The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

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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A Root-Knot Nematode Secretory Peptide Functions as a Ligand for a Plant Transcription Factor

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-0463 ◽

2006 ◽

Vol 19 (5) ◽

pp. 463-470 ◽

Cited By ~ 143

Author(s):

Guozhong Huang ◽

Ruihua Dong ◽

Rex Allen ◽

Eric L. Davis ◽

Thomas J. Baum ◽

...

Keyword(s):

Regulatory Protein ◽

Direct Interaction ◽

Giant Cells ◽

Root Knot Nematode ◽

Root Cells ◽

Host Interaction ◽

Nematode Parasitism ◽

Parasitism Genes

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.

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The mechanism of mouse egg-cylinder morphogenesis in vitro

Development ◽

10.1242/dev.61.1.277 ◽

1981 ◽

Vol 61 (1) ◽

pp. 277-287

Author(s):

A. J. Copp

Keyword(s):

Giant Cell ◽

Cell Formation ◽

Cell Movement ◽

Giant Cells ◽

Cell Number ◽

Dependent Change ◽

Morphogenesis In Vitro ◽

Trophoblast Giant Cells

The number of trophoblast giant cells in outgrowths of mouse blastocysts was determined before, during and after egg-cylinder formation in vitro. Giant-cell numbers rose initially but reached a plateau 12 h before the egg cylinder appeared. A secondary increase began 24 h after egg-cylinder formation. Blastocysts whose mural trophectoderm cells were removed before or shortly after attachment in vitro formed egg cylinders at the same time as intact blastocysts but their trophoblast outgrowths contained fewer giant cells at this time. The results support the idea that egg-cylinder formation in vitro is accompanied by a redirection of the polar to mural trophectoderm cell movement which characterizes blastocysts before implantation. The resumption of giant-cell number increase in trophoblast outgrowths after egg-cylinder formation may correspond to secondary giant-cell formation in vivo. It is suggested that a time-dependent change in the strength of trophoblast cell adhesion to the substratum occurs after blastocyst attachment in vitro which restricts the further entry of polar cells into the outgrowth and therefore results in egg-cylinder formation.

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The biochemistry of differentiation of mouse trophoblast: studies on polyploidy

Development ◽

10.1242/dev.27.2.447 ◽

1972 ◽

Vol 27 (2) ◽

pp. 447-465

Author(s):

Peter W. Barlow ◽

Michael I. Sherman

Keyword(s):

Giant Cell ◽

Zona Pellucida ◽

Giant Cells ◽

In Utero ◽

Cell Nuclei ◽

Maternal Environment ◽

Ploidy Levels

1. Trophoblast development in utero in the first half of gestation is accompanied by a rise in the ploidy levels in giant cell nuclei. Giant cells constitute up to one-third of the trophoblast population over this period. 2. The expression of polyploidy is independent of the maternal environment; the extent of polyploidy and the degree to which trophoblast develops morphologically under various conditions appear to be related. 3. The following events are not necessary for the initiation of polyploidization in trophoblast: (a) hatching from the zona pellucida, (b) oestrogen sensitization, (c) implantation, (d) postimplantation changes in topology. 4. That earlier developmental events such as the formation of the blastocoel cavity may in some way trigger polyploidization of trophoblast is not inconsistent with the studies described.

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Pyrrolizidine alkaloids of Chromolaena odorata act as nematicidal agents and reduce infection of lettuce roots by Meloidogyne incognita

Nematology ◽

10.1163/156854107781352016 ◽

2007 ◽

Vol 9 (3) ◽

pp. 343-349 ◽

Cited By ~ 18

Author(s):

Michael Boppré ◽

Tim Thoden ◽

Johannes Hallmann

Keyword(s):

Meloidogyne Incognita ◽

Pyrrolizidine Alkaloids ◽

Invasive Weeds ◽

Chromolaena Odorata ◽

Root Knot Nematode ◽

In Vivo Experiments ◽

Valuable Element ◽

Plant Compounds

Abstract1,2-dehydropyrrolizidine alkaloids (PAs) represent a class of secondary plant compounds that are active in defence against herbivory. They are present in Chromolaena odorata, one of the most invasive weeds of Asia and Africa. In vitro studies demonstrate that pure PAs from C. odorata roots have nematicidal effects on the root-knot nematode Meloidogyne incognita, even at concentrations of 70-350 ppm. In vivo experiments show that mulch or aqueous crude extracts from C. odorata roots reduce the infection of lettuce by M. incognita. Thus, the use of PA-containing plants appears to be a valuable element for integrated nematode management.

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Biocontrol potential of Lysobacter antibioticus HS124 against the root-knot nematode, Meloidogyne incognita, causing disease in tomato

Nematology ◽

10.1163/15685411-00002700 ◽

2013 ◽

Vol 15 (5) ◽

pp. 545-555 ◽

Cited By ~ 14

Author(s):

Yong Seong Lee ◽

Muhammad Anees ◽

Hae Nam Hyun ◽

Kil Yong Kim

Keyword(s):

Meloidogyne Incognita ◽

Bacterial Strain ◽

Tap Water ◽

Nematicidal Activity ◽

Root Knot Nematode ◽

Lytic Enzymes ◽

Pot Experiments ◽

Hydroxyphenylacetic Acid

Lysobacter antibioticus HS124 is an antagonistic bacterial strain that was previously isolated from the rhizosphere soil of pepper and showed an enhanced ability to produce lytic enzymes as well as an antibiotic that was identified as 4-hydroxyphenylacetic acid (4-HPAA). In the present study, nematicidal activity of the strain and 4-HPAA against the root-knot nematode, Meloidogyne incognita, causing disease in tomato was investigated in both in vitro and in vivo conditions. For this purpose, adding different concentrations of culture filtrate, crude extract collected from extraction with ethyl acetate and 4-HPAA, in 24-well plates containing ca 500 eggs or 300 second-stage juveniles (J2), significantly decreased the rate of nematode hatch and caused higher mortality of J2 compared with the control treatments. Nematicidal activity of the bacterial strain was further confirmed by conducting pot experiments in which tomato plants were inoculated with M. incognita and the HS124 culture (BC). The control pots were treated with commercial nematicide (CN, 5% Ethoprophos), tap water (TW) or the non-inoculated bacterial culture medium (BCM). In these pot experiments, results demonstrated a strong antagonistic potential of L. antibioticus HS124 against M. incognita where the disease was significantly reduced in the pots treated with BC as compared to TW or BCM. Furthermore, the shoot fresh weight was also increased significantly, which may be attributed to the disease control ability of the strain. Hence, L. antibioticus HS124 may be further developed as a potential biocontrol of root knot nematode in the field.

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Concentration of β-ecydisone (20E) in susceptible and resistant accessions of Pfaffia glomerata infected with Meloidogyne incognita and histological characterisation of resistance

Nematology ◽

10.1163/138855409x12597616267771 ◽

2010 ◽

Vol 12 (5) ◽

pp. 701-709 ◽

Cited By ~ 8

Author(s):

Ana Cristina M.M. Gomes ◽

Michel Nicole ◽

Jean Kleber Mattos ◽

Sarazete Izidia Vaz Pereira ◽

Paulo Pereira ◽

...

Keyword(s):

Meloidogyne Incognita ◽

Uv Light ◽

Pearson Correlation ◽

Resistance Mechanism ◽

Giant Cells ◽

Resistance Mechanisms ◽

Root Production ◽

Limiting Factor ◽

Root Knot Nematode ◽

Pfaffia Glomerata

Abstract Pfaffia glomerata is a medicinal plant widely distributed in Brazil, which is considered the world's greatest supplier of P. glomerata roots. Among active ingredients contained in this plant, the steroid β-ecydisone (20E) is the most important compound extracted from roots. This steroid presents therapeutic properties for the treatment of diabetes and haemorrhoids, besides having bioenergy, tonic and aphrodisiac effects. The root-knot nematode Meloidogyne spp. is a major limiting factor in root production. Recent studies showed resistance of accessions of P. glomerata to Meloidogyne incognita. The aims of this work were: i) to correlate the concentration of 20E with resistance and susceptibility of P. glomerata accessions to M. incognita in inoculated and non-inoculated plants; ii) to study the effect of the parasitism of M. incognita on the concentration of the steroid 20E in the roots; and iii) to clarify resistance mechanisms by comparing the response of a highly resistant UFV with a highly susceptible accession (Farm) to nematode infection. The concentration of 20E in the healthy susceptible Farm accession was significantly higher than in the healthy resistant UFV accession, showing that the resistance mechanism was not related to 20E concentrations. Plants of the Farm accession infected with M. incognita showed higher levels of 20E than the non-infected control. A positive and significant Pearson correlation coefficient was observed between 20E concentrations and gall indexes. Resistance of UFV to the root-knot nematode M. incognita was associated with unidentified factors that limited nematode penetration or emigration of second-stage juveniles and with post-penetration responses, including the hypersensitive response. Giant cells were sometimes found in the resistant cultivar, but displayed a highly vacuolated and degraded cytoplasm with thinner cell walls than those induced in the susceptible accession. Microscope observations under UV light showed a strong autofluorescence, suggesting that phenolic compounds may be involved in ginseng UFV resistance.

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Root-Knot Nematode Parasitism Suppresses Host RNA Silencing

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-08-16-0160-r ◽

2017 ◽

Vol 30 (4) ◽

pp. 295-300 ◽

Cited By ~ 4

Author(s):

E. Walsh ◽

J. M. Elmore ◽

C. G. Taylor

Keyword(s):

Rna Silencing ◽

Plant Pathogens ◽

Giant Cells ◽

Root Knot Nematode ◽

Root Cells ◽

Feeding Site ◽

Nematode Parasitism ◽

Silencing Pathways ◽

Plant Pathosystems ◽

Viral Suppressors

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.

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Investigating the in vitro and in vivo nematicidal performance of structurally related macrolides against the root-knot nematode, Meloidogyne incognita

Hellenic Plant Protection Journal ◽

10.2478/hppj-2019-0005 ◽

2019 ◽

Vol 12 (1) ◽

pp. 24-37

Author(s):

M.A. Radwan ◽

A.S.A. Saad ◽

H.A. Mesbah ◽

H.S. Ibrahim ◽

M.S. Khalil

Keyword(s):

Meloidogyne Incognita ◽

Root Length ◽

Egg Mass ◽

Root Knot Nematode ◽

Egg Hatching ◽

Shoot Height ◽

Egg Masses ◽

New Family

Summary Avermectins and spinosyns are structurally related natural products of microbial origin and belong to a new family of macrolides which are active against a vast array of invertebrate pests. In the present study, the effects of four members of macrolides; abamectin (ABM), emamectin benzoate (EMB), spinosad (SPI) and spinetoram (SPIT), on Meloidogyne incognita were investigated under in vitro and in vivo conditions. All compounds reduced egg hatching and led to high mortality of the nematode second-stage juveniles (J2). ABM showed the maximum rate of egg hatching inhibition and J2 mortality while SPIT recorded the minimum. All treatments reduced the number of galls, egg masses, eggs/egg mass in roots and J2 in the soil when compared to the control. Based on the 10 folds of the 24 h-LC50 values of J2 mortality in vitro, EMB and ABM exhibited higher percent reduction in galls (79.68 and 71.45%), egg masses (75.19 and 70.54%), eggs/egg mass (60.49 and 40.91%) and J2 in the soil (90.31 and 86.54%), respectively, compared to SPI and SPIT. Significant increase in tomato shoot height occurred in all biopesticides (10 folds) and SPIT (20 folds). SPI at 10 folds of the 24 h-LC50 values of J2 mortality in vitro, significantly increased root length while ABM at 50 folds and SPIT at 20 folds decreased root length by 5.15% and 5.88%, respectively, compared to the untreated inoculated plants. In all treatments, the dry shoot and root weights increased, compared to the untreated control. Our findings suggest that these macrolides have the ability to regulate nematode population densities and may be an alternative to classical nematicides.

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Chitosan Oligosaccharide Fluorinated Derivative Control Root-Knot Nematode (Meloidogyne incognita) Disease Based on the Multi-Efficacy Strategy

Marine Drugs ◽

10.3390/md18050273 ◽

2020 ◽

Vol 18 (5) ◽

pp. 273 ◽

Cited By ~ 1

Author(s):

Zhaoqian Fan ◽

Yukun Qin ◽

Song Liu ◽

Ronge Xing ◽

Huahua Yu ◽

...

Keyword(s):

Meloidogyne Incognita ◽

Plant Root ◽

Photosynthetic Pigment ◽

Good Control ◽

Chitosan Oligosaccharide ◽

Root Knot Nematode ◽

Control Effect ◽

Low Cytotoxicity

Plant root-knot nematode disease is a great agricultural problem and commercially available nematicides have the disadvantages of high toxicity and limited usage; thus, it is urgent to develop new nematicides derived from nature substances. In this study, a novel fluorinated derivative was synthesized by modifying chitosan oligosaccharide (COS) using the strategy of multiple functions. The derivatives were characterized by FTIR, NMR, elemental analysis, and TG/DTG. The activity assays show that the derivatives can effectively kill the second instar larvae of Meloidogyne incognita in vitro, among them, chitosan-thiadiazole-trifluorobutene (COSSZFB) perform high eggs hatching inhibitory activity. The derivatives can regulate plant growth (photosynthetic pigment), improve immunity (chitinase and β-1,3-glucanase), and show low cytotoxicity and phytotoxicity. According to the multi-functional activity, the derivatives exhibit a good control effect on plant root-knot nematode disease in vivo. The results demonstrate that the COS derivatives (especially fluorinated derivative) perform multiple activities and show the potential to be further evaluated as nematicides.

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Differentiation of Trophoblast Giant Cells and Their Metabolic Functions Are Dependent on Peroxisome Proliferator-Activated Receptor β/δ

Molecular and Cellular Biology ◽

10.1128/mcb.26.8.3266-3281.2006 ◽

2006 ◽

Vol 26 (8) ◽

pp. 3266-3281 ◽

Cited By ~ 142

Author(s):

Karim Nadra ◽

Silvia I. Anghel ◽

Elisabeth Joye ◽

Nguan Soon Tan ◽

Sharmila Basu-Modak ◽

...

Keyword(s):

Cell Differentiation ◽

Giant Cell ◽

Giant Cells ◽

Peroxisome Proliferator ◽

Phosphatidylinositol 3 Kinase ◽

Peroxisome Proliferator Activated Receptor ◽

Metabolic Functions ◽

Integrin Linked Kinase ◽

Trophoblast Giant Cells

ABSTRACT Mutation of the nuclear receptor peroxisome proliferator-activated receptor β/δ (PPARβ/δ) severely affects placenta development, leading to embryonic death at embryonic day 9.5 (E9.5) to E10.5 of most, but not all, PPARβ/δ-null mutant embryos. While very little is known at present about the pathway governed by PPARβ/δ in the developing placenta, this paper demonstrates that the main alteration of the placenta of PPARβ/δ-null embryos is found in the giant cell layer. PPARβ/δ activity is in fact essential for the differentiation of the Rcho-1 cells in giant cells, as shown by the severe inhibition of differentiation once PPARβ/δ is silenced. Conversely, exposure of Rcho-1 cells to a PPARβ/δ agonist triggers a massive differentiation via increased expression of 3-phosphoinositide-dependent kinase 1 and integrin-linked kinase and subsequent phosphorylation of Akt. The links between PPARβ/δ activity in giant cells and its role on Akt activity are further strengthened by the remarkable pattern of phospho-Akt expression in vivo at E9.5, specifically in the nucleus of the giant cells. In addition to this phosphatidylinositol 3-kinase/Akt main pathway, PPARβ/δ also induced giant cell differentiation via increased expression of I-mfa, an inhibitor of Mash-2 activity. Finally, giant cell differentiation at E9.5 is accompanied by a PPARβ/δ-dependent accumulation of lipid droplets and an increased expression of the adipose differentiation-related protein (also called adipophilin), which may participate to lipid metabolism and/or steroidogenesis. Altogether, this important role of PPARβ/δ in placenta development and giant cell differentiation should be considered when contemplating the potency of PPARβ/δ agonist as therapeutic agents of broad application.

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