Alleviation of lead toxicity and phytostimulation in perennial ryegrass by the Pb-resistant fungus Trichoderma asperellum SD-5
Xin Sun A B , Mingjie Sun A , Ying Chao C , Hui Wang A , Hong Pan A , Quangang Yang A , Xiumin Cui A , Yanhong Lou
A D and Yuping Zhuge A D
+ Author Affiliations
- Author Affiliations
A National Engineering Laboratory for Efficient Utilisation of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Daizong Road, Tai’an, Shandong, 271018, PR China.
B School of Geography, Nanjing Normal University, Wenyuan Road, Nanjing, Jiangsu, 210023, PR China.
C Tai’an Hi-Tech Industrial Development Zone, Nantianmen Street, Tai’an City, Shandong, 271000, PR China.
D Corresponding authors. Email: yanhonglou1985@163.com; zhugeyp@sdau.edu.cn
Functional Plant Biology - https://doi.org/10.1071/FP20237
Submitted: 8 August 2020 Accepted: 13 November 2020 Published online: 1 December 2020
Abstract
Lead (Pb), a highly toxic metal ion, is detrimental to plants and humans. Existing botanical techniques for Pb-contaminated soil remediation are limited in their efficiency. Here, we investigated the use of the fungus Trichoderma asperellum Samuels, Lieckf & Nirenberg SD-5, which we identified previously as being Pb-resistant, for phytoremediation and for its effects on plant growth, Pb adsorption, and physiological responses in perennial ryegrass (Lolium perenne L. ‘Lark’). We set up four soil treatments: CK (uncontaminated by Pb), T1 (1000 mg kg–1 Pb), T2 (1:9 ratio of sawdust to T1), and T3 (T2 inoculated with T. asperellum SD-5). A pot experiment revealed that the addition of the Pb-resistant microorganism promoted growth and increased biomass in ryegrass under Pb stress, in addition to significantly enhancing photosynthesis by increasing the leaf chlorophyll content and improving the total protein content and expression of the pAPX, POD, SOD, and GPX genes, evidence of an improved antioxidant system and the alleviation of Pb stress. We demonstrated that Pb-resistant microorganisms can enhance Pb extraction from the soil, thus improving remediation. Mitigation mechanisms operating at the physiological and gene expression levels were also determined, providing a scientific basis for the role of combined plant–microorganism methods in remediating Pb-contaminated soil.
Keywords: antioxidant enzymes, contaminated soil, crop Pb uptake, gene expression, heavy metal, hyperaccumulator, phytoremediation, phytostimulation, ryegrass.
References
Arena C, Figlioli F, Sorrentino MC, Izzo LG, Capozzi F, Giordano S, Spagnuolo V (2017) Ultrastructural, protein and photosynthetic alterations induced by Pb and Cd in Cynara cardunculus L., and its potential for phytoremediation. Ecotoxicology and Environmental Safety 145, 83–89.| Ultrastructural, protein and photosynthetic alterations induced by Pb and Cd in Cynara cardunculus L., and its potential for phytoremediation.Crossref | GoogleScholarGoogle Scholar | 28708985PubMed |
Arumugam R, Rajasekaran S, Nagarajan SM (2010) Response of arbuscular mycorrhizal fungi and Rhizobium inoculation on growth and chlorophyll content of Vigna unguiculata (L) Walp var. Pusa 151. Journal of Applied Science & Environmental Management 14, 113–115.
Bai XY, Dong YJ, Wang QH, Xu LL, Kong J, Liu S (2015) Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biologia Plantarum 59, 163–170.
| Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Ban YH, Xu ZY, Yang YR, Zhang HH, Chen H, Tang M (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27, 283–292.
| Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |
Chen X, Zhao Y, Zhang C, Zhang D, Yao C, Meng Q, Zhao R, Wei Z (2020) Speciation, toxicity mechanism and remediation ways of heavy metals during composting: a novel theoretical microbial remediation method is proposed. Journal of Environmental Management 272, 111109
| Speciation, toxicity mechanism and remediation ways of heavy metals during composting: a novel theoretical microbial remediation method is proposed.Crossref | GoogleScholarGoogle Scholar | 32854897PubMed |
Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiology Ecology 92, fiw036
| Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants.Crossref | GoogleScholarGoogle Scholar | 26906097PubMed |
Cozzolino V, De Martino A, Nebbioso A, Di Meo V, Salluzzo A, Piccolo A (2016) Plant tolerance to mercury in a contaminated soil is enhanced by the combined effects of humic matter addition and inoculation with arbuscular mycorrhizal fungi. Environmental Science and Pollution Research International 23, 11312–11322.
| Plant tolerance to mercury in a contaminated soil is enhanced by the combined effects of humic matter addition and inoculation with arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 26931658PubMed |
Debnath B, Islam W, Li M, Sun YT, Lu XC, Mitra S, Hussain M, Liu S, Qiu DL (2019) Melatonin mediates enhancement of stress tolerance in plants. International Journal of Molecular Sciences 20, 1040
| Melatonin mediates enhancement of stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Gan L, Han LB, Yin SX, Jiang YW (2020) Chlorophyll metabolism and gene expression in response to submergence stress and subsequent recovery in perennial ryegrass accessions differing in growth habits. Journal of Plant Physiology 251, 153195
| Chlorophyll metabolism and gene expression in response to submergence stress and subsequent recovery in perennial ryegrass accessions differing in growth habits.Crossref | GoogleScholarGoogle Scholar | 32485524PubMed |
Han F, Sun MJ, He W, Cui XM, Pan H, Wang H, Song FP, Lou YH, Zhuge YP (2019) Ameliorating effects of exogenous Ca2+ on foxtail millet seedlings under salt stress. Functional Plant Biology 46, 407–416.
| Ameliorating effects of exogenous Ca2+ on foxtail millet seedlings under salt stress.Crossref | GoogleScholarGoogle Scholar | 30940338PubMed |
Kaur Kohli S, Handa N, Bali S, Arora S, Sharma A, Kaur R, Bhardwaj R (2018) Modulation of antioxidative defense expression and osmolyte content by co-application of 24-epibrassinolide and salicylic acid in Pb exposed Indian mustard plants. Ecotoxicology and Environmental Safety 147, 382–393.
| Modulation of antioxidative defense expression and osmolyte content by co-application of 24-epibrassinolide and salicylic acid in Pb exposed Indian mustard plants.Crossref | GoogleScholarGoogle Scholar | 28881317PubMed |
Khan M, Daud MK, Basharat A, Khan MJ, Azizullah A, Muhammad N, Muhammad N, Ur Rehman Z, Zhu SJ (2016) Alleviation of lead-induced physiological, metabolic, and ultramorphological changes in leaves of upland cotton through glutathione. Environmental Science and Pollution Research International 23, 8431–8440.
| Alleviation of lead-induced physiological, metabolic, and ultramorphological changes in leaves of upland cotton through glutathione.Crossref | GoogleScholarGoogle Scholar | 26782322PubMed |
Kolbas A, Kidd P, Guinberteau J, Jaunatre R, Herzig R, Mench M (2015) Endophytic bacteria take the challenge to improve Cu phytoextraction by sunflower. Environmental Science and Pollution Research International 22, 5370–5382.
| Endophytic bacteria take the challenge to improve Cu phytoextraction by sunflower.Crossref | GoogleScholarGoogle Scholar | 25561255PubMed |
Lei K, Giubilato E, Critto A, Pan H, Lin C (2016) Contamination and human health risk of lead in soils around lead/zinc smelting areas in China. Environmental Science and Pollution Research International 23, 13128–13136.
| Contamination and human health risk of lead in soils around lead/zinc smelting areas in China.Crossref | GoogleScholarGoogle Scholar | 27000119PubMed |
Li X, Zhang X, Cui Z (2017) Combined bioremediation for lead in mine tailings by Solanum nigrum L. and indigenous fungi. Chemistry and Ecology 33, 932–948.
| Combined bioremediation for lead in mine tailings by Solanum nigrum L. and indigenous fungi.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Lou Y, Zhao P, Wang D, Amombo E, Sun X, Wang H, Zhuge Y (2017) Germination, physiological responses and gene expression of tall fescue (Festuca arundinacea Schreb.) growing under Pb and Cd. PLoS One 12, e0169495
| Germination, physiological responses and gene expression of tall fescue (Festuca arundinacea Schreb.) growing under Pb and Cd.Crossref | GoogleScholarGoogle Scholar | 28837625PubMed |
Lou Y, Guan R, Sun M, Han F, He W, Wang H, Song F, Cui X, Zhuge Y (2018) Spermidine application alleviates salinity damage to antioxidant enzyme activity and gene expression in alfalfa. Ecotoxicology (London, England) 27, 1323–1330.
| Spermidine application alleviates salinity damage to antioxidant enzyme activity and gene expression in alfalfa.Crossref | GoogleScholarGoogle Scholar |
Norini MP, Thouin H, Miard F, Battaglia-Brunet F, Gautret P, Guégan R, Forestier LL, Morabito D, Bourgerie S, Motelica-Heino M (2019) Mobility of Pb, Zn, Ba, As and Cd toward soil pore water and plants (willow and ryegrass) from a mine soil amended with biochar. Journal of Environmental Management 232, 117–130.
| Mobility of Pb, Zn, Ba, As and Cd toward soil pore water and plants (willow and ryegrass) from a mine soil amended with biochar.Crossref | GoogleScholarGoogle Scholar | 30471545PubMed |
Park JH, Bolan N, Megharaj M, Naidu R (2011) Comparative value of phosphate sources on the immobilization of lead, and leaching of lead and phosphorus in lead contaminated soils. Science of the Total Environment 409, 853–860.
| Comparative value of phosphate sources on the immobilization of lead, and leaching of lead and phosphorus in lead contaminated soils.Crossref | GoogleScholarGoogle Scholar |
Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171, 710–721.
| Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives.Crossref | GoogleScholarGoogle Scholar | 28061428PubMed |
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Le Journal de Botanique 2012, 1–26.
| Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions.Crossref | GoogleScholarGoogle Scholar |
Shen J, Song L, Müller K, Hu Y, Song Y, Yu W, Wang H, Wu J (2016) Magnesium alleviates adverse effects of lead on growth, photosynthesis, and ultrastructural alterations of Torreya grandis seedlings. Frontiers in Plant Science 7, 1819
| Magnesium alleviates adverse effects of lead on growth, photosynthesis, and ultrastructural alterations of Torreya grandis seedlings.Crossref | GoogleScholarGoogle Scholar | 27965704PubMed |
Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environmental Pollution 156, 1164–1170.
| Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape.Crossref | GoogleScholarGoogle Scholar | 18490091PubMed |
Shukla S, Naik G, Mishra SK (2015) Potential antimicrobial activity of bacterial endophytes isolated from Flacourtia jangomas (Lour.) Raeusch, a less explored medicinal plant. Journal of Microbiology, Biotechnology and Food Sciences 4, 473–477.
| Potential antimicrobial activity of bacterial endophytes isolated from Flacourtia jangomas (Lour.) Raeusch, a less explored medicinal plant.Crossref | GoogleScholarGoogle Scholar |
Sun X, Han F, Wang H, Song FP, Cui XM, Lou YH, Zhuge YP (2018) Characterization of three Pb-resistant fungi and their potential Pb2+ ions adsorption capacities. Water Science and Technology 78, 2616–2625.
| Characterization of three Pb-resistant fungi and their potential Pb2+ ions adsorption capacities.Crossref | GoogleScholarGoogle Scholar | 30767926PubMed |
Visavadiya NP, Patel SP, VanRooyen JY, Sullivan PG, Rabchevsky AG (2016) Cellular and subcellular oxidative stress parameters following severe spinal cord injury. Redox Biology 8, 59–67.
| Cellular and subcellular oxidative stress parameters following severe spinal cord injury.Crossref | GoogleScholarGoogle Scholar | 26760911PubMed |
Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17. Journal of Applied Microbiology 111, 1065–1074.
| Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17.Crossref | GoogleScholarGoogle Scholar | 21895895PubMed |
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan Z (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regulation 69, 11–20.
| Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Wei S, Li Y, Zhou Q, Srivastava M, Chiu S, Zhan J, Wu Z, Sun T (2010) Effect of fertilizer amendments on phytoremediation of Cd-contaminated soil by a newly discovered hyperaccumulator Solanum nigrum L. Journal of Hazardous Materials 176, 269–273.
| Effect of fertilizer amendments on phytoremediation of Cd-contaminated soil by a newly discovered hyperaccumulator Solanum nigrum L.Crossref | GoogleScholarGoogle Scholar | 19951826PubMed |
Wu H, Liu Y, Zhang X, Zhang J, Ma E (2019) Antioxidant defenses at enzymatic and transcriptional levels in response to acute lead administration in Oxya chinensis. Ecotoxicology and Environmental Safety 168, 27–34.
| Antioxidant defenses at enzymatic and transcriptional levels in response to acute lead administration in Oxya chinensis.Crossref | GoogleScholarGoogle Scholar | 30384164PubMed |
Xie Y, Fan JB, Zhu WX, Amombo E, Lou YH, Chen L, Fu JM (2016) Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Frontiers in Plant Science 7, 755
| Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation.Crossref | GoogleScholarGoogle Scholar | 27303431PubMed |
Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10, e0145726
| The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L.Crossref | GoogleScholarGoogle Scholar | 26717317PubMed |
