Negative regulation of root-knot nematode parasitic behavior by root-derived volatiles of wild relatives of Cucumis metuliferus CM3

Abstract

Root-knot nematodes (RKN; Meloidogyne spp.) cause a significant decrease in the yield of cucumber crops every year. Cucumis metuliferus is an important wild germplasm that has resistance to RKN in which plant root volatiles are thought to play a role. However, the underlying molecular mechanism is unclear. To investigate it, we used the resistant C. metuliferus line CM3 and the susceptible cucumber line Xintaimici (XTMC). CM3 roots repelled Meloidogyne incognita second-stage larvae (J2s), while the roots of XTMC plants attracted the larvae. CM3 and XTMC were found to contain similar amounts of root volatiles, but many volatiles, including nine hydrocarbons, three alcohols, two aldehydes, two ketones, one ester, and one phenol, were only detected in CM3 roots. It was found that one of these, (methoxymethyl)-benzene, could repel M. incognita , while creosol and (Z)-2-penten-1-ol could attract M. incognita . Interestingly, creosol and (Z)-2-penten-1-ol effectively killed M. incognita at high concentrations. Furthermore, we found that a mixture of CM3 root volatiles increased cucumber resistance to M. incognita . The results provide insights into the interaction between the host and plant-parasitic nematodes in the soil, with some compounds possibly acting as nematode biofumigation, which can be used to manage nematodes.

References

[1] Trudgill DL, Blok VC . Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol. 2001; 39: 53-77.

[2] Jones JT, Haegeman A, Danchin EGJ et al. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol. 2013; 14: 946-61.

[3] Taylor AL, Sasser JN . Biology, Identification and Control of Root-Knot Nematodes (Meloidogyne Species) . Raleigh, NC: Department of Plant Pathology, North Carolina State University and United States Agency for International Development; 1978.

[4] Bebber DP, Holmes T, Smith D et al. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 2014; 202: 901-10.

[5] Murungi LK, Kirwa H, Coyne D et al. Identification of key root volatiles signaling preference of tomato over spinach by the root knot nematode Meloidogyne incognita . J Agric Food Chem. 2018; 66: 7328-36.

[6] Yang G, Zhou B, Zhang X et al. Effects of tomato root exudates on Meloidogyne incognita . PLoS One. 2016; 11: e0154675.

[7] Kihika R, Murungi LK, Coyne D et al. Parasitic nematode Meloidogyne incognita interactions with different Capsicum annum cultivars reveal the chemical constituents modulating root herbivory . Sci Rep. 2017; 7: 2903.

[8] Kirwa HK, Murungi LK, Beck JJ et al. Elicitation of differential responses in the root-knot nematode Meloidogyne incognita to tomato root exudate cytokinin, flavonoids, and alkaloids. J Agric Food Chem. 2018; 66: 11291-300.

[9] Pedroso LA, Campos VP, Pedroso MP et al. Volatile organic compounds produced by castor bean cake incorporated into the soil exhibit toxic activity against Meloidogyne incognita . Pest Manag Sci. 2019; 75: 476-83.

[10] Gao ZH, Zhang H, Cao C et al. QTL mapping for cucumber fruit size and shape with populations from long and round fruited inbred lines. Hortic Plant J. 2020; 6: 132-44.

[11] Ornat C, Verdejo-Lucas S, Sorribas FJ . Effect of the previous crop on population densities of Meloidogyne javanica and yield of cucumber. Nematropica. 1997; 27: 85-90.

[12] Cheng CY, Wang X, Liu X et al. Candidate genes underlying the quantitative trait loci for root-knot nematode resistance in a Cucumis hystrix introgression line of cucumber based on population sequencing. J Plant Res. 2019; 132: 813-23.

[13] Exposito A, Munera M, Giné A et al. Cucumis metuliferus is resistant to root-knot nematode Mi1.2 gene (a)virulent isolates and a promising melon rootstock . Plant Pathol. 2018; 67: 1161-7.

[14] Faske TR . Penetration, post-penetration development, and reproduction of Meloidogyne incognita on Cucumis melo var. texanus . J Nematol. 2013; 45: 58-65.

[15] Chen JF, Moriarty G, Jahn M et al. Some disease resistance tests in Cucumis hystrix and its progenies from interspecific hybridization with cucumber. In: Proceedings of Cucurbitaceae 2004, the 8th EUCARPIA Meeting on Cucurbit Genetics and Breeding, Palacky University, Olomouc (Czech Republic), 2004, pp 189-196.

[16] Fassuliotis G . Resistance of Cucumis spp. to the root-knot nematode, Meloidogyne incognita acrita . J Nematol 1970; 2: 174.

[17] Ye DY, Qi YH, Cao SF et al. Histopathology combined with transcriptome analyses reveals the mechanism of resistance to Meloidogyne incognita in Cucumis metuliferus . J Plant Physiol. 2017; 212: 115-24.

[18] Ma JH, Zuo ZC, Li HX et al. Resistance identification of Cucumis metuliferus to Meloidogyne incognita and characteristic analysis . Acta Hortic Sinica. 2014; 1: 73-9.

[19] Kihika R, Tchouassi DP, Ng’ang’a MM et al. Compounds associated with infection by the root-knot nematode, Meloidogyne javanica, influence the ability of infective juveniles to recognize host plants. J Agric Food Chem. 2020; 68: 9100-9.

[20] Qi W, Wang H, Zhou Z et al. Ethylene emission as a potential indicator of Fuji apple flavor quality evaluation under low temperature. Hortic Plant J. 2020; 6: 231-9.

[21] Wang L, Qian C, Bai J et al. Difference in volatile composition between the pericarp tissue and inner tissue of tomato (Solanum lycopersicum) fruit . J Food Process Preserv. 2018; 42: e13387.

[22] Wang LB, Baldwin EA, Zhao W et al. Suppression of volatile production in tomato fruit exposed to chilling temperature and alleviation of chilling injury by a pre-chilling heat treatment. Lwt-Food Sci Technol. 2015; 62: 115-21.

[23] Bett B, Randolph TF, Irungu P et al. Field trial of a synthetic tsetse-repellent technology developed for the control of bovine trypanosomosis in Kenya. Prev Vet Med. 2010; 97: 220-7.

[24] Masiga DK, Igweta L, Saini R et al. Building endogenous capacity for the management of neglected tropical diseases in Africa: the pioneering role of ICIPE. PLoS Negl Trop Dis. 2014; 8: e2687.

[25] Nyalala SO, Petersen MA, Grout BWW . Volatile compounds from leaves of the African spider plant (Gynandropsis gynandra) with bioactivity against spider mite (Tetranychus urticae) . Ann Appl Biol. 2013; 162: 290-8.

[26] Perry RN, Moens M, Starr JL . Root-knot Nematodes . Wallingford: CABI; 2009.

[27] Li X, Sun Y, Yang Y et al. Transcriptomic and histological analysis of the response of susceptible and resistant cucumber to Meloidogyne incognita infection revealing complex resistance via multiple signaling pathways. Front Plant Sci. 2021; 12: 675429.

[28] Ling J, Mao Z, Zhai M et al. Transcriptome profiling of Cucumis metuliferus infected by Meloidogyne incognita provides new insights into putative defense regulatory network in Cucurbitaceae . Sci Rep. 2017; 7: 3544.

[29] Wehner TC, Walters SA, Barker KR . Resistance to root-knot nematodes in cucumber and horned cucumber. J Nematol. 1991; 23: 611.

[30] Weng Y . Genetic diversity among Cucumis metuliferus populations revealed by cucumber microsatellites. Hortic Sci. 2010; 45: 214-9.

[31] Höckelmann C, Jüttner M . Odor compounds from cyanobacterial biofilms acting as attractants and repellents for free-living nematodes. Limnol Oceanogr. 2004; 49: 1809-19.

[32] Klingler J . On the orientation of plant nematodes and of some other soil animals. Nematologica. 1965; 11: 4-18.

[33] Sikder MM, Vestergard M . Impacts of root metabolites on soil nematodes. Front Plant Sci. 2019; 10: 1792.

[34] Exposito A, Garcia S, Gine A et al. Cucumis metuliferus reduces Meloidogyne incognita virulence against the Mi1.2 resistance gene in a tomato-melon rotation sequence . Pest Manag Sci. 2019; 75: 1902-10.

[35] Ye D, Jiang Y, Wang C et al. Expression analysis of microRNAs and their target genes in Cucumis metuliferus infected by the root-knot nematode Meloidogyne incognita . Physiol Mol Plant Pathol. 2020; 111: 101491.

[36] Birkett M, Dutta TK, Powers SJ et al. Effect of small lipophilic molecules in tomato and rice root exudates on the behaviour of Meloidogyne incognita and M. graminicola . Nematology. 2012; 14: 309-20.

[37] Dias MC, Perpétuo S, Cabral AT et al. Effects of Solanum sisymbriifolium on potato cyst nematode populations in Portugal. Plant Soil. 2017; 4: 211-4.

[38] Dong L, Li X, Huang C et al. Reduced Meloidogyne incognita infection of tomato in the presence of castor and the involvement of fatty acids. Sci Hortic. 2018; 237: 169-75.

[39] Farnier K, Bengtsson M, Becher PG et al. Novel bioassay demonstrates attraction of the white potato cyst nematode Globodera pallida (Stone) to non-volatile and volatile host plant cues. J Chem Ecol. 2012; 38: 795-801.

[40] Shivakumara TN, Dutta TK, Rao U . A novel in vitro chemotaxis bioassay to assess the response of Meloidogyne incognita towards various test compounds. J Nematol. 2018; 50: 487-94.

[41] Thoden T, Boppré M, Hallmann J . Pyrrolizidine alkaloids of Chromolaena odorata act as nematicidal agents and reduce infection of lettuce roots by Meloidogyne incognita . Nematology. 2007; 9: 343- 9.

[42] Wuyts N, Swennen R, Waele DD . Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita . Nematology. 2006; 8: 89-101.

[43] Zhao X, Schmitt M, Hawes MC . Species-dependent effects of border cell and root tip exudates on nematode behavior. Phytopathology. 2000; 90: 1239-45.

[44] Barros AF, Campos V, Silva JCP et al. Nematicidal activity of volatile organic compounds emitted by Brassica juncea, Azadirachta indica, Canavalia ensiformis, Mucuna pruriens and Cajanus cajan against Meloidogyne incognita . Appl Soil Ecol. 2014; 80: 34-43.

[45] Mojtahedi H . Managing Meloidogyne chitwoodi on potato with rapeseed as green manure. Plant Dis. 1993; 77: 42.

[46] Lord JS, Lazzeri L, Atkinson HJ et al. Biofumigation for control of pale potato cyst nematodes: activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil . J Agric Food Chem. 2011; 59: 7882-90.

[47] Wu H, Wang CJ, Bian XW et al. Nematicidal efficacy of isothiocyanates against root-knot nematode Meloidogyne javanica in cucumber. Crop Prot. 2011; 30: 33-7.

[48] Ntalli N, Caboni P . A review of isothiocyanates biofumigation activity on plant parasitic nematodes. Phytochem Rev. 2017; 16: 827-34.