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flp-32 Ligand/receptor silencing phenocopy faster plant pathogenic nematodes.

Atkinson LE, Stevenson M, McCoy CJ, Marks NJ, Fleming C, Zamanian M, Day TA, Kimber MJ, Maule AG, Mousley A - PLoS Pathog. (2013)

Bottom Line: This study investigates the role of flp-32 in G. pallida and shows that: (i) Gp-flp-32 encodes the peptide AMRNALVRFamide; (ii) Gp-flp-32 is expressed in the brain and ventral nerve cord of G. pallida; (iii) migration rate increases in Gp-flp-32-silenced worms; (iv) the ability of G. pallida to infect potato plant root systems is enhanced in Gp-flp-32-silenced worms; (v) a novel putative Gp-flp-32 receptor (Gp-flp-32R) is expressed in G. pallida; and, (vi) Gp-flp-32R-silenced worms also display an increase in migration rate.This work demonstrates that Gp-flp-32 plays an intrinsic role in the modulation of locomotory behaviour in G. pallida and putatively interacts with at least one novel G-protein coupled receptor (Gp-flp-32R).This is the first functional characterisation of a parasitic nematode FLP-GPCR.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biosciences-Parasitology, Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast, Belfast, United Kingdom.

ABSTRACT
Restrictions on nematicide usage underscore the need for novel control strategies for plant pathogenic nematodes such as Globodera pallida (potato cyst nematode) that impose a significant economic burden on plant cultivation activities. The nematode neuropeptide signalling system is an attractive resource for novel control targets as it plays a critical role in sensory and motor functions. The FMRFamide-like peptides (FLPs) form the largest and most diverse family of neuropeptides in invertebrates, and are structurally conserved across nematode species, highlighting the utility of the FLPergic system as a broad-spectrum control target. flp-32 is expressed widely across nematode species. This study investigates the role of flp-32 in G. pallida and shows that: (i) Gp-flp-32 encodes the peptide AMRNALVRFamide; (ii) Gp-flp-32 is expressed in the brain and ventral nerve cord of G. pallida; (iii) migration rate increases in Gp-flp-32-silenced worms; (iv) the ability of G. pallida to infect potato plant root systems is enhanced in Gp-flp-32-silenced worms; (v) a novel putative Gp-flp-32 receptor (Gp-flp-32R) is expressed in G. pallida; and, (vi) Gp-flp-32R-silenced worms also display an increase in migration rate. This work demonstrates that Gp-flp-32 plays an intrinsic role in the modulation of locomotory behaviour in G. pallida and putatively interacts with at least one novel G-protein coupled receptor (Gp-flp-32R). This is the first functional characterisation of a parasitic nematode FLP-GPCR.

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Globodera pallida flp-32 (Gp-flp-32) encodes a single peptide (AMRNALVRFG) and is expressed in at least 16 nematode species.Gp-flp-32 encodes one FMRFamide-like peptide, AMRNALVRFG (highlighted in yellow; A), flanked by dibasic cleavage sites (KK/KR; highlighted in green; A), and preceded by a predicted 28 amino acid N-terminal signal peptide (underlined; A). At least 16 nematode species from clades IV (species boxed in blue) and V (species boxed in red) express flp-32, encoding the single highly conserved AMRNA/SLVRFG FLP-32 peptide (highlighted in yellow; B), flanked by conserved dibasic cleavage sites (KK/KR; highlighted in green; B). B. xylophilis: Bursaphelenchus xylophilus; G. pallida: Globodera pallida; G. rostochiensis: Globodera rostochiensis; M. hapla: Meloidogyne hapla; M. incognita: Meloidogyne incognita; M. paranaensis: Meloidogyne paranaensis; R. similis: Radopholus similis; S. ratti: Strongyloides ratti; A. caninum: Ancylostoma caninum; A. cantonensis: Ancylostoma cantonensis; A. ceylanicum; Ancylostoma ceylanicum; C. elegans: Caenorhabditis elegans; H. polygyrus: Heligmosomoides polygyrus; N. americanus: Necator americanus; N. brasiliensis: Nippostrongylus brasiliensis; T. circumcincta: Teladorsagia circumcincta.
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ppat-1003169-g001: Globodera pallida flp-32 (Gp-flp-32) encodes a single peptide (AMRNALVRFG) and is expressed in at least 16 nematode species.Gp-flp-32 encodes one FMRFamide-like peptide, AMRNALVRFG (highlighted in yellow; A), flanked by dibasic cleavage sites (KK/KR; highlighted in green; A), and preceded by a predicted 28 amino acid N-terminal signal peptide (underlined; A). At least 16 nematode species from clades IV (species boxed in blue) and V (species boxed in red) express flp-32, encoding the single highly conserved AMRNA/SLVRFG FLP-32 peptide (highlighted in yellow; B), flanked by conserved dibasic cleavage sites (KK/KR; highlighted in green; B). B. xylophilis: Bursaphelenchus xylophilus; G. pallida: Globodera pallida; G. rostochiensis: Globodera rostochiensis; M. hapla: Meloidogyne hapla; M. incognita: Meloidogyne incognita; M. paranaensis: Meloidogyne paranaensis; R. similis: Radopholus similis; S. ratti: Strongyloides ratti; A. caninum: Ancylostoma caninum; A. cantonensis: Ancylostoma cantonensis; A. ceylanicum; Ancylostoma ceylanicum; C. elegans: Caenorhabditis elegans; H. polygyrus: Heligmosomoides polygyrus; N. americanus: Necator americanus; N. brasiliensis: Nippostrongylus brasiliensis; T. circumcincta: Teladorsagia circumcincta.

Mentions: flp-32 is expressed in at least 16 nematode species where it encodes a highly conserved peptide with a characteristic VRFamide C-terminal motif, AMRN(A/S)LVRFG (see Fig. 1B). Previous interrogation of G. pallida ESTs [11] identified a transcript encoding a putative FLP-32-like peptide (GenBank accession number CV578361), which was used in this study to aid PCR confirmation of the full length Gp-flp-32 transcript. Primers designed to confirm the open reading frame of Gp-flp-32 generated a 321 nucleotide cDNA sequence (GenBank accession number JQ685131), encoding a 107 amino acid (aa) protein (Fig. 1A). The confirmed Gp-flp-32 aa sequence encodes a single copy of the FLP-32 peptide, AMRNALVRFG, flanked at both ends by dibasic residues (KK/KR), and a 28 aa signal peptide (see Fig. 1A; [16]). Further interrogation of the G. pallida EST database (GenBank) and genome assembly (Wellcome Trust Sanger Institute, G. pallida November 2010 supercontig assembly) in April-August 2011 did not reveal additional AMRNALVRFG encoding transcripts.


flp-32 Ligand/receptor silencing phenocopy faster plant pathogenic nematodes.

Atkinson LE, Stevenson M, McCoy CJ, Marks NJ, Fleming C, Zamanian M, Day TA, Kimber MJ, Maule AG, Mousley A - PLoS Pathog. (2013)

Globodera pallida flp-32 (Gp-flp-32) encodes a single peptide (AMRNALVRFG) and is expressed in at least 16 nematode species.Gp-flp-32 encodes one FMRFamide-like peptide, AMRNALVRFG (highlighted in yellow; A), flanked by dibasic cleavage sites (KK/KR; highlighted in green; A), and preceded by a predicted 28 amino acid N-terminal signal peptide (underlined; A). At least 16 nematode species from clades IV (species boxed in blue) and V (species boxed in red) express flp-32, encoding the single highly conserved AMRNA/SLVRFG FLP-32 peptide (highlighted in yellow; B), flanked by conserved dibasic cleavage sites (KK/KR; highlighted in green; B). B. xylophilis: Bursaphelenchus xylophilus; G. pallida: Globodera pallida; G. rostochiensis: Globodera rostochiensis; M. hapla: Meloidogyne hapla; M. incognita: Meloidogyne incognita; M. paranaensis: Meloidogyne paranaensis; R. similis: Radopholus similis; S. ratti: Strongyloides ratti; A. caninum: Ancylostoma caninum; A. cantonensis: Ancylostoma cantonensis; A. ceylanicum; Ancylostoma ceylanicum; C. elegans: Caenorhabditis elegans; H. polygyrus: Heligmosomoides polygyrus; N. americanus: Necator americanus; N. brasiliensis: Nippostrongylus brasiliensis; T. circumcincta: Teladorsagia circumcincta.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585147&req=5

ppat-1003169-g001: Globodera pallida flp-32 (Gp-flp-32) encodes a single peptide (AMRNALVRFG) and is expressed in at least 16 nematode species.Gp-flp-32 encodes one FMRFamide-like peptide, AMRNALVRFG (highlighted in yellow; A), flanked by dibasic cleavage sites (KK/KR; highlighted in green; A), and preceded by a predicted 28 amino acid N-terminal signal peptide (underlined; A). At least 16 nematode species from clades IV (species boxed in blue) and V (species boxed in red) express flp-32, encoding the single highly conserved AMRNA/SLVRFG FLP-32 peptide (highlighted in yellow; B), flanked by conserved dibasic cleavage sites (KK/KR; highlighted in green; B). B. xylophilis: Bursaphelenchus xylophilus; G. pallida: Globodera pallida; G. rostochiensis: Globodera rostochiensis; M. hapla: Meloidogyne hapla; M. incognita: Meloidogyne incognita; M. paranaensis: Meloidogyne paranaensis; R. similis: Radopholus similis; S. ratti: Strongyloides ratti; A. caninum: Ancylostoma caninum; A. cantonensis: Ancylostoma cantonensis; A. ceylanicum; Ancylostoma ceylanicum; C. elegans: Caenorhabditis elegans; H. polygyrus: Heligmosomoides polygyrus; N. americanus: Necator americanus; N. brasiliensis: Nippostrongylus brasiliensis; T. circumcincta: Teladorsagia circumcincta.
Mentions: flp-32 is expressed in at least 16 nematode species where it encodes a highly conserved peptide with a characteristic VRFamide C-terminal motif, AMRN(A/S)LVRFG (see Fig. 1B). Previous interrogation of G. pallida ESTs [11] identified a transcript encoding a putative FLP-32-like peptide (GenBank accession number CV578361), which was used in this study to aid PCR confirmation of the full length Gp-flp-32 transcript. Primers designed to confirm the open reading frame of Gp-flp-32 generated a 321 nucleotide cDNA sequence (GenBank accession number JQ685131), encoding a 107 amino acid (aa) protein (Fig. 1A). The confirmed Gp-flp-32 aa sequence encodes a single copy of the FLP-32 peptide, AMRNALVRFG, flanked at both ends by dibasic residues (KK/KR), and a 28 aa signal peptide (see Fig. 1A; [16]). Further interrogation of the G. pallida EST database (GenBank) and genome assembly (Wellcome Trust Sanger Institute, G. pallida November 2010 supercontig assembly) in April-August 2011 did not reveal additional AMRNALVRFG encoding transcripts.

Bottom Line: This study investigates the role of flp-32 in G. pallida and shows that: (i) Gp-flp-32 encodes the peptide AMRNALVRFamide; (ii) Gp-flp-32 is expressed in the brain and ventral nerve cord of G. pallida; (iii) migration rate increases in Gp-flp-32-silenced worms; (iv) the ability of G. pallida to infect potato plant root systems is enhanced in Gp-flp-32-silenced worms; (v) a novel putative Gp-flp-32 receptor (Gp-flp-32R) is expressed in G. pallida; and, (vi) Gp-flp-32R-silenced worms also display an increase in migration rate.This work demonstrates that Gp-flp-32 plays an intrinsic role in the modulation of locomotory behaviour in G. pallida and putatively interacts with at least one novel G-protein coupled receptor (Gp-flp-32R).This is the first functional characterisation of a parasitic nematode FLP-GPCR.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biosciences-Parasitology, Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast, Belfast, United Kingdom.

ABSTRACT
Restrictions on nematicide usage underscore the need for novel control strategies for plant pathogenic nematodes such as Globodera pallida (potato cyst nematode) that impose a significant economic burden on plant cultivation activities. The nematode neuropeptide signalling system is an attractive resource for novel control targets as it plays a critical role in sensory and motor functions. The FMRFamide-like peptides (FLPs) form the largest and most diverse family of neuropeptides in invertebrates, and are structurally conserved across nematode species, highlighting the utility of the FLPergic system as a broad-spectrum control target. flp-32 is expressed widely across nematode species. This study investigates the role of flp-32 in G. pallida and shows that: (i) Gp-flp-32 encodes the peptide AMRNALVRFamide; (ii) Gp-flp-32 is expressed in the brain and ventral nerve cord of G. pallida; (iii) migration rate increases in Gp-flp-32-silenced worms; (iv) the ability of G. pallida to infect potato plant root systems is enhanced in Gp-flp-32-silenced worms; (v) a novel putative Gp-flp-32 receptor (Gp-flp-32R) is expressed in G. pallida; and, (vi) Gp-flp-32R-silenced worms also display an increase in migration rate. This work demonstrates that Gp-flp-32 plays an intrinsic role in the modulation of locomotory behaviour in G. pallida and putatively interacts with at least one novel G-protein coupled receptor (Gp-flp-32R). This is the first functional characterisation of a parasitic nematode FLP-GPCR.

Show MeSH
Related in: MedlinePlus