author(s):  
Nhat My Truong ◽  
Yongpan Chen ◽  
Joffrey Mejias ◽  
Salomé Soulé ◽  
Karine Mulet ◽  
...  

Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with Arabidopsis GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.


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