Online citations, reference lists, and bibliographies.
← Back to Search

Direct Identification Of The Meloidogyne Incognita Secretome Reveals Proteins With Host Cell Reprogramming Potential

Stéphane Bellafiore, Z. Shen, Marie-Noelle Rosso, P. Abad, Patrick Shih, S. Briggs
Published 2008 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
The root knot nematode, Meloidogyne incognita, is an obligate parasite that causes significant damage to a broad range of host plants. Infection is associated with secretion of proteins surrounded by proliferating cells. Many parasites are known to secrete effectors that interfere with plant innate immunity, enabling infection to occur; they can also release pathogen-associated molecular patterns (PAMPs, e.g., flagellin) that trigger basal immunity through the nematode stylet into the plant cell. This leads to suppression of innate immunity and reprogramming of plant cells to form a feeding structure containing multinucleate giant cells. Effectors have generally been discovered using genetics or bioinformatics, but M. incognita is non-sexual and its genome sequence has not yet been reported. To partially overcome these limitations, we have used mass spectrometry to directly identify 486 proteins secreted by M. incognita. These proteins contain at least segmental sequence identity to those found in our 3 reference databases (published nematode proteins; unpublished M. incognita ESTs; published plant proteins). Several secreted proteins are homologous to plant proteins, which they may mimic, and they contain domains that suggest known effector functions (e.g., regulating the plant cell cycle or growth). Others have regulatory domains that could reprogram cells. Using in situ hybridization we observed that most secreted proteins were produced by the subventral glands, but we found that phasmids also secreted proteins. We annotated the functions of the secreted proteins and classified them according to roles they may play in the development of root knot disease. Our results show that parasite secretomes can be partially characterized without cognate genomic DNA sequence. We observed that the M. incognita secretome overlaps the reported secretome of mammalian parasitic nematodes (e.g., Brugia malayi), suggesting a common parasitic behavior and a possible conservation of function between metazoan parasites of plants and animals.
This paper references
Reactive oxygen species signaling in response to pathogens. Plant physiology
MA Torres (2006)
The innate immune response to bacterial flagellin is mediated by Toll-like receptor
F Hayashi (2001)
10.1094/MPMI.2004.17.8.846
A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes.
T. Tytgat (2004)
10.1104/pp.106.079467
Reactive Oxygen Species Signaling in Response to Pathogens1
M. A. Torres (2006)
10.1146/ANNUREV.PY.27.090189.001011
Disease-Inducing Secretions of Plant-Parasitic Nematodes
R. Hussey (1989)
10.1101/GR.5646507
Improving gene annotation using peptide mass spectrometry.
S. Tanner (2007)
10.1105/tpc.104.023903
The Arabidopsis Transthyretin-Like Protein Is a Potential Substrate of BRASSINOSTEROID-INSENSITIVE 1
K. H. Nam (2004)
10.1094/MPMI.2003.16.8.720
The parasitome of the phytonematode Heterodera glycines.
B. Gao (2003)
10.1017/S0031182099004448
Direct analysis of the secretions of the potato cyst nematode Globodera rostochiensis.
L. Robertson (1999)
10.1105/tpc.105.035394
RNA Interference Identifies a Calcium-Dependent Protein Kinase Involved in Medicago truncatula Root Developmentw⃞
Sergey Ivashuta (2005)
10.1111/j.1364-3703.2007.00435.x
Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes.
Erwin Roze (2008)
10.1016/J.EXPPARA.2006.07.008
Meloidogyne incognita: molecular and biochemical characterisation of a cathepsin L cysteine proteinase and the effect on parasitism following RNAi.
J. Shingles (2007)
10.1093/embo-reports/kvd092
Finding nuclear localization signals
M. Cokol (2000)
10.1094/MPMI-19-0463
A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor.
G. Huang (2006)
10.1007/978-3-642-00646-3_8
The transthyretin-retinol-binding protein complex.
H. Monaco (2000)
10.1186/gb-2003-4-4-r26
Analysis and functional classification of transcripts from the nematode Meloidogyne incognita
J. McCarter (2002)
Nematode esophageal glands and plant protection
RS Hussey (2004)
10.1046/J.1432-1327.2000.01356.X
Biochemical characterization of MI-ENG1, a family 5 endoglucanase secreted by the root-knot nematode Meloidogyne incognita.
C. Béra-Maillet (2000)
Transport of ER vesicles on actin filaments in neurons by myosin V.
J. Tabb (1998)
10.1038/427030a
Plant degradation: A nematode expansin acting on plants
Ling Qin (2004)
10.1104/pp.106.086231
Modifications to the Arabidopsis Defense Proteome Occur Prior to Significant Transcriptional Change in Response to Inoculation with Pseudomonas syringae1[W][OA]
A. Jones (2006)
A method for staining nematode secretions and structures.
R. D. Riggs (1988)
10.1016/S0020-7519(02)00260-6
Protein disulphide isomerase of Ostertagia ostertagi: an excretory-secretory product of L4 and adult worms?
P. Geldhof (2003)
10.1023/A:1005930625920
Cloning of genes whose expression is correlated with mitosis and localized in dividing cells in root caps of Pisum sativum L.
H. Woo (2004)
Revised draft guidelines for proteomic data publication.
R. Bradshaw (2005)
Fine structure of the phasmid of 2nd-stage juveniles of heterodera schachtii (Tylenchida: Nematoda) Canadian
JG Baldwin (1985)
10.1111/J.1365-313X.2005.02532.X
Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis.
Fabien Jammes (2005)
10.1105/tpc.11.5.793
Molecular Markers and Cell Cycle Inhibitors Show the Importance of Cell Cycle Progression in Nematode-Induced Galls and Syncytia
J. de Almeida Engler (1999)
10.1094/MPMI.2003.16.5.376
A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita.
G. Huang (2003)
10.1023/A:1026556928624
Plant proteolytic enzymes: possible roles during programmed cell death
E. Beers (2004)
10.1016/J.IJPARA.2005.01.006
Developmental expression and molecular analysis of two Meloidogyne incognita pectate lyase genes.
G. Huang (2005)
10.1002/BIES.950100106
Proteinase inhibitor gene families: Strategies for transformation to improve plant defenses against herbivores
C. Ryan (1989)
10.1186/1471-2105-4-41
The COG database: an updated version includes eukaryotes
R. Tatusov (2003)
10.1016/S1357-2725(03)00213-9
The translationally controlled tumour protein (TCTP).
Ulrich-Axel Bommer (2004)
10.1016/J.MOLBIOPARA.2005.01.018
An aspartyl protease inhibitor of Ostertagia ostertagi: molecular cloning, analysis of stage and tissue specific expression and vaccine trial.
V. De Maere (2005)
10.1105/tpc.107.052332
An Ustilago maydis Gene Involved in H2O2 Detoxification Is Required for Virulence[W]
L. Molina (2007)
10.1021/BI0023089
Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: evidence for a cystine knot.
H. W. van den Hooven (2001)
10.1016/J.IJPARA.2004.02.008
Comparative analysis of two 14-3-3 homologues and their expression pattern in the root-knot nematode Meloidogyne incognita.
S. Jaubert (2004)
10.1016/J.PBI.2007.04.018
Defense suppression by virulence effectors of bacterial phytopathogens.
Luis da Cunha (2007)
Antioxidant enzymes in phytoparasitic nematodes.
S. Molinari (1997)
10.1016/S0960-9822(02)00510-9
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response
A. Levine (1996)
The Arabidopsis TransthyretinLike protein is a potential substrate of BRASSINOSTEROIDINSENSITIVE 1
KH Nam (2004)
10.1111/J.1567-1364.2007.00292.X
Analysis of the Paracoccidioides brasiliensis triosephosphate isomerase suggests the potential for adhesin function.
L. A. Pereira (2007)
10.1016/j.pbi.2008.04.003
Parasitism proteins in nematode-plant interactions.
E. Davis (2008)
10.1094/MPMI-20-0041
Identification and characterization of plant genes involved in Agrobacterium-mediated plant transformation by virus-induced gene silencing.
Ajith Anand (2007)
10.1016/S0962-8924(00)01745-1
Pathways for protein disulphide bond formation.
A. Frand (2000)
10.1094/MPMI.2001.14.1.72
Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita.
J. P. Semblat (2001)
10.1079/9780851996455.0175
Nematode morphology, sensory structure and function
J. Baldwin (2004)
Transgenic plant transformed with a translationally controlled tumor protein (TCTP) gene. C12N005/10
J G Kang (2003)
10.1094/MPMI.1999.12.7.585
Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism.
M. Rosso (1999)
10.1126/SCIENCE.1108633
Activation of a Phytopathogenic Bacterial Effector Protein by a Eukaryotic Cyclophilin
G. Coaker (2005)
10.1146/ANNUREV.PY.21.090183.001415
THE INTERNATIONAL MELOIDOGYNE PROJECT-ITS GOALS AND ACCOMPLISHMENTS
J. Sasser (1983)
10.1016/S1369-5266(03)00043-8
Establishing compatibility between plants and obligate biotrophic pathogens.
R. Panstruga (2003)
10.1371/journal.ppat.1000084
The Malaria Secretome: From Algorithms to Essential Function in Blood Stage Infection
Christiaan van Ooij (2008)
10.1002/j.1460-2075.1995.tb00250.x
The higher plant Arabidopsis thaliana encodes a functional CDC48 homologue which is highly expressed in dividing and expanding cells.
H. Feiler (1995)
10.1111/J.1365-313X.2006.02978.X
The ubiquitin pathway is required for innate immunity in Arabidopsis.
S. Goritschnig (2007)
10.1073/PNAS.97.2.948
An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration.
K. Mysore (2000)
10.1016/S0960-9822(98)70469-5
Caspases and programmed cell death in the hypersensitive response of plants to pathogens
Olga María del Pozo (1998)
10.1094/MPMI-20-3-0262
Characterization of genomic clones and expression analysis of the three types of superoxide dismutases during nodule development in Lotus japonicus.
M. C. Rubio (2007)
The identification and characterization of the SPRYSEC-gene family as effectors in Globodera rostochiensis plant-parasitism
S. Rehman (2007)
Transgenic plant transformed with a translationally controlled tumor protein (TCTP) gene
JG Kang (2003)
10.1007/s004250050281
Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs
P. Urwin (1998)
Ultrastructure of the Phasmids of Scutellonema brachyurum.
K. C. Wang (1985)
In planta localization of a beta-1,4-endoglucanase secreted by Heterodera glycines.
X. Wang (1999)
10.1094/MPMI-21-5-0576
Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence.
C. A. Gleason (2008)
Oxidative stress response in Paracoccidioides brasiliensis.
E. Campos (2005)
10.1016/s0960-9822(07)00555-6
Caspases and programmed cell death in the hypersensitive response of plants to pathogens
Olga María del Pozo (1998)
10.1016/S0166-6851(02)00034-8
Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach.
S. Jaubert (2002)
10.1017/S0022149X07850243
Responses of Heterodera glycines and Meloidogyne incognita to exogenously applied neuromodulators.
E. P. Masler (2007)
10.1139/O06-088
Structure and function of nucleosome assembly proteins.
Y. Park (2006)
10.1007/s00438-007-0267-4
Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica)
S. Ray (2007)
10.1073/PNAS.0407926102
Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus.
Ravisha R Weerasinghe (2005)
10.1196/annals.1327.086
Evolution of the Thyroid Hormone Distributor Protein Transthyretin in Microbes, C. elegans, and Vertebrates
S. Richardson (2005)
10.1094/MPMI-18-0615
Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins.
M. Rosso (2005)
10.3389/978-2-88945-399-3
Trends in Comparative Endocrinology and Neurobiology
H. Vaudry (2005)
Enzymes released during hatching of Globodera rostochiensis and Meloidogyne incognita
Roland N. Perry (1992)
10.1111/J.1365-313X.2004.02019.X
Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots.
J. de Almeida Engler (2004)
10.1073/PNAS.95.9.4906
Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes.
G. Smant (1998)
10.1094/MPMI.1999.12.1.64
In Planta Localization of a β-1,4-Endoglucanase Secreted by Heterodera glycines
X. Wang (1999)
10.1094/MPMI-18-1277
In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode.
S. Jaubert (2005)
Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots.
U. Wyss (1986)
10.1016/S0065-2776(06)92006-9
Antigen Presentation and the Ubiquitin‐Proteasome System in Host–Pathogen Interactions
Joana Loureiro (2006)
10.1038/nbt.1482
Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita
P. Abad (2008)
10.1021/PR025556V
Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome.
J. Peng (2003)
10.1016/S0014-5793(03)00723-3
Cold‐inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells 1
S. Imamura (2003)
10.1038/35017641
Enzymology: Degradation of plant cell walls by a nematode
H. Popeijus (2000)
A method for staining nematode secretions and structures.
D. Premachandran (1988)
10.1016/j.molbiopara.2008.02.007
The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products.
J. Hewitson (2008)
10.1016/J.JPLPH.2007.05.007
Root-knot nematodes manipulate plant cell functions during a compatible interaction.
Marie-Cécile Caillaud (2008)
10.1016/J.PHYTOCHEM.2007.07.027
Suppression of reactive oxygen species by glyceraldehyde-3-phosphate dehydrogenase.
D. Baek (2008)
10.2307/3276690
Changes associated with parasitism in nematodes. II. Histochemical and microspectrophotometric analyses of preparasitic and parasitic larvae of Meloidogyne javanica.
A. F. Bird (1967)
10.1139/Z85-079
Fine structure of the phasmid of second-stage juveniles of Heterodera schachtii (Tylenchida: Nematoda)
J. Baldwin (1985)
10.1146/ANNUREV.PHYTO.34.1.181
Chemoreception in plant parasitic nematodes.
Roland N. Perry (1996)
10.1017/S0031182000068293
Changes in host muscles induced by excretory/secretory products of larval Trichinella spiralis and Trichinella pseudospiralis.
R. Ko (1994)
Specific activation of the Gpa2 gene by members of the RBP effector gene familly from the potato cyst nematode Globodera pallida
K Koropacka (2008)
10.1016/S1360-1385(02)02261-6
Flagellin perception: a paradigm for innate immunity.
L. Gómez-Gómez (2002)
10.1094/MPMI-18-1269
MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence.
A. Boisson-Dernier (2005)
10.1094/MPMI.1998.11.10.952
A secretory cellulose-binding protein cDNA cloned from the root-knot nematode (Meloidogyne incognita).
X. Ding (1998)
10.1038/35074106
The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5
F. Hayashi (2001)



This paper is referenced by
10.1371/journal.pone.0147511
Analysis of the Transcriptome of the Infective Stage of the Beet Cyst Nematode, H. schachtii
John Fosu-Nyarko (2016)
10.1016/j.jbiosc.2013.01.003
Making headway in understanding pine wilt disease: what do we perceive in the postgenomic era?
Ryoji Shinya (2013)
10.1111/nph.13701
A novel nematode effector suppresses plant immunity by activating host reactive oxygen species‐scavenging system
Borong Lin (2016)
10.1146/annurev-phyto-080508-081839
The genomes of root-knot nematodes.
D. Bird (2009)
Funktionelle Charakterisierung des Ustilago maydis Effektorproteins Pit2
A. Mueller (2014)
Evaluación de diferentes estrategias de control de Meloidogyne sp. en cultivos de interés agronómico
F. Calle (2019)
10.1094/MPMI-09-15-0209-R
A Fungal Effector With Host Nuclear Localization and DNA-Binding Properties Is Required for Maize Anthracnose Development.
W. Vargas (2016)
Identific ation and characterization of effec tors secreted from sedentary endoparasitic phytonematodes
William Brock (2013)
10.1038/s41598-018-34174-4
Analysis of the Trichuris suis excretory/secretory proteins as a function of life cycle stage and their immunomodulatory properties
L. Leroux (2018)
10.1016/j.crvi.2015.04.002
Intraspecific variability of the facultative meiotic parthenogenetic root-knot nematode (Meloidogyne graminicola) from rice fields in Vietnam.
Stéphane Bellafiore (2015)
10.1016/j.gene.2011.10.040
Functional roles of effectors of plant-parasitic nematodes.
A. Haegeman (2012)
10.1038/nrg2812
Plant immunity: towards an integrated view of plant–pathogen interactions
P. Dodds (2010)
10.1155/2014/964350
Harnessing the Helminth Secretome for Therapeutic Immunomodulators
D. Ditgen (2014)
10.1186/1756-3305-5-140
First analysis of the secretome of the canine heartworm, Dirofilaria immitis
J. Geary (2012)
10.1094/MPMI-01-16-0015-R
Poplar-Root Knot Nematode Interaction: A Model for Perennial Woody Species.
F. Baldacci-Cresp (2016)
10.1016/j.plaphy.2016.10.021
Protease activity and phytocystatin expression in Arabidopsis thaliana upon Heterodera schachtii infection.
M. Labudda (2016)
10.1002/9781119949138.CH13
Nematode Effector Proteins: Targets and Functions in Plant Parasitism
Marie-Noëlle Rosso (2011)
10.1016/j.jbiosc.2014.01.006
Robust in vitro assay system for quantitative analysis of parasitic root-knot nematode infestation using Lotus japonicus.
A. N. Amin (2014)
10.1094/phyto-05-19-0163-ia
Advances in Plant-Nematode Interactions with Emphasis on the Notorious Nematode Genus Meloidogyne.
Isgouhi Kaloshian (2019)
10.1111/mpp.12671
A novel Meloidogyne graminicola effector, MgMO237, interacts with multiple host defence-related proteins to manipulate plant basal immunity and promote parasitism.
Jiansong Chen (2018)
10.1146/annurev-phyto-081211-173008
Role of nematode peptides and other small molecules in plant parasitism.
M. Mitchum (2012)
10.1093/bioinformatics/btr110
Identifying discriminative classification-based motifs in biological sequences
C. Vens (2011)
TRANSCRIPTOME AND PROTEOME ALTERATIONS DURING THE NEMATODE-SOYBEAN INTERACTION
A. Prince (2014)
10.5897/AJAR2016.11517
Plant defense elicitors purification in soybean and bean from pathogenic nematode
Edilaine Della Valentina Gonalves-Trevisoli (2016)
10.5539/JAS.V3N4P86
Molecular Cloning and Phylogenetic Analysis of Two Plant-Parasitic Nematode 14-3-3 Genes
Dandan Liu (2011)
10.1016/j.crvi.2014.03.003
Fast assembly of the mitochondrial genome of a plant parasitic nematode (Meloidogyne graminicola) using next generation sequencing.
G. Besnard (2014)
10.1021/pr1006069
Proteomic and bioinformatic analysis of the root-knot nematode Meloidogyne hapla: the basis for plant parasitism.
Flaubert Mbeunkui (2010)
Identification of soil nematodes in Ngere tea catchment area of Murang’a County, Kenya
Tom Kosgei Kibet (2013)
10.1007/s42360-020-00240-z
Fusarium-nematode wilt disease complexes, etiology and mechanism of development
Mujeebur Rahman Khan (2020)
10.14201/gredos.127301
Trasferencia horizontal de genes y mimetismo molecular en hongos fitopatógenos del género Colletotrichum
A. Jaramillo (2014)
10.3390/proteomes2040527
Enhanced Synthesis of Antioxidant Enzymes, Defense Proteins and Leghemoglobin in Rhizobium-Free Cowpea Roots after Challenging with Meloydogine incognita
J. A. Oliveira (2014)
10.1104/pp.112.199281
Ubiquitination during Plant Immune Signaling1
D. Marino (2012)
See more
Semantic Scholar Logo Some data provided by SemanticScholar