Biotechnology Research and Innovation Journal
http://www.biori.periodikos.com.br/article/doi/10.1016/j.biori.2017.10.003
Biotechnology Research and Innovation Journal
Plant Biotechnology Research article

Prospection and identification of nematotoxic compounds from Canavalia ensiformis seeds effective in the control of the root knot nematode Meloidogyne incognita  

Thales L. Rocha, Carla Becker Soll, Berin A. Boughton, Tiago S. Silva, Klaus Oldach, Alexandre A.P. Firmino, Damien L. Callahan, John Sheedy, Edilberto R. Silveira, Regina M.D.G. Carneiro, Luciano P. Silva, Vera L.P. Polez, Patrícia B. Pelegrini, Antony Bacic, Maria F. Grossi-de-Sa, Ute Roessner

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Abstract

Meloidogyne incognita is responsible for significant crop losses worldwide. The main strategy to control this phytopathogen is still based on synthetic nematicides that are harmful to human health and the environment. In this context, aqueous seed extracts of antagonistic plants were screened for molecules effective toward the infective stage (J2) of M. incognita. The aqueous crude extract of Canavalia ensiformis (ACECe) showed the highest nematicidal activity (87 ± 3% mortality). ACECe dialysis fractionation allowed the collection of an external dialysate (EDCe) containing molecules smaller than 3.5 kDa effective against J2 (96 ± 3.0% mortality); innocuous toward non targeted organisms as saprophytic nematodes, fungi, bacterium and insects larvae; active against J2 (96 ± 2% mortality) after heating (50 °C); no cytotoxic for bovine red blood cells; reduction of M. incognita eggs masses by 82.5% in tomato plants at green house conditions. Fractionation of the EDCe by reversed-phase high-performance liquid chromatography (RP-HPLC) separated five nematotoxic fractions. Analyses of those fractions based on gas chromatography–mass spectrometry (GC–MS), liquid chromatography–mass spectrometry (LCMS) and nuclear magnetic resonance (NMR) identified nine specific metabolites, follow-up testing of the individual authentic standards of each metabolite as the compounds: d-glucose, l-canavanine, xanthotoxin, cis-aconitic acid, trans-aconitic acid, malic acid, citric acid, palmitic acid and S-carboxymethylcysteine; all them confirmed to possess nematotoxic properties. However, some of those metabolites were not described previously demonstrating biological action against M. incognita.

Keywords

Meloidogyne incognita,  Canavalia ensiformis,  Nematotoxic compounds  

References

Abad et al., 1996
L.R. Abad, M.P. D’Urzo, D. Liu, M.L. Narasimhan, M. Reuveni, J.K. Zhu, R.A. Bressan
Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization
Plant Science, 118 (1) (1996), pp. 11-23

Abad et al., 2003
P. Abad, B. Favery, M.N. Rosso, P. Castagnone-Sereno
Root–knot nematode parasitism and host response: Molecular basis of a sophisticated interaction
Molecular Plant Pathology, 4 (4) (2003), pp. 217-224

Barbosa et al., 1999
L.C.A. Barbosa, F.F. Barcelos, A.J. Demuner, M.A. Santos
Chemical constituents from Mucuna aterrima with activity against Meloidogyne incognita and Heterodera glycines
Nematropica, 29 (1999), pp. 81-88

Berny, 2007
P. Berny
Pesticides and the intoxication of wild animals
Journal of Veterinary Pharmacology and Therapeutics, 30 (2) (2007), pp. 93-100

Birch et al., 1992
Birch, A. N. E., Fellows, L. E., Geoghegan, I. E., Robertson, W. M., & Watson, A. A. (1992). Control of parasitic nematodes. Patent Application No. 9216903.6.

Bird and Bird, 1991
A.F. Bird, J. Bird
The structure of nematodes
Academic Press, San Diego (1991)

Boudart, 1989
G. Boudart
Antibacterial activity of sirodesmin PL phytotoxin: Application to the selection of phytotoxin-deficient mutants
Applied and Environmental Microbiology, 55 (6) (1989), pp. 1555-1559

Caboni et al., 2014
P. Caboni, M. Saba, C. Oplos, N. Aissani, A. Maxia, U. Menkissoglu-Spiroudi, N. Ntalli
Nematicidal activity of furanocoumarins from parsley against Meloidogyne spp.
Pest Management Science (2014)

Carlini and Grossi-de-Sá, 2002
C.R. Carlini, M.F. Grossi-de-Sá
Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides
Toxicon, 40 (11) (2002), pp. 1515-1539

Chaubal et al., 2005
R. Chaubal, P.V. Pawar, G.D. Hebbalkar, V.B. Tungikar, V.G. Puranik, V.H. Deshpande, N.R. Deshpande
Larvicidal activity of Acacia nilotica extracts and isolation of d-pinitol – A bioactive carbohydrate
Chemistry & Biodiversity, 2 (5) (2005), pp. 684-688

Duke, 1990
S.O. Duke
Natural pesticides from plants
J Janick, J.E. Simon (Eds.), Advances in new crops, Timber Press, Portland (1990), pp. 511-517

EC, 2013
EC. European Commission. (2013). Available from: http://ec.europa.eu/food/plant/pesticides/index_en.htm/ Accessed 10.05.16.

Elbadri et al., 2008
G.A. Elbadri, D.W. Lee, J.C. Park, H.B. Yu, H.Y. Choo
Evaluation of various plant extracts for their nematicidal efficacies against juveniles of Meloidogyne incognita
Journal of Asia-Pacific Entomology, 11 (2) (2008), pp. 99-102

EPA, 2009
EPA
Registering pesticides
(2009)
Available from: http://www.epa.gov/pesticides/regulating/re-gistering/index.htm/ Accessed 04.13.16

FAO, 2016
Food and Agriculture Organization of the United Nations – http://www.fao.org/docrep/v9978e/v9978e08.htm/ Accessed 07.05.16.

Ferraz and Freitas, 2000
S. Ferraz, L.G. Freitas
O controle de fitonematóides por plantas antagonistas e produtos naturais
Sociedade Brasileira de Nematologia (2000)

Ferraz and Freitas, 2004
Ferraz, S., & Freitas, L. G. (2004). Use of antagonistic plants and natural products. In Z. X. Chen, S. Y. Chen, & D. W. Dickson (Orgs.), Nematology: Advances and perspectives. Volume 2: Nematode management and utilization (p. 931–977). Wallingford: CABI. Retrieved from: http://www.cabi.org/cabebooks/ebook/20043189783

Fiehn et al., 2000
O. Fiehn, J. Kopka, R.N. Trethewey, L. Willmitzer
Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry
Analytical Chemistry, 72 (15) (2000), pp. 3573-3580

Hill et al., 2013
C.B. Hill, D. Jha, A. Bacic, M. Tester, U. Roessner
Characterization of ion contents and metabolic responses to salt stress of different Arabidopsis AtHKT1; 1 genotypes and their parental strains
Molecular Plant, 6 (2) (2013), pp. 350-368

Hu and Feng, 2003
Q. Hu, S. Feng
A daily soil temperature dataset and soil temperature climatology of the contiguous United States
Journal of Applied Meteorology, 42 (8) (2003), pp. 1139-1156

Hussey and Barker, 1973
R.S. Hussey, K.R. Barker
Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique
Plant Disease Reporter (1973)

Jang et al., 2014
J.Y. Jang, Q. Le Dang, Y.H. Choi, G.J. Choi, K.S. Jang, B. Cha, ..., J.-C. Kim
Nematicidal activities of 4-quinolone alkaloids isolated from the aerial part of Triumfetta grandidens against Meloidogyne incognita
Journal of Agricultural and Food Chemistry (2014)

Jatala and Bridge, 1990
P. Jatala, J. Bridge
Nematode parasites of root and tuber crops
Plant Parasitic Nematodes in Subtropical and Tropical Agriculture (1990), pp. 137-180

Jenkins, 1964
W. Jenkins
A rapid centrifugal-flotation technique for separating nematodes from soil
Plant Disease Reporter, 48 (1964), p. 9

Kar et al., 1993
S. Kar, K. Kar, P.K. Bhattacharya, D.K. Ghosh
Experimental visceral leishmaniasis: Role of trans-aconitic acid in combined chemotherapy
Antimicrobial Agents and Chemotherapy, 37 (11) (1993), pp. 2459-2465

Khurma and Mangotra, 2004
U.R. Khurma, A. Mangotra
Screening of some Leguminosae seeds for nematicidal activity
South Pacific Journal of Natural and Applied Sciences, 22 (1) (2004), pp. 51-53

Kim et al., 2010
H.K. Kim, Y.H. Choi, R. Verpoorte
NMR-based metabolomic analysis of plants
Nature Protocols, 5 (3) (2010), pp. 536-549

Kopka et al., 2005
J. Kopka, N. Schauer, S. Krueger, C. Birkemeyer, B. Usadel, E. Bergmüller, D. Steinhauser
GMD@CSB.DB: The golm metabolome database
Bioinformatics, 21 (8) (2005), pp. 1635-1638

Krishnan et al., 2005
P. Krishnan, N.J. Kruger, R.G. Ratcliffe
Metabolite fingerprinting and profiling in plants using NMR
Journal of Experimental Botany, 56 (410) (2005), pp. 255-265

Lopes et al., 2009
E.A. Lopes, S. Ferraz, O.D. Dhingra, P.A. Ferreira, L.G. Freitas
Soil amendment with castor bean oilcake and jack bean seed powder to control Meloidogyne javanica on tomato roots
Nematologia Brasileira, V33 (2009), pp. 106-109

McCarter, 2009
McCarter, J. P. (2009). Molecular approaches toward resistance to plant–parasitic nematodes. In D. Berg Integrated Microscopy Facility R. Howard & P. I. C. G. Taylor (Orgs.), Cell biology of plant nematode parasitism, 239–267.

Meyer et al., 2006
S.L.F. Meyer, I.A. Zasada, D.P. Roberts, B.T. Vinyard, D.K. Lakshman, J.-K. Lee, ..., L.K. Carta
Plantago lanceolata and Plantago rugelii extracts are toxic to Meloidogyne incognita but not to certain microbes
Journal of Nematology, 38 (3) (2006), pp. 333-338

Monnerat et al., 2000
R.G. Monnerat, S.C. Dias, O.B. Oliveira-Neto, S.D. Nobre, J.O. Silva-Werneck, M.F. Grossi-de-Sá
Comunicado Técnico Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brasil
(2000)
ISSN 0102-0099, 4pp.

Naz et al., 2016
I. Naz, S. Abdulkafi, I. Munir, M. Ahmad, A. Ali, J.E. Palomares-Rius, I. Ahmad
Cis-and trans-protopinium, a novel nematicide, for the eco-friendly management of root–knot nematodes
Crop Protection, 81 (2016), pp. 138-144

Ntalli and Caboni, 2012
N.G. Ntalli, P. Caboni
Botanical nematicides: A review
Journal of Agricultural and Food Chemistry, 60 (40) (2012), pp. 9929-9940

Oksman-Caldentey and Inzé, 2004
K.-M. Oksman-Caldentey, D. Inzé
Plant cell factories in the post-genomic era: New ways to produce designer secondary metabolites
Trends in Plant Science, 9 (9) (2004), pp. 433-440

Oliveira et al., 2009
D.F. Oliveira, H.W.P. Carvalho, A.S. Nunes, G.H. Silva, V.P. Campos, H.M.S. Júnior, A.J. Cavalheiro
The activity of amino acids produced by Paenibacillus macerans and from commercial sources against the root–knot nematode Meloidogyne exigua
European Journal of Plant Pathology, 124 (1) (2009), pp. 57-63

Osman, 1993
G.Y. Osman
Effect of amino acids and ascorbic acid on Meloidogyne javanica Chitw. (Tylenchidae, Nematoda)
Anzeiger Für Schädlingskunde, Pflanzenschutz, Umweltschutz, 66 (7) (1993), pp. 140-142

Potter et al., 1993
J.W. Potter, T.H. Olthof, K. Evans, D.L. Trudgill, J.M. Webster
Nematode pests of vegetable crops
Plant Parasitic Nematodes in Temperate Agriculture (1993), pp. 171-207

Praça et al., 2004
L. Praça, E. Martins, A.C. Batista, R.G. Monnerat
Prospecção de estirpes de Bacillus thuringiensis efetivas contra insetos da ordem Lepidoptera, Diptera e Coleoptera
Pesquisa Agropecuária Brasileira, DF, 39 (2004), pp. 11-16

Prakash et al., 2014
A. Prakash, J. Rao, J. Berliner, S.S. Pokhare, T. Adak, K. Saikia
Botanical pesticides for the management of plant nematode and mite pests
Advances in Plant Biopesticides (2014), pp. 89-118

Reynolds et al., 2011
A.M. Reynolds, T.K. Dutta, R.H.C. Curtis, S.J. Powers, H.S. Gaur, B.R. Kerry
Chemotaxis can take plant–parasitic nematodes to the source of a chemo-attractant via the shortest possible routes
Journal of the Royal Society Interface, 8 (57) (2011), pp. 568-577

Rockström et al., 2016
J. Rockström, J. Williams, G. Daily, A. Noble, N. Matthews, L. Gordon, C. de Fraiture
Sustainable intensification of agriculture for human prosperity and global sustainability
Ambio (2016), pp. 1-14

Roessner and Bowne, 2009
U. Roessner, J. Bowne
What is metabolomics all about?
BioTechniques, 46 (5) (2009), pp. 363-365

Roessner et al., 2001
U. Roessner, A. Luedemann, D. Brust, O. Fiehn, T. Linke, L. Willmitzer, A.R. Fernie
Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems
Plant Cell, 13 (1) (2001), pp. 11-29

Rosenthal, 1990
G.A. Rosenthal
Metabolism of l-canavanine and l-canaline in leguminous plants
Plant Physiology, 94 (1) (1990), pp. 1-3

Sano, 2005
Z. Sano
Cultural control of the nematode damage
Large encyclopedia of environmental conservation agriculture. Noubunkyo, Tokyo (2005), pp. 281-316

Santiago et al., 2005
D.C. Santiago, M. Homechin, R. Montalvan, A.A. Krzyzanowski
Potential of sucrose and Pennisetum purpureum cv. Cameroon mulch on the management of Meloidogyne javanica and M. incognita
Brazilian Archives of Biology and Technology, 48 (6) (2005), pp. 873-883

Sasser and Freckman, 1987
J.N. Sasser, D.W. Freckman
A world perspective on nematology: The role of the society
(1987)
http://agris.fao.org/agris-search/search.do?recordID=US8903406

Schliemann et al., 2008
W. Schliemann, C. Ammer, D. Strack
Metabolite profiling of mycorrhizal roots of Medicago truncatula
Phytochemistry, 69 (1) (2008), pp. 112-146

Schripsema, 2010
J. Schripsema
Application of NMR in plant metabolomics: Techniques, problems and prospects
Phytochemical Analysis: PCA, 21 (1) (2010), pp. 14-21

Schultes, 1978
R.E. Schultes
The kingdom of plants
W.A.R. Thomson (Ed.), Medicines from the earth (1978)

Seiber et al., 2014
J.N. Seiber, J. Coats, S.O. Duke, A.D. Gross
Biopesticides: State of the art and future opportunities
Journal of Agricultural and Food Chemistry, 62 (48) (2014), pp. 11613-11619

Shemshura et al., 2016
O.N. Shemshura, N.E. Bekmakhanova, M.N. Mazunina, S.L. Meyer, C.P. Rice, E.P. Masler
Isolation and identification of nematode-antagonistic compounds from the fungus Aspergillus candidus
FEMS Microbiology Letters, 363 (5) (2016)

Silva et al., 2002
G.S. Silva, I.M.R. Souza, F.A. Cutrim
Efeito da incorporação de sementes trituradas de Feijão de porco ao solo sobre o parasitismo de Meloidogyne incognita em tomateiro
Fitopatologia Brasileira (2002), p. 27

Talavera and Mizukubo, 2005
M. Talavera, T. Mizukubo
Effects of dl-methionine on hatching and activity of Meloidogyne incognita eggs and juveniles
Pest Management Science, 61 (4) (2005), pp. 413-416

Taylor and Sasser, 1978
A.L. Taylor, J.N. Sasser
Biology, identification and control of root–knot nematodes
North Carolina State University Graphics (1978)

Trethewey, 2004
R.N. Trethewey
Metabolite profiling as an aid to metabolic engineering in plants
Current Opinion in Plant Biology, 7 (2) (2004), pp. 196-201

Ward et al., 2007
J.L. Ward, J.M. Baker, M.H. Beale
Recent applications of NMR spectroscopy in plant metabolomics
FEBS Journal, 274 (5) (2007), pp. 1126-1131

Williamson and Gleason, 2003
V.M. Williamson, C.A. Gleason
Plant–nematode interactions
Current Opinion in Plant Biology, 6 (4) (2003), pp. 327-333

Wink, 1988
M. Wink
Plant breeding: Importance of plant secondary metabolites for protection against pathogens and herbivores
Theoretical and Applied Genetics, 75 (2) (1988), pp. 225-233

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