Hostname: page-component-7bb8b95d7b-lvwk9 Total loading time: 0 Render date: 2024-09-21T01:14:48.610Z Has data issue: false hasContentIssue false

The effects of lead (Pb) and pest damage on soil enzyme activities, pakchoi and Spodoptera litura performance

Published online by Cambridge University Press:  19 September 2024

Huiyang Liu
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China
Yimeng Shi
Affiliation:
College of Food and Chemical Engineering, Shaoyang University, Shaoyang, China
Yuxuan Zou
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China
Zaiya Song
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China
Huai Tian
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China
Xianjun Yang
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China
Xiaohong Li*
Affiliation:
College of Agriculture and Forestry Ecology, Shaoyang University, Shaoyang, China College of Food and Chemical Engineering, Shaoyang University, Shaoyang, China
*
Corresponding author: Xiaohong Li; Email: [email protected]

Abstract

Plant–soil interactions have bottom–up and top–down effects within a plant community. Heavy metal pollution can change plant–soil interactions, directly influence bottom–up effects and indirectly affect herbivores within the community. In turn, herbivores can affect plant–soil interactions through top–down effects. However, the combined effects of heavy metals and herbivores on soil enzymes, plants and herbivores have rarely been reported. Therefore, the effects of lead (Pb), Spodoptera litura and their combined effects on soil enzyme activities, pakchoi nutrition, defence compounds and S. litura fitness were examined here. Results showed that Pb, S. litura and their combined effects significantly affected soil enzymes, pakchoi and S. litura. Specifically, exposure to double stress (Pb and S. litura) decreased soil urease, phosphatase and sucrase activities compared with controls. Furthermore, the soluble protein and sugar contents of pakchoi decreased, and the trypsin inhibitor content and antioxidant enzyme activity increased. Finally, the S. litura development period was extended, and survival, emergence rates and body weight decreased after exposure to double stress. The combined stress of Pb and S. litura significantly decreased soil enzyme activities. Heavy metal accumulation in plants may create a superposition or synergistic effect with heavy metal-mediated plant chemical defence, further suppressing herbivore development. Pb, S. litura and their combined effects inhibited soil enzyme activities, improved pakchoi resistance and reduced S. litura development. The results reveal details of soil–plant–herbivore interactions and provide a reference for crop pest control management in the presence of heavy metal pollution.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdu, N, Abdullahi, AA and Abdulkadir, A (2017) Heavy metals and soil microbes. Environmental Chemistry Letters 15, 6584.CrossRefGoogle Scholar
Adetunji, AT, Lewu, FB, Mulidzi, R and Ncube, B (2017) The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: a review. Journal of Soil Science and Plant Nutrition 17, 794807.CrossRefGoogle Scholar
Aponte, H, Meli, P, Butler, B, Paolini, J, Matus, F, Merino, C, Cornejo, P and Kuzyakov, Y (2020) Meta-analysis of heavy metal effects on soil enzyme activities. Science of the Total Environment 737, 139744.CrossRefGoogle ScholarPubMed
Barto, EK and Cipollini, D (2005) Testing the optimal defense theory and the growth-differentiation balance hypothesis in Arabidopsis thaliana. Oecologia 146, 169178.CrossRefGoogle ScholarPubMed
Bhaduri, AM and Fulekar, MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Reviews in Environmental Science and Biotechnology 11, 5569.CrossRefGoogle Scholar
Bhattacharyya, A, Leighton, SM and Babu, CR (2007) Bioinsecticidal activity of Archidendron ellipticum trypsin inhibitor on growth and serine digestive enzymes during larval development of Spodoptera litura. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 145, 669677.Google ScholarPubMed
Boyd, RS (2012) Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Science 195, 8895.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Butler, CD and Trumble, JT (2008) Effects of pollutants on bottom-up and top-down processes in insect-plant interactions. Environmental Pollution 156, 110.CrossRefGoogle ScholarPubMed
Cantarel, AA, Pommier, T, Desclos-Theveniau, M, Diquélou, S, Dumont, M, Grassein, F, Kastl, EM, Grigulis, K, Laîné, P, Lavorel, S, Lemauviel-Lavenant, S, Personeni, E, Schloter, M and Poly, F (2015) Using plant traits to explain plant-microbe relationships involved in nitrogen acquisition. Ecology 96, 788799.CrossRefGoogle ScholarPubMed
Carrillo, J, Ingwell, LL, Li, X and Kaplan, I (2019) Domesticated tomatoes are more vulnerable to negative plant-soil feedbacks than their wild relatives. Journal of Ecology 107, 17531766.CrossRefGoogle Scholar
Chance, B and Maehly, AC (1955) Assay of catalases and peroxidases. Methods in Enzymology 2, 764775.CrossRefGoogle Scholar
Chen, J, Wang, JW and Shu, YH (2020) Review on the effects of heavy metal pollution on herbivorous insects. Journal of Applied Ecology 31, 17731782.Google ScholarPubMed
Cheruiyot, DJ, Boyd, RS and Moar, W (2015) Testing the joint effects hypothesis of elemental defense using Spodoptera exigua. Journal of Chemical Ecology 41, 168177.CrossRefGoogle ScholarPubMed
Classen, AT, DeMarco, J, Hart, SC, Whitham, TG, Cobb, NS and Koch, GW (2006) Impacts of herbivorous insects on decomposer communities during the early stages of primary succession in a semi-arid woodland. Soil Biology and Biochemistry 38, 972982.CrossRefGoogle Scholar
Dicke, M (2015) Herbivore-induced plant volatiles as a rich source of information for arthropod predators: fundamental and applied aspects. Journal of the Indian Institute of Science 95, 3542.Google Scholar
Dowd, PF and Lagrimini, LM (2006) Examination of the biological effects of high anionic peroxidase production in tobacco plants grown under field conditions. I. Insect pest damage. Transgenic Research 15, 197204.CrossRefGoogle ScholarPubMed
Gao, Y, Zhou, P, Mao, L, Zhi, YE and Shi, WJ (2010) Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD. Environmental Earth Sciences 60, 603612.CrossRefGoogle Scholar
Guan, SY (1986) Soil Enzyme and Research Methods. Beijing, Agriculture Press, pp. 260346.Google Scholar
Gupta, AS, Webb, RP, Holaday, AS and Allen, RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiology 103, 10671073.CrossRefGoogle ScholarPubMed
Han, P, Lavoir, AV, Rodriguez-Saona, C and Desneux, N (2022) Bottom-up forces in agroecosystems and their potential impact on arthropod pest management. Annual Review of Entomology 67, 239259.CrossRefGoogle ScholarPubMed
Hoysted, GA, Bell, CA, Lilley, CJ and Urwin, PE (2018) Aphid colonization affects potato root exudate composition and the hatching of a soil-borne pathogen. Frontiers in Plant Science 9, 1278.CrossRefGoogle ScholarPubMed
Hu, LL (2004) Intra- and Interspecific Interactions of Myzus Persicae (Sulzer) and Lipaphis Erysimi (Kaltenbach) on Cabbage (Brassica Oleracea var. Capitata). Shandong: Shandong Agricultural University.Google Scholar
Huang, JH, Liu, MQ, Chen, XY, Chen, J, Chen, FJ, Li, HX and Hu, F (2013) Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth. Plant and Soil 367, 437447.CrossRefGoogle Scholar
Huang, J, Chen, Y, Huang, Y and Yu, J (2021) The effects of heavy metal accumulation on plant and herbivore interaction: a review. Journal of Agriculture 11, 4245.Google Scholar
Huberty, M, Choi, YH, Heinen, R and Bezemer, TM (2020) Above-ground plant metabolomic responses to plant-soil feedbacks and herbivory. Journal of Ecology 108, 17031712.CrossRefGoogle Scholar
Huberty, M, Steinauer, K, Heinen, R, Jongen, R, Hannula, SE, Choi, YH and Bezemer, TM (2022) Temporal changes in plant-soil feedback effects on microbial networks, leaf metabolomics, and plant-insect interactions. Journal of Ecology 110, 13281343.CrossRefGoogle Scholar
Jiang, D, Wang, YY, Dong, XW and Yan, SC (2018) Inducible defense responses in Populus alba berolinensis to Pb stress. South African Journal of Botany 119, 295300.CrossRefGoogle Scholar
Jiang, D, Wang, GR and Yan, SC (2020) The improved resistance against gypsy moth in Larix olgensis seedlings exposed to Cd stress association with elemental and chemical defenses. Pest Management Science 76, 17131721.CrossRefGoogle ScholarPubMed
Jiang, D, Tan, M, Guo, Q and Yan, S (2021) Transfer of heavy metal along the food chain: a mini-review on insect susceptibility to entomopathogenic microorganisms under heavy metal stress. Pest Management Science 77, 11151120.CrossRefGoogle ScholarPubMed
Jin, K, Sleutel, S, Buchan, D, De Neve, S, Cai, DX, Gabriels, D and Jin, JY (2009) Changes of soil enzyme activities under different tillage practices in the Chinese Loess Plateau. Soil and Tillage Research 104, 115120.CrossRefGoogle Scholar
Karban, R (2011) The ecology and evolution of induced resistance against herbivores. Functional Ecology 25, 339347.CrossRefGoogle Scholar
Karban, R and Baldwin, IT (1997) Induced Responses to Herbivory. Chicago, University of Chicago Press, pp. 3338.CrossRefGoogle Scholar
Kooyers, NJ, Blackman, BK and Holeski, LM (2017) Optimal defense theory explains deviations from latitudinal herbivory defense hypothesis. Ecology 98, 10361048.CrossRefGoogle ScholarPubMed
Kos, M, Tuijl, MA, de Roo, J, Mulder, PP and Bezemer, TM (2015) Plant-soil feedback effects on plant quality and performance of an aboveground herbivore interact with fertilization. Oikos 124, 658667.CrossRefGoogle Scholar
Lei, GJ, Sun, L, Sun, Y, Zhu, XF, Li, GX and Zheng, SJ (2020) Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. Journal of Integrative Plant Biology 62, 218227.CrossRefGoogle ScholarPubMed
Li, XH (2016) Effects of Interaction Between Constitutive and Induced Resistance in Soybean Plants on Fitness Traits and Behavior of Spodoptera litura and its Parasitoid. Najing: Najing Agricultural University.Google Scholar
Li, J, Fang, L, Lv, Z and Zhang, Z (2008) Relationships between the cotton aphid (Aphis gossypii) and the content of soluble sugars. Plant Protection 2, 2630.Google Scholar
Li, K, Chen, J, Jin, P, Li, J, Wang, J and Shu, Y (2018) Effects of Cd accumulation on cutworm (Spodoptera litura) larvae via Cd-treated Chinese flowering cabbage (Brassica campestris) and artificial diets. Chemosphere 200, 151163.CrossRefGoogle ScholarPubMed
Li, XH, Yang, XJ, Huang, ZY and Wu, SL (2021) Effects of herbivore-feeding induced tobacco defenses on developmental performances and oviposition preference of Spodoptera litura. Acta Tabacaria Sinica 27, 101107.Google Scholar
Liang, SX, Ding, L, Shen, S, Liu, W, Li, J and Xi, X (2018) Assessment of the remediation effect of nano-hydroxyapatite in exogenous Pb-contaminated soil using toxicity characteristic leaching procedure and soil enzyme activities. Bulletin of Environmental Contamination and Toxicology 101, 250256.CrossRefGoogle ScholarPubMed
Lin, H, Wang, Z, Liu, C and Dong, Y (2022a) Technologies for removing heavy metal from contaminated soils on farmland: a review. Chemosphere 305, 135457.CrossRefGoogle ScholarPubMed
Lin, T, Zhu, G, He, W, Xie, J, Li, S, Han, S, Li, S, Yang, C, Liu, Y and Zhu, T (2022b) Soil cadmium stress reduced host plant odor selection and oviposition preference of leaf herbivores through the changes in leaf volatile emissions. Science of the Total Environment 814, 152728.CrossRefGoogle ScholarPubMed
Long, Y, Liu, JP and Li, XH (2022) Effects of Spodoptera litura feeding on soybean agronomic characters and soil enzyme activities. Plant Protection 48, 122128.Google Scholar
Lou, YG and Baldwin, IT (2003) Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proceedings of the National Academy of Sciences 100(Suppl_2), 1458114586.CrossRefGoogle ScholarPubMed
Maksymiec, W, Wianowska, D, Dawidowicz, AL, Radkiewicz, S, Mardarowicz, M and Krupa, Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. Journal of Plant Physiology 162, 13381346.CrossRefGoogle ScholarPubMed
Mao, F, Nan, G, Cao, M, Gao, Y, Guo, L, Meng, X and Yang, G (2018) The metal distribution and the change of physiological and biochemical process in soybean and mung bean plants under heavy metal stress. International Journal of Phytoremediation 20, 11131120.CrossRefGoogle ScholarPubMed
Martijn Bezemer, T, van der Putten, WH, Martens, H, van de Voorde, TF, Mulder, PP and Kostenko, O (2013) Above–and below–ground herbivory effects on below–ground plant–fungus interactions and plant–soil feedback responses. Journal of Ecology 101, 325333.CrossRefGoogle Scholar
Nurzhan, A, Tian, H, Nuralykyzy, B and He, W (2022) Soil enzyme activities and enzyme activity indices in long-term arsenic-contaminated soils. Eurasian Soil Science 55, 14251435.CrossRefGoogle Scholar
Orwin, KH, Buckland, SM, Johnson, D, Turner, BL, Smart, S, Oakley, S and Bardgett, RD (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. Journal of Ecology 98, 10741083.CrossRefGoogle Scholar
Paudel, S, Lin, PA, Foolad, MR, Ali, JG, Rajotte, EG and Felton, GW (2019) Induced plant defenses against herbivory in cultivated and wild tomato. Journal of Chemical Ecology 45, 693707.CrossRefGoogle ScholarPubMed
Pineda, A, Zheng, SJ, van Loon, JJ, Pieterse, CM and Dicke, M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in Plant Science 15, 507514.CrossRefGoogle ScholarPubMed
R Development Core Team (2022) R Language. R Foundation Statistical Computing. Available at https://www.R-project.org/Google Scholar
Sahu, S, Dutta, A, Ray, DK, Pradhan, J and Dandapat, J (2018) Host plant-derived allelochemicals and metal components are associated with oxidative predominance and antioxidant plasticity in the larval tissues of silkworm, Antheraea mylitta: further evidence of joint effects hypothesis. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 223, 3949.CrossRefGoogle ScholarPubMed
Sang, W, Xu, J, Bashir, MH and Ali, S (2018) Developmental responses of Cryptolaemus montrouzieri to heavy metals transferred across multi-trophic food chain. Chemosphere 205, 690697.CrossRefGoogle ScholarPubMed
Sidhu, GPS, Bali, AS, Bhardwaj, R, Singh, HP, Batish, DR and Kohli, RK (2018) Bioaccumulation and physiological responses to lead (Pb) in Chenopodium murale L. Ecotoxicology and Environmental Safety 151, 8390.CrossRefGoogle ScholarPubMed
Song, GC, Lee, S, Hong, J, Choi, HK, Hong, GH, Bae, DW, Mysore, KS, Park, YS and Ryu, CM (2015) Aboveground insect infestation attenuates belowground Agrobacterium-mediated genetic transformation. New Phytologist 207, 148158.CrossRefGoogle ScholarPubMed
Sznajder, B and Harvey, JA (2003) Second and third trophic level effects of differences in plant species reflect dietary specialization of herbivores and their endoparasitoids. Entomologia Experimentalis et Applicata 109, 7382.CrossRefGoogle Scholar
Tan, XP, He, JH, Guo, ZM, Wang, ZQ, Nie, YX, Ye, Q, He, WX and Shen, WJ (2023) Research progresses on soil enzymes as indicators of soil health and their responses to heavy metal pollution. Acta Pedologica Sinica 60, 5052.Google Scholar
Tang, B, Xu, H, Song, F, Ge, H and Yue, S (2022) Effects of heavy metals on microorganisms and enzymes in soils of lead-zinc tailing ponds. Environmental Research 207, 112174.CrossRefGoogle ScholarPubMed
Tibbett, M, Green, I, Rate, A, De Oliveira, VH and Whitaker, J (2021) The transfer of trace metals in the soil-plant-arthropod system. Science of the Total Environment 779, 146260.CrossRefGoogle ScholarPubMed
Wang, M, Ruan, W, Kostenko, O, Carvalho, S, Hannula, SE, Mulder, PP, Bu, F, van der Putten, WH and Bezemer, TM (2019) Removal of soil biota alters soil feedback effects on plant growth and defense chemistry. New Phytologist 221, 14781491.CrossRefGoogle ScholarPubMed
Watanabe, T and Kitagawa, H (2000) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). Journal of Economic Entomology 93, 11921198.CrossRefGoogle ScholarPubMed
Winiarska-Mieczan, A, Jachimowicz, K, Kwiecień, M, Krusiński, R, Kislova, S, Sowińska, L, Zasadna, Z and Yanovych, D (2023) The content of Cd and Pb in herbs and single-component spices used in Polish cuisine. Biological Trace Element Research 201, 35673581.CrossRefGoogle ScholarPubMed
Winter, TR, Borkowski, L, Zeier, J and Rostás, M (2012) Heavy metal stress can prime for herbivore-induced plant volatile emission. Plant, Cell and Environment 35, 12871298.CrossRefGoogle ScholarPubMed
Yactayo-Chang, JP, Tang, HV, Mendoza, J, Christensen, SA and Block, AK (2020) Plant defense chemicals against insect pests. Agronomy 10, 1156.CrossRefGoogle Scholar
Yin, F, Feng, X, Zhang, DY, Li, ZY, Lin, QS, Hu, ZD and Chen, HY (2012) Contents changes of protein and sugar in host plants after damaged by the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Journal of Environmental Entomology 34, 168173.Google Scholar
Zavala, JA, Patankar, AG, Gase, K and Baldwin, IT (2004) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proceedings of the National Academy of Sciences of the USA 101, 16071612.CrossRefGoogle ScholarPubMed
Zhang, SW, Zong, YJ, Fang, CY, Huang, SH, Li, J, Xu, JH, Wang, YF and Liu, CH (2020) Optimization of anthrone colorimetric method for rapid determination of soluble sugar in barley. Food Research and Development 41, 196200.Google Scholar
Zhang, Q, Zhou, M and Wang, J (2022) Increasing the activities of protective enzymes is an important strategy to improve resistance in cucumber to powdery mildew disease and melon aphid under different infection/infestation patterns. Frontiers in Plant Science 13, 950538.CrossRefGoogle ScholarPubMed
Zhao, A, Li, Y, Leng, C, Wang, P and Li, Y (2019) Inhibitory effect of protease inhibitors on larval midgut protease activities and the performance of Plutella xylostella (Lepidoptera: Plutellidae). Frontiers in Physiology 9, 1963.CrossRefGoogle ScholarPubMed