A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system

The hydroponic farming significantly enhances the yield and enables multiple cropping per year. These advantages can be improved by using plant growth-promoting fungi (PGPF) either under normal or stress conditions. In this study, the fungal strain (A3) isolated from the rhizosphere of the halophyte...

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Main Authors: Mohamed Tarroum, Walid Ben Romdhane, Fahad Al-Qurainy, Ahmed Abdelrahim Mohamed Ali, Abdullah Al-Doss, Lotfi Fki, Afif Hassairi
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.996054/full
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author Mohamed Tarroum
Walid Ben Romdhane
Fahad Al-Qurainy
Ahmed Abdelrahim Mohamed Ali
Abdullah Al-Doss
Lotfi Fki
Afif Hassairi
Afif Hassairi
author_facet Mohamed Tarroum
Walid Ben Romdhane
Fahad Al-Qurainy
Ahmed Abdelrahim Mohamed Ali
Abdullah Al-Doss
Lotfi Fki
Afif Hassairi
Afif Hassairi
author_sort Mohamed Tarroum
collection DOAJ
description The hydroponic farming significantly enhances the yield and enables multiple cropping per year. These advantages can be improved by using plant growth-promoting fungi (PGPF) either under normal or stress conditions. In this study, the fungal strain (A3) isolated from the rhizosphere of the halophyte plant Aeluropus littoralis was identified as Penicillium olsonii based on sequence homology of its ITS region. The A3 fungus was shown to be halotolerant (up to 1 M NaCl) and its optimal growth was at 27°C, but inhibited at 40°C. In liquid culture medium, the A3 produced indole acetic acid (IAA) especially in the presence of L-tryptophan. Tobacco plants grown under hydroponic farming system were used to evaluate the promoting activity of the direct effect of A3 mycelium (DE) and the indirect effect (IDE) of its cell-free culture filtrate (A3CFF). The results showed that for the two conditions (DE or IDE) the tobacco seedlings exhibited significant increase in their height, leaf area, dry weight, and total chlorophyll content. Interestingly, the A3CFF (added to the MS liquid medium or to nutrient solution (NS), prepared from commercial fertilizers) induced significantly the growth parameters, the proline concentration, the catalase (CAT) and the superoxide dismutase (SOD) activities of tobacco plants. The A3CFF maintained its activity even after extended storage at 4°C for 1 year. Since the A3 is a halotolerant fungus, we tested its ability to alleviate salt stress effects. Indeed, when added at 1:50 dilution factor to NS in the presence of 250 mM NaCl, the A3CFF enhanced the plant salt tolerance by increasing the levels of total chlorophyll, proline, CAT, and SOD activities. In addition, the treated plants accumulated less Na+ in their roots but more K+ in their leaves. The A3CFF was also found to induce the expression of five salt stress related genes (NtSOS1, NtNHX1, NtHKT1, NtSOD, and NtCAT1). Finally, we proved that the A3CFF can reduce by half the chemical fertilizers inputs. Indeed, the tobacco plants grown in a hydroponic system using 0.5xNS supplemented with A3CFF (1:50) exhibited significantly higher growth than those grown in 0.5xNS or 1xNS. In an attempt to explain this mechanism, the expression profile of some growth related genes (nitrogen metabolism (NR1, NRT1), auxin (TRYP1, YUCCA6-like), and brassinosteroid (DET2, DWF4) biosynthesis) was performed. The results showed that all these genes were up-regulated following plant treatment with A3CFF. In summary the results revealed that the halotolerant fungus P. olsonii can stimulates tobacco plant growth, enhances its salt tolerance, and reduces by half the required chemical fertilizer inputs in a hydroponic farming system.
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spelling doaj.art-c975c7e64fc945f4822b081a80031ac62022-12-22T02:41:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-10-011310.3389/fmicb.2022.996054996054A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic systemMohamed Tarroum0Walid Ben Romdhane1Fahad Al-Qurainy2Ahmed Abdelrahim Mohamed Ali3Abdullah Al-Doss4Lotfi Fki5Afif Hassairi6Afif Hassairi7Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi ArabiaDepartment of Plant Production, College of Food and Agricultural Science, King Saud University, Riyadh, Saudi ArabiaDepartment of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi ArabiaDepartment of Plant Production, College of Food and Agricultural Science, King Saud University, Riyadh, Saudi ArabiaDepartment of Plant Production, College of Food and Agricultural Science, King Saud University, Riyadh, Saudi ArabiaLaboratory of Plant Biotechnology Applied to Crop Improvement, Faculty of Sciences of Sfax, University of Sfax, Sfax, TunisiaDepartment of Plant Production, College of Food and Agricultural Science, King Saud University, Riyadh, Saudi ArabiaCentre of Biotechnology of Sfax, University of Sfax, Sfax, TunisiaThe hydroponic farming significantly enhances the yield and enables multiple cropping per year. These advantages can be improved by using plant growth-promoting fungi (PGPF) either under normal or stress conditions. In this study, the fungal strain (A3) isolated from the rhizosphere of the halophyte plant Aeluropus littoralis was identified as Penicillium olsonii based on sequence homology of its ITS region. The A3 fungus was shown to be halotolerant (up to 1 M NaCl) and its optimal growth was at 27°C, but inhibited at 40°C. In liquid culture medium, the A3 produced indole acetic acid (IAA) especially in the presence of L-tryptophan. Tobacco plants grown under hydroponic farming system were used to evaluate the promoting activity of the direct effect of A3 mycelium (DE) and the indirect effect (IDE) of its cell-free culture filtrate (A3CFF). The results showed that for the two conditions (DE or IDE) the tobacco seedlings exhibited significant increase in their height, leaf area, dry weight, and total chlorophyll content. Interestingly, the A3CFF (added to the MS liquid medium or to nutrient solution (NS), prepared from commercial fertilizers) induced significantly the growth parameters, the proline concentration, the catalase (CAT) and the superoxide dismutase (SOD) activities of tobacco plants. The A3CFF maintained its activity even after extended storage at 4°C for 1 year. Since the A3 is a halotolerant fungus, we tested its ability to alleviate salt stress effects. Indeed, when added at 1:50 dilution factor to NS in the presence of 250 mM NaCl, the A3CFF enhanced the plant salt tolerance by increasing the levels of total chlorophyll, proline, CAT, and SOD activities. In addition, the treated plants accumulated less Na+ in their roots but more K+ in their leaves. The A3CFF was also found to induce the expression of five salt stress related genes (NtSOS1, NtNHX1, NtHKT1, NtSOD, and NtCAT1). Finally, we proved that the A3CFF can reduce by half the chemical fertilizers inputs. Indeed, the tobacco plants grown in a hydroponic system using 0.5xNS supplemented with A3CFF (1:50) exhibited significantly higher growth than those grown in 0.5xNS or 1xNS. In an attempt to explain this mechanism, the expression profile of some growth related genes (nitrogen metabolism (NR1, NRT1), auxin (TRYP1, YUCCA6-like), and brassinosteroid (DET2, DWF4) biosynthesis) was performed. The results showed that all these genes were up-regulated following plant treatment with A3CFF. In summary the results revealed that the halotolerant fungus P. olsonii can stimulates tobacco plant growth, enhances its salt tolerance, and reduces by half the required chemical fertilizer inputs in a hydroponic farming system.https://www.frontiersin.org/articles/10.3389/fmicb.2022.996054/fullPenicillium olsoniihalophilic PGPFcell-free culture filtratesalt stressplant growth promotionsustainable agriculture
spellingShingle Mohamed Tarroum
Walid Ben Romdhane
Fahad Al-Qurainy
Ahmed Abdelrahim Mohamed Ali
Abdullah Al-Doss
Lotfi Fki
Afif Hassairi
Afif Hassairi
A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
Frontiers in Microbiology
Penicillium olsonii
halophilic PGPF
cell-free culture filtrate
salt stress
plant growth promotion
sustainable agriculture
title A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
title_full A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
title_fullStr A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
title_full_unstemmed A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
title_short A novel PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis promotes plant growth, enhances salt stress tolerance, and reduces chemical fertilizers inputs in hydroponic system
title_sort novel pgpf penicillium olsonii isolated from the rhizosphere of aeluropus littoralis promotes plant growth enhances salt stress tolerance and reduces chemical fertilizers inputs in hydroponic system
topic Penicillium olsonii
halophilic PGPF
cell-free culture filtrate
salt stress
plant growth promotion
sustainable agriculture
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.996054/full
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