The Effect of Endophytic Talaromyces pinophilus on Growth, Absorption and Accumulation of Heavy Metals of Triticum aestivum Grown on Sandy Soil Amended by Sewage Sludge
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Isolation and Identification
2.2. Morphological Identification of the Fungal Isolate
2.3. Molecular Identification
2.4. Fungal Inoculum Preparation
2.5. Extraction and Determination of Phytohormones
2.6. Plant Material and Growth Conditions
2.7. Determination of Growth Parameters
2.8. Determination of Photosynthetic Pigments
2.9. Determination of Organic Solutes
2.10. Antioxidant Enzymes Activity
2.11. Determination of Mineral Ions and Heavy Metals
2.12. Determination of the Bioconcentration Factor (BCF) and Translocation Factor (TF)
2.13. Statistical Analysis
3. Results
3.1. Isolation and Morphological Identification of the Fungal Isolate
3.2. Nucleotide Sequence Accession Number and Phylogenetic Analysis
3.3. Phytohormones
3.4. Water Content (WC) and Growth of T. aestivum Plants Grown on Different Sewage Sludge Levels and Phytoremediation by T. pinophilus
3.5. Photosynthetic Pigments of T. aestivum Plants Grown on Different Sewage Sludge Levels and Phytoremediation by T. pinophilus
3.6. Osmolytes of T. aestivum Plants Grown on Different Sludge Levels and Phytoremediation by T. pinophilus
3.7. Antioxidant Enzymes of T. aestivum Plants Grown on Different Sludge Levels and Phytoremediation by T. pinophilus
3.8. Translocation and Content of Minerals in Wheat Plant Cations
3.9. Effects of Sewage Sludge and T. pinophilus on Growth Media
3.10. The Content and Distribution of Heavy Metals in T. aestivum
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Fadiji, A.E.; Babalola, O.O. Elucidating Mechanisms of Endophytes Used in Plant Protection and Other Bioactivities With Multifunctional Prospects. Front. Bioeng. Biotechnol. 2020, 8, 467. Available online: www.frontiersin.org (accessed on 15 May 2020). [CrossRef]
- Abbas, A.M.; Abd-Elmabod, S.K.; El-Ashry, S.M.; Soliman, W.S.; El-Tayeh, N.; Castillo, J.M. Capability of the Invasive Tree Prosopis glandulosa Torr. To Remediate Soil Treated with Sewage Sludge. Sustainability 2019, 11, 2711. [Google Scholar] [CrossRef] [Green Version]
- Khan, S.A.; Hamayun, M.; Khan, A.L.; Lee, I.J.; Shinwari, Z.K.; Kim, J. Isolation of plant growth promotic fungi from dicots inhabiting coastal sand dunes of Korea. J. Bot. 2012, 44, 1453–1460. [Google Scholar]
- Tumangger, B.S.; Nadilla, F.; Baiduri, N.; Mardina, F.V. In vitro Screening of Endophytic Fungi Associated with Mangroveas Biofertilizer on the Growth of Black Rice (Oryza sativaL. Cempo Ireng). In Proceedings of the 2nd Nommensen International Conference on Technology and Engineering IOP Publishing Materials Science and Engineering, Medan, Indonesia, 19–20 July 2018; ISBN 420012080. [Google Scholar] [CrossRef]
- Rigobelo, E.C.; Noemi Carla Baron, N.C. Endophytic fungi: A tool for plant growth promotion and sustainable agriculture. Mycology 2021, 1–17. [Google Scholar] [CrossRef]
- Ma, Y.; Prasad, M.N.V.; Rajkumar, M.; Freitas, H. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol. Adv. 2011, 29, 248–258. [Google Scholar] [CrossRef]
- Pendergrass, A.; Butcher, D.J. Uptake of lead and arsenic in food plants grown in contaminated soil from Barber Orchard, NC. Microchem. J. 2006, 83, 14–16. [Google Scholar] [CrossRef]
- Baker, A.J.M.; Reeves, R.D.; McGrath, S.P. In Situ Decontamination of Heavy Metal Polluted Soils Using Crops of Metal-Accumulating Plants—A Feasibility Study. In Situ Bioreclam. 1991, 7, 600–605. [Google Scholar]
- Greipsson, S. Phytoremediation. Nat. Educ. Knowl. 2011, 3, 7. [Google Scholar]
- Rajkumar, M.; Ae, N.; Prasad, M.N.V.; Freitas, H. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 2010, 28, 142–149. [Google Scholar] [CrossRef]
- Gerhardt, K.E.; Huang, X.D.; Glick, B.R.; Greenberg, B.M. Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challenges. Plant Sci. 2009, 176, 20–30. [Google Scholar] [CrossRef]
- Glick, B.R. Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 2010, 28, 367–374. [Google Scholar] [CrossRef] [PubMed]
- Rajkumar, M.; Sandhya, S.; Prasad, M.N.; Freitas, H. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 2012, 30, 1562–1574. [Google Scholar] [CrossRef] [PubMed]
- Li, H.Y.; Li, D.W.; He, C.M.; Zhou, Z.P.; Mei, T.; Xu, H.M. Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb-Zn mine wasteland in China. Fungal Ecol. 2012, 5, 309–315. [Google Scholar] [CrossRef]
- Li, H.Y.; Shen, M.; Zhou, Z.P.; Li, T.; Wei, Y.L.; Lin, L.B. Diversity and cold adaptation of endophytic fungi from five dominant plant species collected from the Baima Snow Mountain, Southwest China. Fungal Divers. 2012, 54, 79–86. [Google Scholar] [CrossRef]
- Ren, A.Z.; Li, C.A.; Gao, Y.B. Endophytic fungus improves growth and metal uptake of Lolium Arundinaceum Darbyshire ex. Schreb. Int. J. Phytoremed. 2011, 13, 233–243. [Google Scholar] [CrossRef] [PubMed]
- Shahabivand, S.; Maivan, H.Z.; Goltapeh, E.M.; Sharifi, M.; Aliloo, A.A. The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol. Biochem. 2012, 60, 53–58. [Google Scholar] [CrossRef]
- Khan, A.L.; Lee, I.J. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol. 2013, 13, 86. [Google Scholar] [CrossRef] [Green Version]
- AbouAlhamed, M.F.; Shebany, Y.M. Endophytic Chaetomium globosum enhances maize seedling copper stress tolerance. Plant Biol. 2012, 14, 859–863. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Hafez, S.I.I.; Abo-Elyousr, K.A.; Abdel-Rahim, I.R. Leaf surface and en- dophytic fungi associated with onion leaves and their antagonistic activity against Alternaria porri. Czech Mycol. 2015, 67, 1–22. [Google Scholar] [CrossRef] [Green Version]
- Zhao, W.T.; Shi, X.; ** sites. Bioresour. Technol. 2007, 98, 1788–1794. [Google Scholar] [CrossRef] [PubMed]
- Dussault, M.; Bécaert, V.; François, M.; Sauvé, S.; Deschênes, L. Effect of copper on soil functional stability measured by relative soil stability index (RSSI) based on two enzyme activities. Chemosphere 2008, 72, 755–762. [Google Scholar] [CrossRef]
- Cerqueira, B.; Vega, F.A.; Silva, L.F.O.; Andrade, L. Effects of vegetation on chemical and mineralogical characteristics of soils developed on a decantation bank from a copper mine. Sci. Total Environ. 2012, 421, 220–229. [Google Scholar] [CrossRef]
- Arenas-Lago, D.; Vega, F.A.; Silva, L.F.O.; Andrade, M.L. Soil interaction and fractionation of added cadmium in some Galician soils. Microchem. J. 2013, 110, 681–690. [Google Scholar] [CrossRef]
- Yang, X.E.; Li, T.Q.; Yang, J.C.; He, Z.L.; Lu, L.L.; Meng, F.H. Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfrediiHance. Planta 2006, 224, 185–195. [Google Scholar] [CrossRef] [PubMed]
- Brallier, S.; Harrison, R.B.; Henry, C.L.; Dongsen, X. Liming effects on availability of Cd, Cu, Ni, and Zn in a soil amended with sewage sludge 16 years previously. Water Air Soil Pollut. 1996, 86, 195–206. [Google Scholar] [CrossRef]
- Sloan, J.J.; Dowdy, R.H.; Dolan, M.S.; Linden, D.R. Long-term effects of biosolids applications on heavy metal bioavailability in agriculture soils. J. Environ. Qual. 1997, 26, 966–974. [Google Scholar] [CrossRef]
- Usman, A.R.A.; Kuzyakov, Y.; Stahr, K. Dynamic of organic C mineralization and the mobile fraction of heavy metals in a calcareous soil incubated with organic wastes. Water Air Soil Pollut. 2004, 158, 401–418. [Google Scholar] [CrossRef] [Green Version]
- Temminghoff, E.J.M.; van der Zee, S.E.A.T.M.; De Haan, F.A.M. Effects of dissolved organic matter on the mobility of copper in a contaminated sandy soil. Eur. J. Soil Sci. 1998, 49, 617–628. [Google Scholar] [CrossRef]
- Codex Alimentarius Commission (FAO/WHO). Food Additives and Contaminants-Joint; FAO/WHO: Rome, Italy, 2001; pp. 1–289. [Google Scholar]
- WHO. Permissible Limits of Heavy Metals in Soil and Plants; WHO: Geneva, Switzerland, 1996. [Google Scholar]
- Herman, D.; Artiola, J.; Miller, R. Removal of cadmium, lead and zinc from soil by a rhamnolipid biosurfactant. Environ. Sci. Technol. 1995, 29, 2280–2285. [Google Scholar] [CrossRef] [PubMed]
- Dubbin, W.E.; Louise Ander, E. Influence of microbial hydroxamate siderophores on Pb(II) desorption from α-FeOOH. Appl. Geol. Chem. 2003, 18, 1751–1756. [Google Scholar] [CrossRef]
- Di Simine, C.D.; Sayer, J.A.; Gadd, G.M. Solubilization of zinc phosphate by a strain of Pseudomonas fluorescence isolated from a forest soil. Biol. Fertil. Soils 1998, 28, 87–94. [Google Scholar] [CrossRef]
- Zhuang, X.; Chen, J.; Shim, H.; Bai, Z. New advances in plant growth promoting rhizobacteria for bioremediation. Environ. Int. 2007, 33, 406–413. [Google Scholar] [CrossRef]
- Khan, A.G. Mycorrhizoremediation—An enhanced from of phytoremediation. J. Zhejiang Univ. Sci. B 2007, 7, 503–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lebeau, T.; Braud, A.; Jezeguel, K. Performance of augmentation assisted phytoextraction applied to metal contaminated soils: A review. Environ. Pollut. 2000, 153, 497–522. Available online: www.aseanenenvironment.info/abstract/41016970.pdf (accessed on 2 November 2021). [CrossRef]
No | Treatments | Treatments Abbreviations |
---|---|---|
1 | Sandy soil without sewage sludge and without endophytic fungus (100% sandy soil) | T1 |
2 | 75% soil + 25% sewage sludge | T2 |
3 | 50% soil +50% sewage sludge | T3 |
4 | 25% soil + 75% sewage sludge | T4 |
5 | 100% sandy soil + endophytic fungus as mentioned in Fungal Inoculum Preparation | T5 |
6 | 75% soil + 25% sewage sludge + endophytic fungus | T6 |
7 | 50% soil + 50% sewage sludge + endophytic fungus | T7 |
8 | 25% soil + 75% sewage sludge + endophytic fungus | T8 |
No | Morphospecies | Strian | Sequence (bp) | Host | Location | GenBank Accessions |
---|---|---|---|---|---|---|
1 | Talaromyces pinophilus | SVU3:83523 | 574 | Rosmarinus officinalis | Egypt | MW695526 |
2 | Talaromyces pinophilus | Y. H. Yeh I0609 | 595 | Ipomoea | Taiwan | MK336445 |
3 | Penicillium pinophilus | FKI-3864 | 596 | - | Japan | AB455516 |
4 | Talaromyces pinophilus | 17F4103 | 600 | - | Japan | MT093464 |
5 | Talaromyces pinophilus | Y. H. Yeh I0520 | 584 | Ipomoea | Taiwan | MK336630 |
6 | Talaromyces pinophilus | C.W. Hsieh CHD152 | 591 | Platostomapalustre | Taiwan | MH777072 |
7 | Talaromyces pinophilus | 1–95 | 6,009,755 | - | China | CP017345 |
Treatment | Gibberellic Acid (μg mL−1) | Abscisic Acid (μg mL−1) |
---|---|---|
T1 | 4.11 | 3.05 |
T2 | 0.41 | 0.09 |
T3 | 2.11 | 2.19 |
T4 | 0.00 | 0.00 |
T5 | 2.00 | 5.14 |
T6 | 5.36 | 0.00 |
T7 | 2.78 | 0.00 |
T8 | 5.22 | 7.13 |
Treatments | T1 | T2 | T3 | T4 | T5 | T6 | T7 | T8 | |
---|---|---|---|---|---|---|---|---|---|
pH | Before | 8.15 f,* | 7.82 e | 7.57 d * | 7.56 d,* | 7.28 c | 6.86 b | 6.92 b | 6.46 a |
After | 7.97 d | 7.63 c | 7.08 b | 6.91 ab | 6.72 a | 6.75 ab | 6.93 ab | 6.69 a | |
OM (%) | Before | 2.73 a,* | 3.60 a * | 6.53 b,* | 8.44 c,* | 3.76 a,* | 5.74 b,* | 16.16 d,* | 22.52 e,* |
After | 2.07 a | 2.87 b | 4.97 d | 6.18 f | 2.68 ab | 3.85 c | 12.72 g | 17.23 h | |
Na (mg g−1) | Before | 1.73 a | 2.08 a | 3.54 b | 4.94 c | 1.05 a | 3.32 b,* | 9.58 e,* | 6.37 d,* |
After | 1.16 a | 2.16 b | 3.07 c | 4.34 d | 0.84 a | 3.41 c | 6.65 e | 8.99 f | |
K (mg g−1) | Before | 3.63 a | 6.04 b,* | 7.99 c,* | 9.52 d,* | 6.09 b,* | 10.14 d | 15.27 e | 25.29 f,* |
After | 2.92 a | 4.85 b | 6.26 c | 7.13 cd | 3.59 ab | 8.28 d | 15.00 e | 19.23 f | |
Ca (mg g−1) | Before | 7.12 a,* | 10.39 b,* | 14.38 c | 16.95 d,* | 13.10 c,* | 18.29 d,* | 20.80 e,* | 28.86 f,* |
After | 4.96 a | 8.31 b | 10.63 d | 12.95 e | 9.65 c | 11.01 d | 16.01 f | 19.73 g | |
Mg (mg g−1) | Before | 3.05 a,* | 4.09 b | 7.04 d | 8.74 e,* | 5.88 c | 9.75 f | 15.79 g,* | 19.24 h,* |
After | 1.50 a | 3.20 ab | 4.74 b | 6.95 c | 4.20 b | 7.37 c | 10.13 d | 13.93 e | |
Cd (µg g−1) | Before | 0.30 b | 0.58 c | 0.79 e | 1.00 f | 0.22 a,* | 0.32 b,* | 0.55 c,* | 0.70 d,* |
After | 0.23 a | 0.53 b | 0.71 c | 0.93 d | 0.19 a | 0.24 a | 0.48 b | 0.55 b | |
Cu (µg g−1) | Before | 10.44 d,* | 12.49 e,* | 18.94 f,* | 20.94 g,* | 4.90 a,* | 5.86 ab,* | 6.69 b,* | 9.05 c,* |
After | 7.34 d | 10.27 e | 14.37 f | 15.18 f | 2.25 a | 3.57b | 5.05 c | 6.79 d | |
Zn (µg g−1) | Before | 40.91 d,* | 45.44 f,* | 55.50 g,* | 77.21 h,* | 22.01 b,* | 20.19 a,* | 32.63 c,* | 43.92 e,* |
After | 31.79 c | 29.78 c | 49.63 e | 70.49 f | 16.32 a | 14.17 a | 23.06b | 34.03d | |
Ni (µg g−1) | Before | 26.85 d,* | 32.31 e,* | 43.23 f,* | 61.95 g,* | 13.54 a,* | 16.71 b,* | 20.72 c,* | 25.84 d,* |
After | 21.78 d | 27.72 e | 36.12 f | 50.27 g | 10.78 a | 13.48 b | 16.62 c | 20.38 d |
Zn | Cd | Ni | Cu | |
---|---|---|---|---|
Bioconcentration factor (BCF) | ||||
T1 | 0.958 | 0.689 | 0.363 | 0.435 |
T2 | 1.410 | 0.790 | 0.424 | 0.633 |
T3 | 1.289 | 0.832 | 0.391 | 0.497 |
T4 | 1.438 | 0.804 | 0.334 | 0.527 |
T5 | 2.111 | 0.769 | 0.690 | 0.869 |
T6 | 2.613 | 1.116 | 0.714 | 0.889 |
T7 | 1.892 | 0.813 | 0.641 | 0.939 |
T8 | 1.861 | 0.670 | 0.489 | 0.531 |
Translocation factor (TF) | ||||
T1 | 0.264 | 0.752 | 1.022 | 0.536 |
T2 | 0.613 | 0.768 | 0.660 | 0.886 |
T3 | 0.683 | 0.720 | 0.832 | 1.081 |
T4 | 0.755 | 0.953 | 0.722 | 0.528 |
T5 | 0.597 | 0.895 | 1.015 | 0.464 |
T6 | 0.729 | 0.501 | 0.643 | 0.708 |
T7 | 0.524 | 0.894 | 0.729 | 0.918 |
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El-Shahir, A.A.; El-Tayeh, N.A.; Ali, O.M.; Abdel Latef, A.A.H.; Loutfy, N. The Effect of Endophytic Talaromyces pinophilus on Growth, Absorption and Accumulation of Heavy Metals of Triticum aestivum Grown on Sandy Soil Amended by Sewage Sludge. Plants 2021, 10, 2659. https://doi.org/10.3390/plants10122659
El-Shahir AA, El-Tayeh NA, Ali OM, Abdel Latef AAH, Loutfy N. The Effect of Endophytic Talaromyces pinophilus on Growth, Absorption and Accumulation of Heavy Metals of Triticum aestivum Grown on Sandy Soil Amended by Sewage Sludge. Plants. 2021; 10(12):2659. https://doi.org/10.3390/plants10122659
Chicago/Turabian StyleEl-Shahir, Amany A., Noha A. El-Tayeh, Omar M. Ali, Arafat Abdel Hamed Abdel Latef, and Naglaa Loutfy. 2021. "The Effect of Endophytic Talaromyces pinophilus on Growth, Absorption and Accumulation of Heavy Metals of Triticum aestivum Grown on Sandy Soil Amended by Sewage Sludge" Plants 10, no. 12: 2659. https://doi.org/10.3390/plants10122659