Raquel CAMPOS-HERRERA, Ignacio VICENTE-DÍEZ, Rubén BLANCO-PÉREZ, Maryam CHELKHA, María del Mar GONZÁLEZ-TRUJILLO, Miguel PUELLES, Rasa ČEPULITĖ, Alicia POU

Positioning entomopathogenic nematodes for the future viticulture: exploring their use against biotic threats and as bioindicators of soil health

Abstract: Vineyards face several biotic threats that compromise the grape quality and quantity. Among those that cause relevant economic impact and have worldwide distribution are the oomycete Plasmopara vitícola, the fungi Erysiphe necator and Botrytis cinerea, and the arthropods Lobesia botrana, Tetranychus urticae, and Phylaenus spumarius (principal vector of the bacterial disease Xylella fastidiosa in Europe). Their management relies primarily on agrochemicals with short persistence; widespread use of these chemicals causes environmental and human health problems. The challenge of sustainable viticulture is to provide ecologically sound alternatives. In this regard, the application of entomopathogenic nematodes (EPNs) and natural products derived from their symbionts can be an alternative. EPNs are well-known biocontrol agents for soil-dwelling insects. However, current research demonstrates the great potential of both EPN and their derivates as direct bio-tools against some of the key fungal and arthropods pests present aboveground. In addition, recent evidence shows that detecting EPN presence and activity and their relation with other soil organisms associated with them can help us to understand the impact of different agricultural practices on vineyard management. Altogether, this review illustrates the great potential of EPN to enhance pest and disease management in the next generation of viticulture.Key words: Vineyards, Steinernema, Heterorhabditis, Photorhabdus, Xenorhabdus, natural products

PDF

___

Aballay E, Prodan S, Correa P, Allende J (2020). Assessment of rhizobacterial consortia to manage plant parasitic nematodes of grapevine. Crop Protection 131: 105103.
Adams BJ, Fodor A, Koppenhöfer HS, Stackebrandt E, Stock SP et al. (2006). Biodiversity and systematics of nematode-bacterium entomopathogens. Biol. Control 38: 4-21.
Armijo G, Schlechter R, Agurto M, Muñoz D, Núñez C et al. (2016). Grapevine pathogenic microorganisms: understanding infection strategies and host response scenarios. Frontiers in Plant Science 7: 382.
Belair G, Dauphinais N, Fournier Y, Mauleon H (2001). Survey of plant-parasitic and entomopathogenic nematodes in vineyards of Quebec. Phytoprotection 82: 49-55.
Blanco-Pérez R, Bueno-Pallero FÁ, Vicente-Díez I, Marco-Mancebón VS, Pérez-Moreno I et al. (2019). Scavenging behavior and interspecific competition decrease off spring fitness of the entomopathogenic nematode Steinernema feltiae. Journal of Invertebrathe Pathology 164: 5-15.
Blanco-Pérez R, Sáenz-Romo MG, Vicente-Díez I, Ibáñez-Pascual S, Martínez-Villar E et al. (2020). Impact of vineyard ground cover management on the occurrence and activity of entomopathogenic nematodes and associated soil organisms. Agriculture Ecosystem and Environmet 301: 107028.
Bode HB (2009). Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology 13: 224-230.
Bongers T (1990). The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-9.
Bongers T, Ferris H (1999). Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology and Evolution (Amsterdam) 14: 224-228.
Bueno-Pallero FÁ, Blanco-Pérez R, Dionísio L, Campos-Herrera R (2018). Simultaneous exposure of nematophagous fungi, entomopathogenic nematodes and entomopathogenic fungi can modulate belowground insect pest control. Journal of Invertebrathe Pathology 154: 85-94.
Cabaleiro C, Vilas R, Padilla B (2020). Cochinillas algodonosas y mosquito verde en viñedo, ¿plagas menores? Vida Rural 484: 40-45. (In Spanish).
Campos–Herrera R (2015) Nematode pathogenesis of insects and other pests - ecology and applied technologies for sustainable plant and crop protection. Series: Sustainability in Plant and Crop Protection., A. Ciancio (series Ed.). Vol 1, Switzerland: Springer International Publishing, pp. 530.
Campos-Herrera R, Gómez-Ros JM. Escuer M, Cuadra L, Barrios L et al. (2008). Diversity, occurrence, and life characteristics of natural entomopathogenic nematode populations from La Rioja (Northern Spain) under different agricultural management and their relationships with soil factors. Soil Biology & Biochemistry 40: 1474-1484.
Campos-Herrera R, Johnson EG, Stuart RJ, Graham JH, Duncan LW (2011). Long-term stability of entomopathogenic nematode spatial patterns in soil as measured by sentinel insects and realtime PCR assays. Annals of Applied Biology 158: 55-68.
Campos-Herrera R, El-Borai FE, Duncan LW (2012). Wide interguild relationships among entomopathogenic and freeliving nematodes in soil as measured by real time qPCR. Journal of Invertebrathe Pathology 111:126-135.
Campos-Herrera R, El-Borai FE, Ebert TE, Schumann A, Duncan LW (2014). Management to control citrus greening alters the soil food web and severity of a pestdisease complex. Biological Control 76: 41-51.
Campos-Herrera R, Blanco-Pérez R, Bueno-Pallero FÁ, Duarte A, Nolasco G et al. (2019). Vegetation drives assemblages of entomopathogenic nematodes and other soil organisms: evidence from the Algarve, Portugal. Soil Biology & Biochemistry 128: 150-163.
Cevizci D, Ulug D, Cimen H, Touray M, Hazir S et al. (2020). Mode of entry of secondary metabolites of the bacteria Xenorhabdus szentirmaii and X. nematophila into Tetranychus urticae, and their toxicity to the predatory mites Phytoseiulus persimilis and Neoseiulus californicus. Journal of Invertebrathe Pathology 174: 107418.
Chacón-Orozco JG, Bueno CJ, Shapiro-Ilan DI, Hazir S, Leite LG et al. (2020). Antifungal activity of Xenorhabdus spp. and Photorhabdus spp. against the soybean pathogenic Sclerotinia sclerotiorum. Scientific Reports 10: 20649.
Daane KM, Vincent C, Isaacs R, Ioriatti C (2018). Entomological Opportunities and Challenges for Sustainable Viticulture in a Global Market. Annual Review of Entomology 63: 193-214.
Da Silva WJ, Pilz-Júnior HL, Heermann R, Da Silva OS (2020). The great potential of entomopathogenic bacteria Xenorhabdus and Photorhabdus for mosquito control: a review. Parasites and Vectors 13: 1-14. 10.1186/s13071-020-04236-6
Damalas CA, Koutroubas SD (2018). Current status and recent developments in biopesticide use. Agriculture 8: 13.
Delcour I, Spanoghe P, Uyttendaele M (2015). Literature review: Impact of climate change on pesticide use. Food Research International 68: 7-15.
Dillman AR, Chaston JM, Adams BJ. Ciche TA, Goodrich-Blair H et al. (2012). An entomopathogenic nematode by any other name. PLoS Pathogen 8:1-5.
Duncan LW, Dunn DC, Bague G, Nguyen K (2003). Competition between entomopathogenic and free-living bactivorous nematodes in larvae of the weevil Diaprepes abbreviatus. Journal of Nematology 35: 187-193.
Duncan LW, Graham JH, Zellers J, Bright D, Dunn DC et al. (2007). Food web responses to augmenting the entomopathogenic nematodes in bare and animal manure-mulched soil. Journal of Nematology 39: 176-189.
Eilenberg J, Hajek A, Lomer C (2001). Suggestions for unifying the terminology in biological control. BioControl 46: 387-400.
English-Loeb G, Villani M, Martinson T, Forsline A, Console N (1999). Use of entomopathogenic nematodes for control of grape phyllosera (Homoptera: Phylloxeridae): a laboratory evaluation. Environmental Entomology 28:890-894.
Eroglu C, Cimen H, Ulug D, Karagoz M, Hazir S et al. (2019). Acaricidal effect of cell-free supernatants from Xenorhabdus and Photorhabdus bacteria against Tetranychus urticae (Acari: Tetranychidae). Journal of Invertebrathe Pathology 160: 61-66.
Ettema CH (1998). Soil nematode diversity: species coexistence and ecosystem function. Journal of Nematology 30: 159-169.
Fang XL, Li ZZ, Wang YH, Zhang X (2011). In vitro and in vivo antimicrobial activity of Xenorhabdus bovienii YL002 against Phytophthora capsici and Botrytis cinerea. Journal of Applied Microbiology 111: 145-154.
Fang X, Zhang M, Tang Q, Wang Y, Zhang X (2014). Inhibitory effect of Xenorhabdus nematophila TB on plant pathogens Phytophthora capsici and Botrytis cinerea in vitro and in planta. Scientific Reports 4: 1-7.
Ferris H (2010). Form and function:metabolic footprints of nematodes in the soil food web. European Journal of Soil Biology 46: 97-104.
Ferris H, Sánchez-Moreno S, Brennan EB (2012). Structure, functions and interguild relationships of the soil nematode assemblage in organic vegetable production. Applied Soil Ecology 61: 16-25.
Flores-Félix JD, Menéndez E, Peix A, García-Fraile P, Velázquez E (2020). History and current taxonomic status of genus Agrobacterium. Systematic and Applied Microbiology 43: 126046.
Fahrentrapp J, Müller L, Schumacher P (2015). Is there need for leafgalling grape phylloxera control? Presence and distribution of Daktulosphaira vitifoliae in Swiss vineyards. International Journal of Pest Management 61: 340-345.
Gliessman SR (2007). Agroecology: The Ecology of Sustainable Food Systems. CRC Press, pp. 383.
Gramaje D, Úrbez-Torres JR, Sosnowski MR (2018). Managing grapevine trunk diseases with respect to etiology and epidemiology: current strategies and future prospects. Plant Disease 102: 12-39
Granett J, Walker MA, Kocsis L, Omer AD (2001). Biology and management of grape phylloxera. Annual Review of Entomology 46: 387-412.
Grewal PS, Bornstein-Forst S, Burnell AM, Glazer I, Jagdale GB (2006). Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biological Control 38: 54-65.
Griffin CT (2015). Behaviour and population dynamics of entomopathogenic nematodes following application. In Campos-Herrera R (Ed.), Nematode Pathogenesis of Insects and Other Pests: Ecology and Applied Technologies for Sustainable Plant and Crop Protection. Springer International Publishing, AG Switzerland, pp. 57-95.
Gumus A, Karagoz M, Shapiro-Ilan D, Hazir S (2015). A novel approach to biocontrol: Release of live insect hosts pre-infected with entomopathogenic nematodes. Journal of Invertebrathe Pathology 130: 56-60.
Gutiérrez C, Campos Herrera R, Jiménez J (2008). Comparative study of selected agrochemical products activity on Steinernema feltiae (Rhabditida: Steinernematidae). Biocontrol Science and Technology 18: 101-108.
Gutiérrez AP, Ponti L, Baumgärtner (2017). Climate warming effects on grape and grapevine moth (Lobesia botrana) in the Palearctic region. Agricultural and Forest Entomology. 10.1111/afe.12256.
Héloir MC, Adrian M, Brulé D, Claverie J, Cordelier S, et al. (2019). Recognition of elicitors in grapevine: from MAMP and DAMP perception to induced resistance. Frontiers in Plant Science 10:1117.
Herrero-Hernández E, Rodríguez-Cruz MS, Pose-Juan E, SánchezGonzález S, Andrades MS et al. (2017). Seasonal distribution of herbicide and insecticide residues in the water resources of the vineyard region of La Rioja (Spain) Science of the Total Environment 609: 161-171.
Hiltpold I (2015). Prospects in the application technology and formulation of entomopathogenic nematodes for biological control of insect pests. In : Campos-Herrera R (Editor). Nematode pathogenesis of insects and other pests, sustainability in plant and crop protection. Vol. 1. Switzerland: Springer International Publishing, pp. 187-205.
Incedayi G, Cimen H, Ulug D, Touray M, Bode E et al. (2021). Relative potency of a novel acaricidal compound from Xenorhabdus, a bacterial genus mutualistically associated with entomopathogenic nematodes. Scientific Reports 11: 11253.
Jean-Baptiste MC, Lima de Brida A, Bernardi D, da Costa Dias S, de Bastos Pazini J et al. (2021). Effectiveness of entomopathogenic nematodes against Ceratitis capitata (Diptera: Tephritidae) pupae and nematode compatibility with chemical insecticides. Journal of Economic Entomology 114: 248-256.
Karimi B, Cahurel JY, Gontier L, Charlier L, Chovelon M et al. (2020). A meta-analysis of the ecotoxicological impact of viticultural practices on soil biodiversity. Environmental Chemistry Letters 18: 1947-1966.
Lacey LA, Georgis R (2012). Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology 44: 218-225.
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M et al. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrathe Pathology 132: 1-41.
Lewis EE, Hazir S, Hodson A, Gulcu B (2015). Trophic relationships of entomopathogenic nematodes in agricultural habitats. In: Campos-Herrera R (Editor). Nematode Pathogenesis of Insects and Other Pests: Ecology and Applied Technologies for Sustainable Plant and Crop Protection. Springer International Publishing, AG Switzerland, pp. 139-163.
Majić I, Sarajlić A, Lakatos T, Tóth T, Raspudić E et al. (2018). First report of entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) from Croatia. Helminthologia 55: 256-260.
Marco V, Carvajal-Montoya LD, García-Ruiz E (2008). Vid. In: Control Biológico de plagas agrícolas, Ed. Jacas, J.A., Urbaneja, A. Phytoma-España, Valencia (in Spanish).
Marin D, Armengol J, Carbonell-Bejerano P, Escalona JM, Gramaje D et al. (2020). Challenges of viticulture adaptation to global change: tackling the issue from the roots. Australian Journal of Grape and Wine Research. 10.1111/ajgw.12463.
Martelli GP (2014). Virus diseases of grapevine. In eLS (Chichester: John Wiley & Sons, Ltd). 10.1002/9780470015902.a0000766. pub3.
Mracek Z, Kindlmann P, Wegster J (2005). Steinernema affine (Nematoda: Steinernematidae), a new record for North America and its distribution relative to other entomopathogenic nematodes in British Columbia. Nematology 7: 495-501.
Nalinci E, Karagoz M, Gulcu B, Ulug D, Hazal Gulsen S et al. (2021). The effect of chemical insecticides on the scavenging performance of Steinernema carpocapsae: direct effects and exposure to insects killed by chemical insecticides. Journal of Invertebrathe Pathology 184: 107641.
Nicholls CI, Altieri MA, Ponti L (2008). Enhancing plant diversity for improved insect pest management in Northern California organic vineyards. Acta Horticulturae 785: 263-278.
Nicholls CI (2010). Contribuciones agroecológicas para renovar las fundaciones del manejo de plagas. Agroecología 5: 7-22 (in Spanish).
Ollat N, Peccoux A, Papura D, Esmenjaud D, Marguerit E et al. (2016). Rootstocks as a component of adaptation to environment. Gerós, H., Chaves, M.M., Gil, H.M. and Delrot, S (Editors). Grapevine in a changing environment (John Wiley: Chichester, England) pp. 68-108.
Özdemir E, Inak E, Evlice E, Laznik Z (2020). Compatibility of entomopathogenic nematodes with pesticides registered in vegetable crops under laboratory conditions. Journal of Plant Disease Protection 127: 529-535.
Pertot I, Caffi T, Rossi V, Mgnai L, Hoffmann C et al. (2017). A critical review of plant protection tools for reducing pesticide use on grapevine and new perspectives for the implementation of IPM in viticulture. Crop Prot.ection 97: 70-84.
Perrone I, Chitarra W, Boccacci P, Gambino G (2017). Grapevine– virus–environment interactions: an intriguing puzzle to solve. New Phytologist 213: 983-987.
Platt T, Stokwe NF, Malan AP (2019). Foliar application of Steinernema yirgalemense to control Planococcus ficus: assessing adjuvants to improve efficacy. South African Journal of Enology and Viticulture 40: 1.
Pose-Juan E, Sánchez-Martín, MJ, Andrades MS, Rodríguez-Cruz, MS, Herrero-Hernández H (2015). Pesticides redidues in vineyard soils from Spain: spatial and temporal distributions. Science of the Total Environment 514: 351-358.
Provost C, Pedneault K (2016). The organic vineyard as a balanced ecosystem: improved organic grape management and impacts on wine quality. Science Horticulturae (Amsterdam) 208: 43- 56.
Rodrigo-Comino J, Keesstra S, Cerdà A (2018). Soil erosion as an environmental concern in vineyards: the case study of Celler del Roure, Eastern Spain, by means of rainfall simulation experiments. Beverages 4: 31.
Sáenz-Romo MG, Veas-Bernal A, Martínez-García H, CamposHerrera R, Ibáñez-Pascual S et al. (2019). Ground cover management in a Mediterranean vineyard: impact on insect abundance and diversity. Agriculture, Ecosystems and Environment 283: 106571.
Saucet SB, van Ghelder C, Abad P, Duval H, Esmenjaud D (2016). Resistance to root-knot nematodes Meloidogyne spp. in woody plants. New Phytologist 211: 41-56.
Shapiro-Ilan DI, Dolinski C (2015). Entomopathogenic nematode application technology. In: Campos-Herrera R (Ed.), Nematode pathogenesis of insects and other pests, sustainability in plant and crop protection (Vol 1) Springer International, 1: 231-54.
Silva V, Mol HGJ, Zomer P, Tienstra M, Ritsema CJ et al. (2019). Pesticide residues in European agricultural soils – A hidden reality unfolded. Science of the Total Environment 653: 1532- 1545.
Steyn VM, Malan AP, Addison P (2021). Efficacy of entomopathogens against Thaumatotibia leucotreta under laboratory conditions. Entomologia Experimentalis et Applicata 169: 449-461.
Stock SP (2015). Diversity, biology and evolutionary relationships, In Campos-Herrera, R (Ed.), Nematode pathogeneses of insects and other pests. Switzerland: Springer International Publishing, 3-27.
Stuart RJ, Barbercheck ME, Grewal PS (2015). Entomopathogenic nematodes in the soil environment: distributions, interactions and the influence of biotic and abiotic factors. In CamposHerrera R (Editor). Nematode Pathogenesis of Insects and Other Pests: Ecology and Applied Technologies for Sustainable Plant and Crop Protection. Springer International Publishing, AG Switzerland, pp. 97-137.
Thiéry D, Louapre P, Muneret L, Rusch A, Sentenak G et al. (2018). Biological protection against grape berry moths. A review. Agronomy for Sustainable Development 38: 15.
Tobias NJ, Wolff H, Djahanschiri B, Grundmann F., Kronenwerth M et al. (2017). Natural product diversity associated with the nematode symbionts Photorhabdus and Xenorhabdus. Nature Microbiology 2: 1676-1685.
Valadas V, Laranjo M, Mota M, Oliveira S (2014). A survey of entomopathogenic nematode species in continental Portugal. Journal of Helminthology 88: 327-341.
Vicente-Díez I, Blanco-Pérez R, González-Trujillo MM, Pou A, Campos-Herrera R (2021). Insecticidal effect of entomopathogenic nematodes and the cell-free supernatant from their symbiotic bacteria against Philaenus spumarius (Hemiptera: Aphrophoridae) nymphs. Insects 12: 448.
Vieux PD, Malan AP (2015). Prospects for using entomopathogenic nematodes to control the vine mealybug, Planococcus ficus, in South African vineyards. South African Journal of Enology and Viticulture 36: 1.
Williams RN, Fickle DS, Grewal PS, Dutcher J (2010). Field efficacy against the grape root borer Vitacea polistiformis (Lepidoptera: Sesiidae) and persistence of Heterorhabditis zealandica and H. bacteriophora (Nematoda: Heterorhabditidae) in vineyards. Biological Control 53: 86-91.
Yan X, Zhao GY, Han R (2019). Integrated management of chive gnats (Bradysia odoriphaga Yang & Zhang) in chives using entomopathogenic nematodes and low-toxicity insecticides. Insects 10: 161.