Paxillus involutus can control Alternaria alternata of Populus davidiana ×  P. bolleana by increasing the transport of heavy metals

Abstract

The ectomycorrhizal fungus Paxillus involutus was inoculated onto tissue-cultures of the hybrid poplar, Populus davidiana ×  P. bolleana, to evaluate the elemental defense effect to heavy metals copper and cadmium at different concentrations by simulating Alternaria alternata fungus infection. The enrichment capacity of Populus davidiana ×  P. bolleana for Cu and Cd was closely associated with the degree of heavy metal stress. There was a significant positive interaction of applying Cu and Cd and the inoculation with P. involutus on A. alternata leaf blight disease index. The incidence rate and disease index of leaf blight underwent a significant reduction compared with the controls. Similarly, the ratio of the area of disease spot to leaf area, incidence rate, and disease index for Populus davidiana ×  P. bolleana leaves inoculated with Paxillus involutus (Batsch) Fr. were significantly lower than those of their non-mycorrhizal counterparts. With increasing the degree of Cu and Cd stress, a gradual increase in the average value of the membership function for the incidence rate and disease index was observed, indicating the weakened pathogen’s ability to cause infection and the improved resistance of Populus davidiana ×  P. bolleana to leaf blight disease under Cu and Cd stress. Moreover, superoxide dismutase enzyme activity in Populus davidiana ×  P. bolleana increased significantly, reaching levels of 411.0 U/g FW and 421.6 U/g FW under Cu and Cd treatments, respectively. These changes in metabolic products and antioxidant enzyme activities suggest that P. involutus may enhance the resistance of Populus davidiana ×  P. bolleana to the fungus, Alternaria alternata Fr. Keissel under heavy metal stress by modulating these physiological indicators.

Keywords

Populus davidiana ×  P. bolleana / Paxillus involutus / Alternaria alternate / Heavy metals / Elemental defense

References

[1] Aghajani H, Hojjati SM, Ali Tajick-Ghanbari M, Puormajidian MR, Borhani A. Molecular identification of ectomycorrhizal fungal communities associated with oriental beech trees (Fagus orientalis lipsky) in Hyrcanian forest of Iran. Iran J Sci Technol Trans A Sci, 2019, 43(1): 25-32

[2] Bashian-Victoroff C, Yanai RD, Horton TR, Lamit LJ. Nitrogen and phosphorus additions affect fruiting of ectomycorrhizal fungi in a temperate hardwood forest. Fungal Ecol, 2025, 73: 101388

[3] Benzarti S, Mohri S, Ono Y. Plant response to heavy metal toxicity: comparative study between the hyperaccumulator Thlaspi caerulescens (ecotype Ganges) and nonaccumulator plants: lettuce, radish, and alfalfa. Environ Toxicol, 2008, 23(5): 607-616

[4] Blaudez D, Botton B, Chalot M. Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology, 2000, 146(Pt 51109-1117

[5] Borowska J, Pyza E. Effects of heavy metals on insect immunocompetent cells. J Insect Physiol, 2011, 57(6): 760-770

[6] Chai LW, Huang MK, Cao XF, Liu MJ, Huang Y. Potential metal-binding ability of proteins in the extracellular slime of Laccaria bicolor exposed to excessive Cu and Cd. Environ Sci Pollut Res Int, 2019, 26(20): 20418-20427

[7] Chen LH, Han Y, Jiang H, Korpelainen H, Li CY. Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot, 2011, 62(14): 5037-5050

[8] Cheruiyot DJ, Boyd RS, Moar WJ. Exploring lower limits of plant elemental defense by cobalt, copper, nickel, and zinc. J Chem Ecol, 2013, 39(5): 666-674

[9] Coleman CM, Boyd RS, Eubanks MD. Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. J Chem Ecol, 2005, 31(8): 1669-1681

[10] Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z. Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza, 2002, 12(4): 185-190

[11] Gadd GM. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res, 2007, 111(Pt 1): 3-49

[12] Giansoldati V, Tassi E, Morelli E, Gabellieri E, Pedron F, Barbafieri M. Nitrogen fertilizer improves boron phytoextraction by Brassica juncea grown in contaminated sediments and alleviates plant stress. Chemosphere, 2012, 87(10): 1119-1125

[13] Guo Y, Martin K, Hrynkiewicz K, Rasche F. Arbuscular mycorrhizal fungi-based bioremediation of mercury: insights from zinc and cadmium transporter studies. Int J Environ Sci Technol, 2024, 21(3): 3475-3488

[14] Guo YK, Mao K, Cao HR, Ali W, Lei D, Teng DY, Chang CY, Yang XF, Yang Q, Niazi NK, Feng XB, Zhang H. Exogenous selenium (cadmium) inhibits the absorption and transportation of cadmium (selenium) in rice. Environ Pollut, 2021, 268(Pt A): 115829

[15] He JL, Ma CF, Ma YL, Li H, Kang JQ, Liu TX, Polle A, Peng CH, Luo ZB. Cadmium tolerance in six poplar species. Environ Sci Pollut Res Int, 2013, 20(1163-174

[16] He WQ, Liu HY, Qi Y, Liu F, Zhu XR. Patterns in nonstructural carbohydrate contents at the tree organ level in response to drought duration. Glob Change Biol, 2020, 26(6): 3627-3638

[17] Huang Q, Wang XG, Yao XG, Gong CW, Shen LT. Effects of bistrifluron resistance on the biological traits of Spodopteralitura (Fab.) (Noctuidae: Lepidoptera). Ecotoxicology, 2019, 28(3): 323-332

[18] Jiang D (2019) Study of the insect resistance of Populus alba × P. berolinensis and the detoxification mechanism of the defoliator, Lymantria dispar under heavy metal stress. Doctoral Thesis, Northeast Forestry University. (In Chinese)

[19] Khan A, Khan S, Khan MA, Qamar Z, Waqas M. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res Int, 2015, 22(18): 13772-13799

[20] Lin T, Wan X, Zhang F. The short-term responses of glutathione and phytochelation synthetic pathways genes to additional nitrogen under cadmium stress in poplar leaves. Russ J Plant Physiol, 2016, 63(6): 754-762

[21] Lin TT, Chen JP, Zhou SS, Yu WH, Chen G, Chen LH, Wang XG, Shi HZ, Han S, Zhang F. Testing the elemental defense hypothesis with a woody plant species: cadmium accumulation protects Populus yunnanensis from leaf herbivory and pathogen infection. Chemosphere, 2020, 247: 125851

[22] Luo ZB, He JL, Polle A, Rennenberg H. Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv, 2016, 34(6): 1131-1148

[23] Ma YL (2013) The ectomycorrhizal fungi Paxillus involutus increased the absorption and tolerance of heavy metal Cd in Populus × canescens. Master Thesis, Northwest A & F University. (In Chinese)

[24] Meng FJ, Zhang TZ, Yin DC. The effects of soil drought stress on growth characteristics, root system, and tissue anatomy of Pinussylvestris var. mongolica. PeerJ, 2023, 11: e14578

[25] Mucha J, Dahm H, Strzelczyk E, Werner A. Synthesis of enzymes connected with mycoparasitism by ectomycorrhizal fungi. Arch Microbiol, 2006, 185(169-77

[26] Oddsdottir ES, Eilenberg J, Sen R, Halldorsson G. The effects of insect pathogenic soil fungi and ectomycorrhizal inoculation of birch seedlings on the survival of Otiorhynchus larvae. Agric for Entomol, 2010, 12(3319-324

[27] Qi JY, Yin DC. Effects of Suillus luteus on the growth, photosynthesis, stomata, and root system of Pinus tabulaeformis under drought stress. J Plant Growth Regul, 2023, 42(6): 3486-3497

[28] Qu LY, Guo MJ, Makoto K, Watanabe Y, Wu G, Koike T. Effects of different charcoal treatments on the growth of Japanese larch seedlings inoculated with ectomycorrhizal fungi. J For Res, 2024, 36(1): 6

[29] Regvar M, Likar M, Piltaver A, Kugonič N, Smith JE. Fungal community structure under goat willows (Salixcaprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil, 2010, 330(1345-356

[30] Smith SE, Read DJ. Mycorrhizal symbiosis, 20083London, UK, Academic Press

[31] Wang HH, Zhang KL, Tappero R, Victor TW, Bhatnagar JM, Vilgalys R, Liao HL. Inorganic nitrogen and organic matter jointly regulate ectomycorrhizal fungi-mediated iron acquisition. New Phytol, 2025, 245(6): 2715-2725

[32] Wang M, Gu ZC, Wang RR, Guo JJ, Ling N, Firbank LG, Guo SW. Plant primary metabolism regulated by nitrogen contributes to plant-pathogen interactions. Plant Cell Physiol, 2019, 60(2): 329-342

[33] Wang YJ (2023) Research on the mining and regulation mechanism of disease-resistant genes in postharvest blueberry fruit in response to Alternaria tenuissima. Master Thesis, Shenyang Agricultural University. (in Chinese)

[34] Xue Y, Liu X, Xiang C (2014) Forest Pathology Research Methods. Northeast Forestry University Press. (in Chinese)

[35] Yan XL, Zhou LY, Chen YM, Liu RQ, Guo LQ, Li N, Kang A, Zhai KY, Zhou GY, Zhou XH. Ectomycorrhizal fungi explain more variation in rhizosphere nutrient availability than root traits in temperate forests. Appl Soil Ecol, 2025, 207: 105923

[36] Yin DC, Qi JY, Deng JF, Du H, Deng X. Effects of Ectomycorrhizal cooperating with exogenous calcium on Pinussylvestris var. mongolica growth. China Environ Sci, 2017, 37(6): 2295-2304(in Chinese)

[37] Yin DC, Song RQ, Qi JY, Deng X. Ectomycorrhizal fungus enhances drought tolerance of Pinussylvestris var. mongolica seedlings and improves soil condition. J Forestry Res, 2018, 29(61775-1788

[38] Zhang TZ, Meng FJ, Yin DC. Promotion of biomass, photosynthesis, and root growth of seedling biomass, photosynthesis, and root growth of Populusdavidiana × P.bolleana by two species of ectomycorrhizal fungi. J For Res, 2024, 35(1): 101

[39] Zhang TZ, Meng FJ, Yin DC. Effects of ectomycorrhizal fungi on the activation and uptake of phosphorus in the mycorrhizal and hypodermal layers of Populusdavidiana × P.bolleana. J Plant Growth Regul, 2025, 44(52504-2513

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