Abstract
Endophytes play essential roles in plant growth under metal(loid)s stress. An endophytic fungus strain MR1 was isolated from the roots of Miscanthus floridulus collected from a lead–zinc mining area (Huayuan, China), which could produce indole-3-acetic acid and have Cadmium (Cd) tolerance. Further 18S rRNA sequencing analysis showed that it was highly similar (99.83%) to Talaromyces pinophilus. In pot experiments, we explored the effects of strain MR1 on the growth and Cd uptake of a wide-type Arabidopsis thaliana under low (LC) and high (HC) Cd concentrations. The results showed that MR1 effectively increased the dry weight of aboveground and underground tissues by 25.95–107.21% in both LC and HC groups. Due to MR1 inoculation, the Cd content in the underground tissues was significantly (p < 0.05) decreased by 39.28% under low Cd concentration, while it was significantly (p < 0.05) increased by 28.28% under high Cd concentration. Besides, MR1 inoculations significantly (p < 0.05) increased the total content of removed Cd (17.080 μg) and BCF (0.064) by 129.77% and 153.95% under high Cd concentration. Therefore, we speculated that MR1 might be selected as the effective microbial agent to increase crop yield and control Cd content in the crop in light Cd-contaminated soil. Besides, MR1 could potentially enhance the phytoremediation efficiency of extremely Cd-contaminated soil.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00284-023-03453-3/MediaObjects/284_2023_3453_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00284-023-03453-3/MediaObjects/284_2023_3453_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00284-023-03453-3/MediaObjects/284_2023_3453_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00284-023-03453-3/MediaObjects/284_2023_3453_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00284-023-03453-3/MediaObjects/284_2023_3453_Fig5_HTML.png)
Similar content being viewed by others
Data Availability
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Brabcová V, Štursová M, Baldrian P (2018) Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. Soil Biol Biochem 118:187–198
Xu C, He S, Liu Y, Zhang W, Lu D (2017) Bioadsorption and biostabilization of cadmium by Enterobacter cloacae TU. Chemosphere 173:622–629
He S, Wu Q, He Z (2014) Synergetic effects of DA-6/GA 3 with EDTA on plant growth, extraction and detoxification of Cd by Lolium perenne. Chemosphere (Oxford) 117:132–138
Dai H, Wei S, Twardowska I, Han R, Xu L (2017) Hyperaccumulating potential of Bidens pilosa L. for Cd and elucidation of its translocation behavior based on cell membrane permeability. Environ Sci Pollut R 24:23161–23167
Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot 83:33–46
Selvam A, Wong JW (2009) Cadmium uptake potential of Brassica napus cocropped with Brassica parachinensis and Zea mays. J Hazard Mater 167:170–178
Pietrini F, Zacchini M, Iori V, Pietrosanti L, Bianconi D, Massacci A (2009) Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Int J Phytoremediat 12:105–120
Lasat MM (2002) Phytoextraction of toxic metals. J Environ Qual 31:109
Sanaei S, Sadeghinia M, Meftahizade H, Ardakani AF, Ghorbanpour M (2022) Cadmium and lead differentially affect growth, physiology, and metal accumulation in guar (Cyamopsis tetragonoloba L.) genotypes. Environ Sci Pollut R 29:4180–4192
Hussain A, Ali S, Rizwan M, Zia Ur Rehman M, Javed MR, Imran M, Chatha SAS, Nazir R (2018) Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environ Pollut 242:1518–1526
Yadav AN, Kumar V, Dhaliwal HS, Prasad R, Saxena AK (2018) Microbiome in crops: diversity, distribution, and potential role in crop improvement. Crop Improvement Through Microbial Biotechnol. https://doi.org/10.1016/B978-0-444-63987-5.00015-3
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Son J, Sumayo M, Hwang Y, Kim B, Ghim S (2014) Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl Soil Ecol 73:1–8
De Marco P (2004) Novel pollutant-resistant methylotrophic bacteria for use in bioremediation. FEMS Microbiol Lett 234:75–80
Souza RD, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419
Hu J, Wu S, Wu F, Leung HM, Lin X, Wong MH (2013) Arbuscular mycorrhizal fungi enhance both absorption and stabilization of Cd by Alfred stonecrop (Sedum alfredii Hance) and perennial ryegrass (Lolium perenne L.) in a Cd-contaminated acidic soil. Chemosphere 93:1359–1365
Andrade SAL, Silveira APD, Mazzafera P (2010) Arbuscular mycorrhiza alters metal uptake and the physiological response of Coffea arabica seedlings to increasing Zn and Cu concentrations in soil. Sci Total Environ 408:5381–5391
You Y, Ju C, Wang L, Wang X, Ma F, Wang G, Wang Y (2022) The mechanism of arbuscular mycorrhizal enhancing cadmium uptake in Phragmites australis depends on the phosphorus concentration. J Hazard Mater 440:129800
Han H, Zhang H, Qin S, Zhang J, Yao L, Chen Z, Yang J (2021) Mechanisms of Enterobacter bugandensis TJ6 immobilization of heavy metals and inhibition of Cd and Pb uptake by wheat based on metabolomics and proteomics. Chemosphere 276:130157
Tang F, Yue J, Tian J, Ge F, Li F, Liu Y, Deng S, Zhang D (2022) Microbial induced phosphate precipitation accelerate lead mineralization to alleviate nucleotide metabolism inhibition and alter Penicillium oxalicum’s adaptive cellular machinery. J Hazard Mater 439:129675
Patel D, Patel A, Patel M, Goswami D (2021) Talaromyces pinophilus strain M13: a portrayal of novel groundbreaking fungal strain for phytointensification. Environ Sci Pollut Res Int 28:8758–8769
Pietrini F, Iori V, Bianconi D, Mughini G, Massacci A, Zacchini M (2015) Assessment of physiological and biochemical responses, metal tolerance and accumulation in two eucalypt hybrid clones for phytoremediation of cadmium-contaminated waters. J Environ Manage 162:221–231
Jiang H, Zhao X, Fang J, **ao Y (2018) Physiological responses and metal uptake of Miscanthus under cadmium/arsenic stress. E Environ Sci Pollut R 25:28275–28284
Khanna K, Kohli SK, Sharma A, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Ahmad P (2019) Histochemical and physicochemical studies reveal improved defense in tomato under Cd stress with rhizobacterial supplementation. Plant Soil 446:393–411
Ali B, Wang X, Saleem MH, Sumaira HA, Afridi MS, Khan S, Zaib-Un-Nisa UI, Amaral JA, Alatawi A, Ali S (2022) PGPR-mediated salt tolerance in maize by modulating plant physiology, antioxidant defense, compatible solutes accumulation and bio-surfactant producing genes. Plants (Basel). https://doi.org/10.3390/plants11030345
Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057
Mitra S, Purkait T, Pramanik K, Maiti TK, Dey RS (2019) Three-dimensional graphene for electrochemical detection of Cadmium in Klebsiella michiganensis to study the influence of Cadmium uptake in rice plant. Mat Sci Eng C 103:109802
François CJ, Batinovic S, Petrovski S, Gendall AR (2021) Draft genome sequence of Enterobacter asburiae NCR1, a plant growth-promoting rhizobacterium isolated from a cadmium-contaminated environment. Microbiol Resour Ann. https://doi.org/10.1128/MRA.00478-21
Sudová R, Vosátka M (2007) Differences in the effects of three arbuscular mycorrhizal fungal strains on P and Pb accumulation by maize plants. Plant Soil 296:77–83
Yang G, Zheng M, Tan A, Liu Y, Feng D, Lv S (2021) Research on the mechanisms of plant enrichment and detoxification of cadmium. Biology 10:544
Dubey S, Shri M, Gupta A, Rani V, Chakrabarty D (2018) Toxicity and detoxification of heavy metals during plant growth and metabolism. Environ Chem Lett 16:1169–1192
Velivelli SLS, Sessitsch A, Prestwich BD (2014) The Role of microbial inoculants in integrated crop management systems. Potato Res 57:291–309
Liu N, Liu Q, Min J, Zhang S, Li S, Chen Y, Dai J (2022) Specific bacterial communities in the rhizosphere of low-cadmium and high-zinc wheat (Triticum aestivum L.). Sci Total Environ 838:156484
Chi Y, You Y, Wang J, Chen X, Chu S, Wang R, Zhang X, Yin S, Zhang D, Zhou P (2022) Two plant growth-promoting bacterial Bacillus strains possess different mechanisms in affecting cadmium uptake and detoxification of Solanum nigrum L. Chemosphere 305:135488
Ajmal AW, Yasmin H, Hassan MN, Khan N, Jan BL, Mumtaz S (2022) Heavy metal–resistant plant growth–promoting citrobacter werkmanii strain WWN1 and enterobacter cloacae strain JWM6 enhance wheat (Triticum aestivum L.) growth by modulating physiological attributes and some key antioxidants under multi-metal stress. Front Microbiol. https://doi.org/10.3389/fmicb.2022.815704
Han H, Wu X, Bolan N, Kirkham MB, Yang J, Chen Z (2022) Inhibition of cadmium uptake by wheat with urease-producing bacteria combined with sheep manure under field conditions. Chemosphere 293:133534
Teng Z, Shao W, Zhang K, Huo Y, Li M (2019) Characterization of phosphate solubilizing bacteria isolated from heavy metal contaminated soils and their potential for lead immobilization. J Environ Manage 231:189–197
Sang MK, Kim KD (2014) Biocontrol activity and root colonization by Pseudomonas corrugata strains CCR04 and CCR80 against phytophthora blight of pepper. Biocontrol 59:437–448
Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Bioch 60:53–58
Kumari D, Pan X, Lee D, Achal V (2014) Immobilization of cadmium in soil by microbially induced carbonate precipitation with Exiguobacterium undae at low temperature. Int Biodeter Biodegr 94:98–102
Złoch M, Thiem D, Gadzała-Kopciuch R, Hrynkiewicz K (2016) Synthesis of siderophores by plant-associated metallotolerant bacteria under exposure to Cd2+. Chemosphere 156:312–325
Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019) Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotox Environ Safe 167:218–226
Liu S, Yang B, Liang Y, **ao Y, Fang J (2020) Prospect of phytoremediation combined with other approaches for remediation of heavy metal-polluted soils. Environ Sci Pollut R 27:16069–16085
Tirry N, Tahri Joutey N, Sayel H, Kouchou A, Bahafid W, Asri M, El Ghachtouli N (2018) Screening of plant growth promoting traits in heavy metals resistant bacteria: prospects in phytoremediation. J Genet Engin Biotech 16:613–619
**ao Y, Liu H, Chen R, Liu S, Hao X, Fang J (2022) Heteroauxin-producing bacteria enhance the plant growth and lead uptake of Miscanthus floridulus (Lab.). Int J Phytoremediat 24:1205–1212
Pan W, Lu Q, Xu Q, Zhang R, Li H, Yang Y, Liu H, Du S (2019) Abscisic acid-generating bacteria can reduce Cd concentration in pakchoi grown in Cd-contaminated soil. Ecotox Environ Safe 177:100–107
Liu S, Liu H, Chen R, Ma Y, Yang B, Chen Z, Liang Y, Fang J, **ao Y (2021) Role of two plant growth-promoting bacteria in remediating cadmium-contaminated soil combined with Miscanthus floridulus (Lab.). Plants 10:912
Sarabia M, Cornejo P, Azcón R, Carreón-Abud Y, Larsen J (2017) Mineral phosphorus fertilization modulates interactions between maize, rhizosphere yeasts and arbuscular mycorrhizal fungi. Rhizosphere 4:89–93
Alori ET, Babalola OO (2018) Microbial inoculants for improving crop quality and human gealth in Africa. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02213
Wang L, Huang X, Ma F, Ho S, Wu J, Zhu S (2017) Role of Rhizophagus irregularis in alleviating cadmium toxicity via improving the growth, micro- and macroelements uptake in Phragmites australis. Environ Sci Pollut R 24:3593–3607
Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2016) Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Appl Soil Ecol 101:57–63
Adelusi OA, Gbashi S, Adebiyi JA et al (2022) Variability in metabolites produced by Talaromyces pinophilus SPJ22 cultured on different substrates. Fungal Biol Biotechnol 9(1):15
Abdel-Rahim IR, Abo-Elyousr KA (2018) Talaromyces pinophilus strain AUN-1 as a novel mycoparasite of Botrytis cinerea, the pathogen of onion scape and umbel blights. Microbiol Res 212:1–9
Acknowledgements
This project was carried out with great support from Professor Langtao **ao and Chao Huang’s research Lab. The study was supported by the National Natural Science Foundation of China (No. 41807135), the Scientific Research Fund of Hunan Provincial Education Department (No. 21A0142, 20A233, 18B107), and the Natural Science Foundation of Hunan province, China (No. 2019JJ50220).
Author information
Authors and Affiliations
Contributions
YX, JF, and LJ contributed to the study’s conception and design. Research, material preparation, data collection, and analysis were performed by RC, LC, and YX. The first draft of the manuscript was written by RC, and YX and BY commented on previous versions of the manuscript. All aforementioned authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
**ao, Y., Chen, R., Chen, L. et al. Endophytic Fungus Talaromyces sp. MR1 Promotes the Growth and Cadmium Uptake of Arabidopsis thaliana L. Under Cadmium Stress. Curr Microbiol 80, 346 (2023). https://doi.org/10.1007/s00284-023-03453-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-023-03453-3