Phytoparasitic nematodes of three enegry crops for biofuel production

A. Lutsiuk
Abstract

The literature review focuses on a comprehensive analysis of scientific research aimed at studying the interaction of phytoparasitic nematodes with energy crops such as Miscanthus, Jerusalem artichoke, and paulownia, as well as examining the factors influencing the spread of these nematodes in cultivation systems of three biofuel crops: giant Miscanthus, velvetleaf, and Jerusalem artichoke. The research is grounded in analyzing the interaction between nematodes and the yield of these crops, along with the potential positive impact of nematode communities from different trophic groups on soil quality and phytoremediation. Special attention is given to phytoparasitic nematodes, which are among the most widespread soil pests of plants. Considering the interaction between nematodes and energy crops is crucial for developing resilient and efficient cultivation systems that ensure high yields and preserve the biodiversity of soil ecosystems.The research concludes that phytoparasitic nematodes have a significant negative impact on the cultivation of energy crops, particularly giant miscanthus. However, certain climatic, chemical, and physical conditions are conducive to the formation of nematode communities that can positively affect soil quality and maintain its fertility. The review provides an overview of three energy crops for biofuel production (giant Miscanthus, velvetleaf, and Jerusalem artichoke), highlighting the nematode pests associated with each of these crops, which have been found in the rhizosphere of plants over many years of published research. Attention is also given to the negative impact of phytoparasitic nematodes on the cultivation of energy crops, especially Miscanthus. However, it has been observed that certain climatic, chemical, and physical conditions favor the formation of nematode communities that can positively influence soil quality and maintain its fertility. This work is significant for the development of strategies to manage the population levels of various trophic levels of nematodes, especially phytoparasitic ones, particularly in the context of cultivating promising energy crops for biofuel production. Additionally, the review describes the important influence of phytoremediation on the population of nematode communities in the soil. The obtained results can serve as a basis for further research in this field and the implementation of effective methods to preserve soil fertility and increase the productivity of energy crops. Furthermore, the findings of this literature review can contribute to the development of environmentally sustainable methods for cultivating energy crops, thereby aiding in the conservation of natural resources and reducing the impact of agricultural activities on the environment

Keywords

phytoparasitic nematodes; energy crops; phytoremediation; Miscanthus giganteus; Paulownia tomentosa; Jerusalem artichoke; biofuel

Suggested citation
Lutsiuk, A. (2024). Phytoparasitic nematodes of three enegry crops for biofuel production. Biological Systems: Theory and Innovation, 15(2), 60-75. https://doi.org/10.31548/biologiya15(2).2024.006
References

[1] Akyildiz, M.H., & Sahil, K.H. (2010). Some technological properties and uses of paulownia (Paulownia tomentosa Steud.) wood. Journal of Environmental Biology, 31(3), 351-355. Retrieved from https://pubmed.ncbi.nlm.nih.gov/21047010/.

[2] al Souki, K.S., Burdová, H., Mamirova, A., & Kuráň, P. (2021). Evaluation of the Miscanthus x giganteus short term impacts on enhancing the quality of agricultural soils affected by single and/or multiple contaminants. Environmental Technology & Innovation, 24, article number 101890. doi: 10.1016/j.eti.2021.101890.

[3] Alasmary, Z., Todd, T., Hettiarachchi, G., & Stefanovska, T. (2020). Effect of soil treatments and amendments on the nematode community under miscanthus growing in a lead contaminated military site. Agronomy, 10(11), 1-18, article number 1727. doi: 10.3390/agronomy10111727.

[4] Aloi, F., Riolo, M., la Spada, F., & Bentivenga, G. (2021). Phytophthora root and collar rot of Paulownia, a new disease for Europe. Forests, 12(12), article number 1664. doi: 10.3390/f12121664.

[5] Bouwman, L.A. (1994). The ecology of bacterivorous protozoans and nematodes in arable soil. Agriculture Ecosystems & Environment, 51(1–2), 145-160. doi: 10.1016/0167-8809(94)90040-X.

[6] Briar, S.S., Wichman, D., & Reddy, G. (2016). Plant-parasitic nematode problems in organic agriculture. In Organic Farming for Sustainable Agriculture (pp. 107-122) Berlin: Springer. doi: 10.1007/978-3-319-26803-3_5.

[7] Buzan, R.L., Maxim, A., Odagiu, A., & Balint, C. (2018). Paulownia sp. used as an energetic plant, for the phytoremediation of soils and in agroforestry systems. Academic Journaldoi: 10.3390/toxics10080465.

[8] Christian, D.G., Riche, A.B., & Yates, N.E. (2008). Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests. Industrial Crops and Products, 13(4), 344-360. doi: 10.1016/j.indcrop.2008.02.009.

[9] Cumagun, C.J.R., & Moosavi, M. (2015). Significance of biocontrol agents of phytonematodes. Biocontrol Agents of Phytonematodes, 2, 50-78. doi: 10.1079/9781780643755.0050.

[10] Cunningham, S.D., Shann, J.R., Crowley, D., & Anderson, T. (1997). Phytoremediation of contaminated water and soil. In ACS Symposium Series (pp. 2-17). Washington: American Chemical Society. doi: 10.1021/bk-1997-0664.ch001.

doi: 10.3390/en15114157.

[11] Ekanayake, R.H.M. (1996). Nematode parasites on agricultural crops and their distribution in Sri Lanka. Japan International Research Center for Agricultural Sciences Journal, 4, 29-39.
Retrieved from https://www.jircas.go.jp/sites/default/files/publication/jircas_journal/jircas_journal4-_29-39.pdf.

[12] Esteves, B., Cruz-Lopez, L., Viana, H., & Ferreira, J.V. (2022). The influence of age on the wood properties of Paulownia tomentosa (Thunb.) steud. Toxics, 10(8), article number 700. doi: 10.3390/f13050700.

[13] Ferris, H. (2010). Contribution of nematodes to the structure and function of the soil food web. Journal of Nematology, 42(1), 63-67. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380510/pdf/63.pdf.

[14] Gebremikael, M.T., Steel H., Buchan, D., & Bert, W. (2016). Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Scientific Reports, 6, article number 32862. doi: 10.1038/srep32862.

[15] Georgieva, S., McGrath, S., Hooper, D., & Chambers, B. (2002). Nematode Communities under stress: The long-term effects of heavy metals in soil treated with sewage sludge. Applied Soil Ecology, 20(1), 27-42. doi: 10.1016/S0929-1393(02)00005-7.

[16] Gunnarson, S. (1985). Jerusalem artichoke (Helianthus tuberosus L.) for biogas production. Biomass, 7(2), 85-97. doi: 10.1016/01444565(85)90036-8.

[17] Gunnarsson, I.B., Svensson, S., Johansson, E., & Karakashev, D. (2014). Potential of Jerusalem artichoke (Helianthus tuberosus L.) as a biorefinery crop. Industrial Crops and Products, 56, 231-240. doi: 10.1016/j.indcrop.2014.03.010.

[18] Hailu, F.A., & Hailu, Y.A. (2020). Agro-Ecological Importance of Nematodes (round worms). Acta Scientific Agriculture, 4(1), 156-162. Retrieved from https://actascientific.com/ASAG/pdf/ASAG-04-0763.pdf

[19] Heaton, E.A., Dohleman, F.G., & Long, S.P. (2008). Meeting US biofuel goals with less land: The potential of MiscanthusGlobal Change Biology, 14(9), 2000-2014. doi: 10.1111/j.1365-2486.2008.01662.x.

[20] Heaton, E.A., Dohleman, F.G., Juvik, J.A., Lozovaya, V., et. al. (2010). Miscanthus: A promising biomass crop. Advances in Botanical Research, 56, 75-137. doi: 10.1016/B978-0-12-381518-7.00003-0.

[21] Hecker, U. (2008). Enzyklopädie der Holzgewächse: Handbuch und atlas der dendrologie. Wangheim: Wiley-VCH.

[22] Heletukha, H.H. (2016). Analysis of criteria for the sustainable development of bioenergy. Industrial Heat Engineering, 38(6), 47-55. doi: 10.31472/ihe.6.2016.07.

[23] Jakubowski, M. (2022). Cultivation potential and uses of paulownia wood: A review. Forests, 13(5), article number 668. doi: 10.3390/f13050668.

[24] Jezierska-Thöle, A., Rudnicki, R., & Kluba, M. (2016). Development of energy crops cultivation for biomass production in Poland. Renewable and Sustainable Energy Reviews, 62, 534-545. doi: 10.1016/j.rser.2016.05.024.

[25] Khandelwal, G., Chaudhary, V., Iyer, R., & Dwivedi, A. (2022). Soil bacteria and nematodes for bioremediation and amelioration of polluted soil. In Microbial and Biotechnological Interventions in Bioremediation and Phytoremediation (pp. 57-79). Berlin: Springer. doi: 10.1007/978-3-031-08830-8_3.

[26] Koppenhöfer, A.M. (Eds). (2007). Field manual of techniques in invertebrate pathology. Entomologia Experimentalis et Applicata. Berlin: Springer. doi: 10.1007/978-1-4020-5933-9.

[27] Lewandowski, I., Scurlock, J., Lindvall, E., & Myrsini, C. (2003). The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy, 25(4), 335-361. doi: 10.1016/S0961-9534(03)00030-8.

[28] Li, J., Wu, X., Gebremikael, M.T., & Wu, H. (2018). Response of soil organic carbon fractions, microbial community composition and carbon mineralization to high-input fertilizer practices under an intensive agricultural system. Plos One, 13(4), p. 0195144. doi: 10.1371/journal.pone.0195144.

[29] Liu, T., Hu, F., & Li, H. (2019). Spatial ecology of soil nematodes: Perspectives from global to micro scales. Soil Biology and Biochemistry, 137, article number 107565. doi: 10.1016/j.soilbio.2019.107565.

[30] López, F., Pérez, A., Zamudio, M., & de Alva, H. (2012). Paulownia as raw material for solid biofuel and cellulose pulp. Biomass and Bioenergy, 45, 77-86. doi: 10.1016/j.biombioe.2012.05.010.

[31] Lv, S., Wang, R., Xiao, Y., & Li, F. (2019). Growth, yield formation, and inulin performance of a non-food energy crop, Jerusalem artichoke (Helianthus tuberosus L.), in a semi-arid area of China. Environment Biodiversity and Soil Security, 4(4), 71-79. doi: 10.1016/j.indcrop.2019.03.064.

[32] Machado, R., & von Reuss Н.S. (2022). Chemical ecology of nematodes. Chemical Ecology 76(11), article number 945. doi: 10.2533/chimia.2022.945.

[33] McCarthy, S.M. (1995). Progress in commercial development of Miscanthus in England. In A.A. Chartier, C.M. Beenackers & G. Grassi (Eds.), Biomass for energy, environment, agriculture and industry: Proceedings of the 8th european biomass conference (pp. 1-63). Vienna: Pergamon.  

[34] McQueen, P.J., & Treonis, A.M. (2019). Cacao agroforestry in Belize: Effects on soil nematode community structure. Agroforestry Systems, 94, 1123-1132. doi: 10.1007/s10457-019-00477-2.

[35] Mekete, T. (2011). Plant Disease Plant-Parasitic Nematodes Are Potential Pathogens of Miscanthus×Giganteusand and Panicum virgatum used for biofuels. The American Phytopathological Society, 95(4), 413-418. doi: 10.1094/PDIS-05-10-0335.

[36] Meketem, T., & Lopez-Nicora, H. (2011). Plant-parasitic nematodes are potential pathogens of Miscanthus×giganteus and Panicum virgatum used for biofuels. Plant Disease, 95(4), 413-418. doi: 10.1094/PDIS-05-10-0335.

[37] Mohamad, M.E., Awad, A.A., Majrashi, A., abd Esadek, O.A. (2022). In vitro study on the effect of cytokines and auxins addition to growth medium on the micropropagation and rooting of Paulownia species (Paulownia hybrid and Paulownia tomentosa). Saudi Journal of Biological Sciences, 29(3), 1598-1603. doi: 10.1016/j.sjbs.2021.11.003.

[38] Mokrzycki, J., Magdziarz, A., & Rutkowski, P. (2022). The influence of the Miscanthus giganteus pyrolysis temperature on the application of obtained biochars as solid biofuels and precursors of high surface area activated carbons. Biomass and Bioenergy, 164, article number 106550. doi: 10.1016/j.biombioe.2022.106550.

[39] Morand, S., Nadler, S., & Skorping, A. (2015). Nematode life-traits diversity in the light of their phylogenetic diversification. Parasite Diversity and Diversification, 473-479. doi: 10.1017/CBO9781139794749.017.

[40] Moura, G., & Franzener, G. (2017). Biodiversity of nematodes biological indicators of soil quality in the agroecosystems, 84(1–8), p. 0142015. doi: 10.1590/1808-1657000142015.

[41] Nabih, M.I., Bloem, G., & Poiesz, T. (1997). Conceptual issues in the study of innovation Adoption Behaviour. Retrieved from https://www.tcrwebsite.org/volumes/8041/volumes/v24/NA-24.

[42] Nacoon, S., Jogloy, S., Riddech, N., & Mongkolthanaruk, W. (2020). Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of Helianthus tuberosus L. Scentific Reports, 10(1), article number 4916.
doi: 10.1038/s41598-020-61846-x.

[43] Neher, D.A. (2001). Role of nematodes in soil health and their use as indicators. The Journal of Nematology, 33(4), 161-168. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2620512/pdf/161.pdf.

[44] Nisa, R.U., Kouser, N., Tantray, A.Y., & Allie, K. (2021). Influence of ecological and edaphic factors on biodiversity of soil nematodes. Saudi Journal of Biological Sciences, 28(5), 3049-3059. doi: 10.1016/j.sjbs.2021.02.046.

[45] Ntalli, N., Adamski, Z., Doula, M., & Monokrousos, N. (2020). Nematicidal amendments and soil remediation. Plants, 9(4), article number 429. doi: 10.3390/plants9040429.

[46] Nykyri, J., Fang, X., Dorati, F., & Bakr, R. (2013). Evidence that nematodes may vector the soft rot-causing enterobacterial phytopathogens. Plant Pathology, 63(4), 747-757. doi: 10.1111/ppa.12159.

[47] Ouattara, M.S., Laurent, A., Barbu, C.M., & Berthou, M. (2020). Effects of several establishment modes of Miscanthus×giganteus and Miscanthus sinensis on yields and yield trends. GCB – Bioenergy, 12(7), 524-538. doi: 10.1111/gcbb.12692.

[48] Pan, L., Sinden, M.R., Kennedy, A.H., & Chai, H. (2009). Bioactive constituents of Helianthus tuberosus (Jerusalem artichoke). Phytochemistry Letters, 2(1), 15-18. doi: 10.1016/j.phytol.2008.10.003.

[49] Pidlisnyuk, V., Stefanovska, T., Lewis, E.E., & Erickson, L.E. (2014). Miscanthus as a productive biofuel crop for phytoremediation. Critical Reviews in Plant Sciences, 33(1), 1-19. doi: 10.1080/07352689.2014.847616.

[50] Pidlisnyuk, V.V., Erickson, L.E., Trögl, J., & Shapoval, P. (2017). Metals uptake behaviour in Miscanthus×giganteus plant during growth at the contaminated soil from the military site in Sliač, Slovakia. Polish Journal of Chemical Technology, 20(2), 1-7. doi: 10.2478/pjct-2018-0016.

[51] Preez, G.D., Daneel, M., Goede, R.D., & Ferris, H. (2022). Nematode-based indices in soil ecology: Application, utility, and future directions. Soil Biology and Biochemistry, 169, retrieved from 108640. doi: 10.1016/j.soilbio.2022.108640.

[52] Rafighi, A., & Tabarsa, T. (2011). Manufacturing high performance wood composite panel from paulownia. Key Engineering Materials, 471–472, 1091-1094. doi: 10.4028/www.scientific.net/KEM.471-472.1091.

[53] Raskin, I., & Ensley, B. (Eds). (1999). Phytoremediation of toxic metals: Using plants to clean up the environment. New York: Wiley.

[54] Rehman, P., Nazir, R., Naqvi, T., & Pervez, A. (2018). Bacterial feeder nematodes: Facilitator or competitor for plant phosphorus in soil. Journal of Soil Science and Plant Nutrition, 18(4). doi: 10.4067/S071895162018005003203.

[55] Renčo, M., Gömöryová, E., & Čerevková, A. (2020). The effect of soil type and ecosystems on the soil nematode and microbial communities. Helminthologia, 57(2), 129-144. doi: 10.2478/helm-2020-0014.

[56] Römkens, P., Bouwman, L., Japenga, J., & Draaisma, C. (2002). Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environmental Pollution, 116(1), 109-121. doi: 10.1016/S0269-7491(01)00150-6 .

[57] Satyendra, K.P., Phillips, G., & Bernard, E. (2022). Increasing levels of physical disturbance affect soil nematode community composition in a previously undisturbed ecosystem. The Journal of Nematology, 54(1). doi: 10.2478/jofnem-2022-0022.

[58] Sawicka, B., Skiba, D., Bienia, B., & Kiełtyka-Dadasiewicz, A. (2019). Jerusalem artichoke (Helianthus tuberosus L.) as energy raw material. In A. Raupelienė (Ed.), Research and innovation for bioeconomy: Proceedings of the 9thinternational scientific conference rural development (pp. 337-342). Kaunas: Vytautas Magnus University. doi: 10.15544/RD.2019.042.

[59] Sharma, V. (1999). Root-knot nematodes of Paulownia and their management. Indian Journal of Forestry, 22(1), 149-154. Retrieved from https://unfao-koha.ptfse.net/cgi-bin/koha/opac-detail.pl?biblionumber=675655&shelfbrowse_itemnumber=281305.

[60] Shavkatovna, K.N. (2023). Taxonomy and ecology of phytonematodes of some plants growing in the greenhouse. International Multidisciplinary Journal for Research & Development, 10(11), 36-38.
Retrieved from https://www.ijmrd.in/index.php/imjrd/article/view/267.

[61] Shokoohi, E. (2024). Interactions of free-living nematodes and associated microorganisms with Plant-parasitic nematodes. In Sustainable management of nematodes in agriculture, 2: Role of microbes-assisted strategies (pp. 127-147). Berlin: Springer. doi: 10.1007/978-3-031-52557-5_5.

[62] Sims, R., Hastings, A., Schlamadinger, B., & Taylor, G. (2006). Energy crops: Current status and future prospects. Global Change Biology, 12(11), 2054-2076. doi: 10.1111/j.1365-2486.2006.01163. x .

[63] Singh, S., Awashti, L., Jangre, A., & Nirmalkar, V. (2020). Transmission of plant viruses through soil-inhabiting nematode vectors. Applied Plant Virology, 291-300. doi: 10.1016/B978-0-12-818654-1.00022-0.

[64] Skwiercz, A.T., Dobosz, R., Flis, L., & Damszel, M. (2019). First report of Meloidogyne hapla on Paulownia tomentosa in Poland. Acta Societatis Botanicorum Poloniae, 88(3), article number 3628. doi: 10.5586/asbp.3628.

[65] Skwiercz, A.T., Zapałowska, A., Litwińczuk, W., & Stefanovska, T. (2022). Plant parasitic nematodes on Paulownia tomentosa in Poland. Journal of Horticultural Research, article number 2020010047. doi: 10.20944/preprints202001.0047.v1.

[66] Sochová, I., Hofman, J., & Holoubek, I. (2006). Using nematodes in soil ecotoxicology. Environment International, 32(3), 374-383. doi: 10.1016/j.envint.2005.08.031.

[67] Stavridou, E., Hastings, A., Webster, R., & Robson, P. (2016). The impact of soil salinity on the yield, composition and physiology of the bioenergy grass Miscanthus×giganteus. GCB – Bioenergy, 9(1), 92-104. https://doi.org/10.1111/gcbb.12351 .

[68] Stefanovska, T., Skwiercz, A., Pidlisnyuk, V., Zhukov, O., & Shapoval, O. (2023). Can nematode communities work as an indicator of soil health in a multiyear Miscanthus х Giganteus plantation growing in lead-contaminated soil? Agronomy, 13(6), 1620. doi: 10.3390/agronomy13061620.

[69] Stefanovska, T.R., Skwiercz A., Zouhar, M., & Pidlisnyuk, V. (2020). Plant feeding nematodes associated with Miscanthus×giganteus and their use as potential indicators of the plantations’ state. International Journal of Environmental Science and Technology, 18(2), 57-72. doi: 10.1007/s13762-020-02865-z.

[70] Szulczewski, W., Zyromski, A., Jakubowski, W., & Biniak-Pierog, M. (2018). A new method for the estimation of biomass yield of giant miscanthus (Miscanthus giganteus) in the course of vegetation. Renewable and Sustainable Energy Reviews, 82(2), 1787-1795. doi: 10.1016/j.rser.2017.07.057.

[71] Taylor, R. (2019). Taylor’s power law: Order and pattern in nature. Cambridge: Academic Press.

[72] Todd, T.C. (2006). Sentinel nematodes of land-use change and restoration in tallgrass prairie. J. Nematol, 38(1), 20-27. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2586438/.

[73] Vodiak Y. T., Tsapko Y., Kucher A., & Krupin V. (2022). Influence of growing Miscanthus x giganteus on ecosystem services of chernozem. Energies, 15(11), article number 4157.

[74] Wajid, M., & Pathak, K (Ed.). (1993). Nematodes as vectors of bacterial and fungal plant pathogens. Berlin: Springer. Retrieved from https://link.springer.com/book/10.1007/978-94-011-1488-2.

[75] Winklerб B., Mangold, A., von Cossel, M., & Clifton-Brown, J. (2020). Implementing miscanthus into farming systems: A review of agronomic practices, capital and labour demand. Renewable and Sustainable Energy Reviews, 132, article number 110053. doi: 10.1016/j.rser.2020.110053.

[76] Yeates, G.W. (2003). Nematodes as soil indicators: Functional and biodiversity aspects. Biology and Fertility of Soils, 37(4), 199-210. doi: 10.1007/s00374-003-0586-5.

[77] Yue, H.N., Wu, Y.F., Shi, Y.Z., & Wu, K.K. (2008). First report of paulownia witches’-broom phytoplasma in China. Plant Disease, 92(7), 1134-1134. doi: 10.1094/PDIS-92-7-1134A.

[78] Zapałowska, A., & Skwiercz, A. (2018). Populations of parasitic nematodes colonizing Jerusalem artichoke (Helianthus tuberosus L.). Acta Societatis Botanicorum Poloniae, 87(2), article number 3578. doi: 10.5586/asbp.3578.

[79] Zegada-Lizarazu, W., & Monti, A. (2011). Energy crops in rotation. A review. Biomass and Bioenergy, 35(1), 12-25. doi: 10.1016/j.biombioe.2010.08.001.

[80] Zhang, X., Zhu, A., Xin, X., Yang, W., Zhang, J., & Ding, S. (2018). Tillage and residue management for long-term wheat-maize cropping in the North China plain: I. Crop yield and integrated soil fertility index. Field Crops Research, 221, 157-165. doi: 10.1016/j.fcr.2018.02.025.

[81] Zhao, C., Shao, Y., Lu, H., & Classen, A. (2024). Drought shifts soil nematode trophic groups and mediates the heterotrophic respiration. Journal of Plant Ecology, 17(2), article number rtae012. doi: 10.1093/jpe/rtae012.

[82] Zhao, J., Li, D., Fu, S., & He, X. (2016). Using the biomasses of soil nematode taxa as weighting factors for assessing soil food web conditions. Ecological Indicators, 60, 310-316. doi: 10.1016/j.ecolind.2015.06.003.

[83] Zhilina, T.M. (2012). Monitoring of the soil nematodes populations status of in natural and anthropogenic transformation coenoses. Scientific Herald of Uzhhorod National University: Biology, 32.