[en] Root knot nematodes are the most devastating root pathogens, causing severe damage and serious economic losses to agriculture worldwide. Octanoic acid has been reported as one of the nematicides, and its mode of action is not fully understood. The main objective of this study was to elucidate the effect of octanoic acid on Meloidogyne incognita by transcriptomic analysis combined with physiological and biochemical assays. In the toxicity assays with octanoic acid, the threshold concentration with nematicidal activity and the maximum concentration to which nematodes could respond were 0.03 μL/mL and 0.08 μL/mL respectively. Microscopic observation combined with protein and carbohydrates assays confirmed that the structure of the second-stage juveniles (J2s) was severely disrupted after 72 h of immersion in octanoic acid. Transcriptome analysis has shown that octanoic acid can interfere with the nematode energy metabolism, lifespan and signaling. Although the effects are multifaceted, the findings strongly point to the cuticle, lysosomes, and extracellular regions and spaces as the primary targets for octanoic acid. In addition, nematodes can withstand the negative effects of low concentration of octanoic acid to some extent by up-regulating the defense enzyme system and heterologous metabolic pathways. These findings will help us to explore the nematicidal mechanism of octanoic acid and provide important target genes for the development of new nematicides in the future.
Disciplines :
Microbiology Biotechnology Agriculture & agronomy
Author, co-author :
Wang, Jian-Yu; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China, Qingdao Zipnow Agricultural Technology Co., Ltd, Qing'dao 266000, China
Li, Qiu-Yue; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China
Ren, Li; College of Resources and Environmental Sciences, China Agricultural University, Bei'jing 100193, China
Guo, Cheng; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China
Qu, Jianping ; Université de Liège - ULiège > TERRA Research Centre > Entomologie, Phytopathologie et Productions Innovantes (EPPI) ; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China
Gao, Zheng; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China. Electronic address: gaozheng@sdau.edu.cn
Wang, Hui-Fang; Institute of Plant Protection, Hainan Academy of Agricultural Sciences, Hai' kou 571100, China. Electronic address: wanghuifang@hnaas.org.cn
Zhang, Qian; Shandong Institute of Pomology, Tai'an 271018, China. Electronic address: sdsgsyjs@shandong.cn
Zhou, Bo; College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China, National Engineering Research Center for Efficient Utilization of Soil and Fertilizer, Tai'an 271018, China. Electronic address: zhoubo@sdau.edu.cn
Language :
English
Title :
Transcriptomic and physiological analysis of the effect of octanoic acid on Meloidogyne incognita.
This work was supported by the Key R&D project of Shandong Province ( 2020CXGC010803 ), Major Applied Agricultural Technology Innovation Projects of Shandong Province ( SD2019ZZ009 ), Key R&D project of Ningxia Hui Autonomous Region ( 2021BBF02006 ), Shandong Provincial Natural Science Foundation , China ( ZR2021MC183 ) and Modern Agricultural Industry Technology System of Shandong Province , China ( SDAIT-06-13 ), National Key Research and Development Program of China (No. 2018YFD0500202 ) and Agriculture Research System of China of MOF and MARA ( CARS-16-E18 ).
Abad, P., Gouzy, J., Aury, J., Castagnone-Sereno, P., Danchin, E.G.J., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V.C., Caillaud, M., Coutinho, P.M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J.V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T.R., Markov, G.V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., Sallet, E., Ségurens, B., Steinbach, D., Tytgat, T., Ugarte, E., van Ghelder, C., Veronico, P., Baum, T.J., Blaxter, M., Bleve-Zacheo, T., Davis, E.L., Ewbank, J.J., Favery, B., Grenier, E., Henrissat, B., Jones, J.T., Laudet, V., Maule, A.G., Quesneville, H., Rosso, M., Schiex, T., Smant, G., Weissenbach, J., Wincker, P., Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26 (2008), 909–915.
Anders, S., Huber, W., Differential Expression of RNA-Seq Data at the Gene Level - the DESeq Package. 2013, EMBL.
Anisimov, V.N., Bartke, A., The key role of growth hormone-insulin-IGF-1 signaling in aging and cancer. Crit. Rev. Oncol. Hemat. 87 (2013), 201–223.
Bansal, R.K., Bajaj, A., Effect of volatile fatty acids on embryogenesis and hatching of Meloidogyne incognita eggs. Nematol. Medit. 31 (2003), 135–140.
Bi, Y., Gao, C., Yu, Z., Rhabdopeptides from Xenorhabdus budapestensis SN84 and their nematicidal activities against Meloidogyne incognita. J. Agr. Food Chem. 66 (2018), 3833–3839.
Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
Brenner, S., The genetics of Caenorhabditis elegans. Genetics 77 (1974), 71–94.
Carmona-Gutierrez, D., Hughes, A.L., Madeo, F., Ruckenstuhl, C., The crucial impact of lysosomes in aging and longevity. Age. Res. Rev. 32 (2016), 2–12.
Chelinho, S., Maleita, C.M.N., Francisco, R., Braga, M.E.M., da Cunha, M.J.M., Abrantes, I., Sousa, J.P., Toxicity of the bionematicide 1,4-naphthoquinone on non-target soil organisms. Chemosphere 181 (2017), 579–588.
Cheng, W., Yang, J., Nie, Q., Huang, D., Yu, C., Zheng, L., Cai, M., Thomashow, L.S., Weller, D.M., Yu, Z., Zhang, J., Volatile organic compounds from Paenibacillus polymyxa KM2501-1 control Meloidogyne incognita by multiple strategies. Sci. Rep., 2017, 7.
Collange, B., Navarrete, M., Peyre, G., Mateille, T., Tchamitchian, M., Root-knot nematode (Meloidogyne) management in vegetable crop production: the challenge of an agronomic system analysis. Crop Prot. 30 (2011), 1251–1262.
Dziki, J.L., Hussey, G., Badylak, S.F., Alarmins of the extracellular space. Semin. Immunol. 38 (2018), 33–39.
El Aimani, A., Houari, A., Laasli, S., Mentag, R., Iraqi, D., Diria, G., Khayi, S., Lahlali, R., Dababat, A.A., Mokrini, F., Antagonistic potential of Moroccan entomopathogenic nematodes against root-knot nematodes, Meloidogyne javanica on tomato under greenhouse conditions. Sci. Rep., 2022, 12.
Engelbrecht, G., Horak, I., Jansen, Van, Rensburg, P.J., Claassens, S., Bacillus-based bionematicides: development, modes of action and commercialisation. Biocontrol. Sci. Techn. 28 (2018), 629–653.
Fetterer, R.H., Rhoads, M.L., Biochemistry of the nematode cuticle: relevance to parasitic nematodes of livestock. Vet. Parasitol., 46, 1993, 103.
Fournier, D., Mutero, A., Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp. Biochem. Phys. 108 (1994), 19–31.
Gao, H., Qi, G., Yin, R., Zhang, H., Li, C., Zhao, X., Bacillus cereus strain S2 shows high nematicidal activity against Meloidogyne incognita by producing sphingosine. Sci. Rep., 6, 2016, 28756.
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., Regev, A., Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotech. 29 (2011), 644–652.
Griffith, M., Walker, J.R., Spies, N.C., Ainscough, B.J., Griffith, O.L., Informatics for RNA sequencing: a web resource for analysis on the cloud. PLoS Comput. Biol., 11, 2015, e1004393.
Hartman, J.H., Widmayer, S.J., Bergemann, C.M., King, D.E., Morton, K.S., Romersi, R.F., Jameson, L.E., Leung, M.C., Andersen, E.C., Taubert, S., Meyer, J.N., Xenobiotic metabolism and transport in Caenorhabditis elegans. J. Toxicol. Environ. Health 24 (2021), 51–94.
Hemingway, J., The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem. Mol. Biol. 30 (2000), 1009–1015.
Hüter, O.F., Use of natural products in the crop protection industry. Phytochem. Rev. 10 (2011), 185–194.
Jagdale, S., Rao, U., Giri, A.P., Effectors of root-knot nematodes: an arsenal for successful parasitism. Front. Plant Sci., 12, 2021.
Jeon, B.S., Kim, S., Sang, B., Megasphaera hexanoica sp. nov., a medium-chain carboxylic acid-producing bacterium isolated from a cow rumen. Int. J. Syst. Evol. Micr. 67 (2017), 2114–2120.
Kaletta, T., Hengartner, M.O., Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 5 (2006), 387–398.
Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T., Yamanishi, Y., KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36 (2007), D480–D484.
Kang, J.S., Moon, Y., Lee, S.H., Park, I., Inhibition of acetylcholinesterase and glutathione S-transferase of the pinewood nematode (Bursaphelenchus xylophilus) by aliphatic compounds. Pestic. Biochem. Phys. 105 (2013), 184–188.
Kaur, T., Jasrotia, S., Ohri, P., Manhas, R.K., Evaluation of in vitro and in vivo nematicidal potential of a multifunctional streptomycete, Streptomyces hydrogenans strain DH16 against Meloidogyne incognita. Microbiol. Res. 192 (2016), 247–252.
Kearn, J., Lilley, C., Urwin, P., O'Connor, V., Holden-Dye, L., Progressive metabolic impairment underlies the novel nematicidal action of fluensulfone on the potato cyst nematode Globodera pallida. Pestic. Biochem. Phys. 142 (2017), 83–90.
Kenyon, C., Chang, J., Gensch, E., Rudner, A., Tabtiang, R.A., C. elegans mutant that lives twice as long as wild type. Nature 366 (1993), 461–464.
Kim, D., Langmead, B., Salzberg, S.L., HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12 (2015), 357–360.
Kim, T.Y., Jang, J.Y., Jeon, S.J., Lee, H.W., Bae, C., Yeo, J.H., Lee, H.B., Kim, I.S., Park, H.W., Kim, J., Nematicidal activity of kojic acid produced by Aspergillus oryzae against Meloidogyne incognita. J. Microbiol. Biotechnol. 26 (2016), 1383–1391.
Kooliyottil, R., Rao, G.K., Solo, N., Dandurand, L.M., ATP-binding cassette (ABC) transporter genes in plant-parasitic nematodes: an opinion for development of novel control strategy. Front. Plant Sci., 11, 2020.
Kumarasingha, R., Young, N.D., Yeo, T., Lim, D.S.L., Tu, C., Palombo, E.A., Shaw, J.M., Gasser, R.B., Boag, P.R., Transcriptional alterations in Caenorhabditis elegans following exposure to an anthelmintic fraction of the plant Picria fel-terrae Lour. Parasite. Vector., 2019, 12.
Kwok, O.C., Plattner, R., Weisleder, D., Wicklow, D.T., A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J. Chem. Ecol. 18 (1992), 127–136.
Lamovšek, J., Urek, G., Trdan, S., Biological control of root-knot nematodes (Meloidogyne spp.): microbes against the pests. Acta Agric. Slov., 101, 2013.
Laquale, S., Avato, P., Argentieri, M.P., Candido, V., Perniola, M.D., Addabbo, T., Nematicidal activity of Echinacea species on the root-knot nematode Meloidogyne incognita. J. Pest Sci. 93 (2020), 1397–1410.
Lawrence, R.E., Zoncu, R., The lysosome as a cellular centre for signalling, metabolism and quality control. Nat. Cell Biol. 21 (2019), 133–142.
Li, J., Zou, C., Xu, J., Ji, X., Niu, X., Yang, J., Huang, X., Zhang, K., Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 53 (2015), 67–95.
Li, X., Liu, Q., Lewis, E.E., Tarasco, E., Activity changes of antioxidant and detoxifying enzymes in Tenebrio molitor (Coleoptera: Tenebrionidae) larvae infected by the entomopathogenic nematode Heterorhabditis beicherriana (Rhabditida: Heterorhabditidae). Parasitol. Res. 115 (2016), 4485–4494.
Lu, C., Meng, Y., Wang, Y., Zhang, T., Yang, G., Mo, M., Ji, K., Liang, L., Zou, C., Zhang, K., Survival and infectivity of second-stage root-knot nematode Meloidogyne incognita juveniles depend on lysosome-mediated lipolysis. J. Biol. Chem., 298, 2022, 101637.
Murungi, L.K., Kirwa, H., Coyne, D., Teal, P.E.A., Beck, J.J., Torto, B., Identification of key root volatiles signaling preference of tomato over spinach by the root knot nematode Meloidogyne incognita. J. Agr. Food Chem. 66 (2018), 7328–7336.
Naz, I., Khan, R.A.A., Masood, T., Baig, A., Siddique, I., Haq, S., Biological control of root knot nematode, Meloidogyne incognita, in vitro, greenhouse and field in cucumber. Biol. Control, 152, 2021, 104429.
Neupane, S., Mathew, F.M., Varenhorst, A.J., Nepal, M.P., Transcriptome profiling of interaction effects of soybean cyst nematodes and soybean aphids on soybean. Sci. Data, 2019, 6.
Nguyen, L.T.T., Jang, J.Y., Kim, T.Y., Yu, N.H., Park, A.R., Lee, S., Bae, C., Yeo, J.H., Hur, J., Park, H.W., Kim, J., Nematicidal activity of verrucarin A and roridin A isolated from Myrothecium verrucaria against Meloidogyne incognita. Pestic. Biochem. Phys. 148 (2018), 133–143.
Niu, Q., Huang, X., Zhang, L., Xu, J., Yang, D., Wei, K., Niu, X., An, Z., Bennett, J.W., Zou, C., Yang, J., Zhang, K.Q., A Trojan horse mechanism of bacterial pathogenesis against nematodes. Proc. Natl. Acad. Sci. USA 107 (2010), 16631–16636.
Rajasekharan, S.K., Kim, S., Kim, J., Lee, J., Nematicidal activity of 5-iodoindole against root-knot nematodes. Pestic. Biochem. Phys. 163 (2020), 76–83.
Seo, S., Kim, J., Koh, S., Ahn, Y., Park, I., Nematicidal activity of natural ester compounds and their analogues against pine wood nematode, Bursaphelenchus xylophilus. J. Agr. Food Chem. 62 (2014), 9103–9108.
Sun, Y., Li, M., Zhao, D., Li, X., Yang, C., Wang, X., Lysosome activity is modulated by multiple longevity pathways and is important for lifespan extension in C.elegans. eLife, 9, 2020, e55745.
Tani, M., Ito, M., Igarashi, Y., Ceramide/sphingosine/sphingosine 1-phosphate metabolism on the cell surface and in the extracellular space. Cell. Signal. 19 (2007), 229–237.
Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotech. 28 (2010), 511–515.
Wang, J.Y., Guo, C., Zhao, P., Yu, F.Y., Su, Y., Qu, J.P., Wang, J.L., Lin, R.S., Wang, B., Gao, Z., Yang, Z.Y., Zhou, B., Biocontrol potential of Bacillus altitudinis AMCC1040 against root-knot nematode disease of ginger and its impact on rhizosphere microbial community. Biol. Control, 158, 2021, 104598.
Wu, H.D., Liu, Q.Z., Li, X.Y., Wang, Y.L., Zhang, H., Activities of four enzymes in Galleria mellonella larvae infected with entomopathogenic nematode Heterorhabditis beicherriana n. sp. African J. Agr. Res. 8 (2013), 3245–3250.
Ye, L., Wang, J.Y., Liu, X.F., Guan, Q., Dou, N.X., Li, J., Zhang, Q., Gao, Y.M., Wang, M., Li, J.S., Zhou, B., Nematicidal activity of volatile organic compounds produced by Bacillus altitudinis AMCC 1040 against Meloidogyne incognita. Arch. Microbiol., 204, 2022, 521.
Yeon, J., Park, A.R., Kim, Y.J., Seo, H.J., Yu, N.H., Ha, S., Park, H.W., Kim, J., Control of root-knot nematodes by a mixture of maleic acid and copper sulfate. Appl. Soil Ecol. 141 (2019), 61–68.
Zhang, B., Helen, H.S., Wang, J., Liu, H., Performance and enzyme activity of beet armyworm Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) under various nutritional conditions. Agr. Sci. China 10 (2011), 737–746.
Zhang, W., Ruan, W., Deng, Y., Gao, Y., Potential antagonistic effects of nine natural fatty acids against Meloidogyne incognita. J. Agr. Food Chem. 60 (2012), 11631–11637.
